Next Article in Journal
Inhibition of Class I Histone Deacetylase Activity Blocks the Induction of TNFAIP3 Both Directly and Indirectly via the Suppression of Endogenous TNF-α
Next Article in Special Issue
Antibiofilm Properties of Antiseptic Agents Used on Pseudomonas aeruginosa Isolated from Diabetic Foot Ulcers
Previous Article in Journal
Next-Generation Sequencing of Local Romanian Tomato Varieties and Bioinformatics Analysis of the Ve Locus
 
 
Search for Articles:
Title / Keyword
Author / Affiliation / Email
Journal
Article Type
 
 
Advanced Search
 
Section
Special Issue
Volume
Issue
Number
Page
 
Journals
IJMS
Volume 23
Issue 17
10.3390/ijms23179751
ijms-logo
Submit to this Journal Review for this Journal Propose a Special Issue
► Article Menu

Article Menu

share Share announcement Help format_quote Cite question_answer Discuss in SciProfiles thumb_up
...
Endorse textsms
...
Comment
first_page
settings
Order Article Reprints
Font Type:
Arial Georgia Verdana
Font Size:
Aa Aa Aa
Line Spacing:
Column Width:
Background:
Review

Exploring the Function of Quorum Sensing Regulated Biofilms in Biological Wastewater Treatment: A Review

by
Sania Sahreen
1,
Hamid Mukhtar
1,*,
Kálmán Imre
2,*,
Adriana Morar
2,
Viorel Herman
3 and
Sundas Sharif
1
1
Institute of Industrial Biotechnology, Government College University, Lahore 54000, Pakistan
2
Department of Animal Production and Veterinary Public Health, Faculty of Veterinary Medicine, Banat’s University of Agricultural Sciences and Veterinary Medicine “King Michael I of Romania”, 300645 Timisoara, Romania
3
Department of Infectious Diseases and Preventive Medicine, Faculty of Veterinary Medicine, Banat’s University of Agricultural Sciences and Veterinary Medicine “King Michael I of Romania”, 300645 Timisoara, Romania
*
Authors to whom correspondence should be addressed.
Int. J. Mol. Sci. 2022, 23(17), 9751; https://doi.org/10.3390/ijms23179751
Submission received: 7 August 2022 / Revised: 21 August 2022 / Accepted: 26 August 2022 / Published: 28 August 2022
(This article belongs to the Special Issue Microbial Biofilms and Antibiofilm Agents 3.0)
Browse Figures
Review Reports Versions Notes

Abstract

:
Quorum sensing (QS), a type of bacterial cell–cell communication, produces autoinducers which help in biofilm formation in response to cell population density. In this review, biofilm formation, the role of QS in biofilm formation and development with reference to biological wastewater treatment are discussed. Autoinducers, for example, acyl-homoserine lactones (AHLs), auto-inducing oligo-peptides (AIPs) and autoinducer 2, present in both Gram-negative and Gram-positive bacteria, with their mechanism, are also explained. Over the years, wastewater treatment (WWT) by QS-regulated biofilms and their optimization for WWT have gained much attention. This article gives a comprehensive review of QS regulation methods, QS enrichment methods and QS inhibition methods in biological waste treatment systems. Typical QS enrichment methods comprise adding QS molecules, adding QS accelerants and cultivating QS bacteria, while typical QS inhibition methods consist of additions of quorum quenching (QQ) bacteria, QS-degrading enzymes, QS-degrading oxidants, and QS inhibitors. Potential applications of QS regulated biofilms for WWT have also been summarized. At last, the knowledge gaps present in current researches are analyzed, and future study requirements are proposed.

1. Introduction

Since the start of microbiology, microorganisms have always been considered as freely suspended cells, having specific physiological, morphological, and growth characteristics in the culture media. However, microbes have been found to interact closely with interfaces and surfaces to form aggregates. These microbial aggregates are usually glued together with a sticky secretion of slime [1,2]. Such types of bacterial associations where a cluster of microbial cells are attached to a surface are termed biofilms (a primary mode of living and growth for bacteria) [3]. The initiation of biofilm formation requires a surface and the availability of nutrients vital for the growth of bacteria [4,5]. Costerton et al. (1978) defined biofilms as an aggregation of single or diverse types of microbial cells, attached to a biotic or abiotic surface, enclosed in a covering of extrapolymeric substance (EPS), where they live in a cooperative manner [6]. In natural reservoirs, various bacterial species, algae, protozoa and fungi form biofilms. About 50% of the total thickness of biofilm (0.2–1.0%) is formed by EPS, and the rest of the portion contains microorganisms [7]. Besides the aqueous matrix and microbial cells, biofilm also contains complex secreted metabolite polymers, cell lysis products, absorbed nutrients, and particulate material [8]. Hence, macromolecules, such as proteins, lipids, polysaccharides, and even DNA and RNA, have also been observed in the biofilm environment [3]. Biofilms also contain ketal-linked pyruvates and uronic acids, i.e., mannuronic acids, D-glucuronic acid, and D-galacturonic acid, which characterize the anionic nature of the biofilm [8]. These particles diffuse in and out of the biofilm, on the basis of their water-binding affinity, mobility, and size [8]. The biofilm structure also influences the mass transport of the available substances. The transportation of solutes is driven via pores and water channels in biofilms [9]. Due to the presence of numerous micro-environments, the biofilm matrix exhibits a high degree of microheterogeneity [5].
Biofilm formation is a dynamic process, whose development has several steps, including the reversible adherence of planktonic bacteria to the surface via van der Waals interaction, irreversible attachment through pili, fimbriae, and flagella, bacterial proliferation and secretion of EPS, followed by quorum sensing (QS) and biofilm maturation (Figure 1) [10,11,12].
Biofilms protect microbial cells from adverse environmental conditions, i.e., pH changes, presence of free radicals or toxic substances and less availability of nutrients as well as antibacterial agents and toxic actions [13]. Within a biofilm, the microbial population ranges from 108 to 1011 microbial cells per g wet weight [14]. The protective EPS layer of biofilm also prevents the microbes from exposure to pesticides, heavy metals, and hydrocarbons [15]. EPS surfactants are capable of solubilizing organic pollutants, which are usually non-degradable [16,17,18]. This advanced tolerance property of biofilm has specific relevance to biotransformation and bioremediation [19,20]. The composition of biofilm is extremely complex, and several techniques are being used to determine its morphology and composition. Atomic force microscopy (AFM), scanning electron microscope (SEM), and confocal laser scanning microscopy (CLSM) are used to determine the roughness, stiffness, and topography of mature biofilms. SEM and Fourier transform infrared (FTIR) are also used to determine the structure of EPS and the interactions among bacterial species in the biofilm. The elements present in the biofilm are also analyzed by energy dispersive X-ray (EDX) spectroscopy, while surface plasmon resonance (SPR) spectroscopy can analyze the whole biofilm formation process. The biofilm growth and microbial adhesion to surfaces are determined by electrical impedance spectroscopy (EIS). The bacterial diversity in a biofilm is assessed by 16S rRNA sequence analysis, and crystal violet assay is used to estimate the growth of biofilm (Figure 2) [21,22].

2. Relationship between Quorum Sensing (QS) and Biofilm Formation

QS is a type of bacterial cell–cell communication, where bacteria produce and release chemical molecules to regulate their gene expressions, responding to the cell population density [23,24,25]. This process was first proposed when bacterial interactions in Streptococcus pneumoniae and Vibrio fischeri were described by Miller and Nealson in the 1970s [24,26,27,28]. In 1998, QS influence in biofilm formation was described in Pseudomonas aeruginosa. However, later studies have revealed that the effect of QS on biofilm formation in P. aeruginosa was due to unnatural experimental conditions [29]. P. aeruginosa exhibits several QS circuits, which affect the biofilm development. At the genetic level of P. aerogenosa, both las and rhl acyl-HSL QS systems show involvement in the production of rhamnolipids required to maintain the architecture and structure of biofilm; hence, understanding the association between QS and the formation of biofilm is a complicated matter [4,30]. In QS, bacteria produce autoinducers (AIs), small signaling molecules, and release them into their surroundings. The concentrations of AIs are proportional to the bacterial population [31]. With the propagation of bacteria, the bacterial population increases, and hence, the concentrations of autoinducers also increase [4]. When a concentration of AIs attains a certain threshold level, they bind with cognate receptors. This binding triggers the downstream gene expression, which controls several bacterial activities, i.e., biofilm formation, virulence factor secretion, bioluminescence, sporulation, antibiotic production, etc. [32,33]. In this way, QS enables the bacteria to survive in a continuously changing environment [34]. In mature biofilms, QS also controls the changes required to allow the entry of nutrients into the cells. These changes usually include the formation of pores, channels, and pillar-like structures. This type of architecture ensures adequate division of nutrients among the cell population in a high-density biofilm. QS also influences biofilm development, as it has an important role in bacterial accumulation on solid surfaces [34].

3. QS Signaling Molecules

Bacteria produce and respond to a diverse variety of AIs; however, there are three well-defined classes of autoinducers that are predominately produced by bacteria. These include acyl homoserine lactones (AHLs), autoinducer oligopeptide (AIP), and autoinducer-2 (AI-2). Usually, Gram-negative bacteria produce AHLs, and Gram-positive bacteria produce AIPs, while AI-2 is used by both types of bacteria for interspecies communication [24,33,35]. Besides these major signaling molecules, streptomyces butyrolactones, indole and diketopiperazines (DKPs) also act as QS molecules in some bacteria [36,37,38,39]. These diverse chemical molecules provide a diverse platform of intraspecies and interspecies crosstalk [4]. Among all these molecules, AHLs are widely studied and characterized as bacterial interspecies signaling molecules [40]. Some bacteria produce more than one type of signaling molecule, which makes the quorum sensing mechanism quite complex to understand [24,31].

3.1. Classical QS Signaling Molecules

3.1.1. Acyl Homoserine Lactones

Acyl homoserine lactones (AHL) are specific to Gram-negative bacteria for their cell-to-cell communication. These autoinducers consist of an acyl side chain attached to a homoserine lactone moiety by an amide linkage [41]. LuxR/I-type is the most studied quorum sensing system. In AHL-mediated communication, AHLs bind to the transcriptional factors, which initiate the signaling cascade to regulate the relevant genes. LuxI homologue synthesizes AHL synthase, which produces AHL molecules. AHL molecules, having short side-chains, easily diffuse across the membrane, while the molecules with larger side-chains used efflux pumps to come out of the cell. On reaching the high concentration, the AHL molecules are taken by the cells, and cytoplasmic LuxR proteins interact with them to regulate the downstream process [42]. Several Gram-negative bacteria, such as P. aeruginosa, P. putida, Serratia liquefacians, and Burkholderia cepacia, are cited in the literature to communicate through AHLs [43,44]. However, Exiguobacterium sp., a Gram-positive bacterium, also communicates with AHL signaling (Figure 3A) [45].

3.1.2. Autoinducing Peptides

Autoinducing peptides (AIPs) are small post-transcriptionally modified peptides produced by Gram-positive bacteria [46,47]. These AIPs regulate the communication process by some specific surface receptors of the cells, via a chain of phosphorylation, and dephosphorylation series, usually by membrane-associated sensor kinases and response regulators of bacteria [44]. Studies report that Gram-positive bacteria, such as S. aureus, Lactobacillus plantarum, Clostridium difficile, C. botulinum, C. perfringens, Enterococcus faecalis and Listeria monocytogenes, communicate via AIPs (Figure 3B) [48,49,50].

3.1.3. Autoinducer-2

Autoinducer-2 is produced via activated methyl cycle and is a derivative of 4, 5-dihydroxy-2, 3 pentanedione (DPD). AI-2 is used as a signaling molecules by both Gram-positive and Gram-negative bacteria. When the concentration of AI-2 reaches a threshold level, a signal transduction cascade is activated to uptake and process AI-2. Cell membrane transporters uptake AI-2 inside the cell where cell kinases carry out phosphorylation of AI-2 and activate the QS circuit by binding to the relevant activator and repressor genes. Vibrio cholera, V. harveyi, S. typhi, Escherichia coli and Deinococcus radiodurans are reported to use the AI-2 signaling pathway (Figure 3C) [51,52,53].

4. Role of QS-Regulated Biofilms in Wastewater Treatment (WWT)

Biological methods of wastewater treatment have long been adopted in wastewater bioremediation. The basic mechanism behind this technique is the utilization of microorganisms in contaminated environments, the contaminants of which act as the energy sources for the bacteria. Microorganisms uptake the contaminants, metabolize them and produce building blocks for their cells. As a result of this process, the contaminants are removed from the environment [4]. In several wastewater treatment systems, bacterial biofilms are employed to perform detrimental roles [54]. A dense microbial population is utilized in biological wastewater treatment in various forms, i.e., granules, flocs, and biofilms. Mostly Gram-negative bacteria producing AHLs are employed for wastewater treatment [54,55,56]. Wastewater with problematic biological oxygen demand (BOD), nitrogen, nitrate ammonia, and dissolved O2 is treated with bacterial biofilms. The organic and inorganic constituents of wastewater induce the growth of indigenous microbes, the metabolites of which also reduce water contamination [22]. The treatment of domestic wastewater and industrial wastewater is carried out in biological contact oxidation tanks, moving bed biofilm reactors (MBBRs), biological aerated filters, biological rotating discs, integrated fixed film activated sludge reactors, and biofilm fluidized beds (BFB). MBBRs, trickling filters, and granular sludge need robust biofilms for wastewater treatment [54]. These reactors eliminate organic and nitrogenous pollutants quickly and generate less sludge [21,57].
The biofilm use in wastewater bioremediation depends on the interaction of microbes with xenobiotic substances present in the environment. The microbial cells immobilized in the biofilm synthesize several enzymes, which contribute significantly to bioremediation. Biofilms are preferred over planktonic cells in performing efficient bioremediation because of the horizontal gene transfer among the members of a biofilm [25]. The functional regulation of biofilms is due to the process of QS. The study at the WWT facility found a strong correlation between AHL production and biofilm development at the growth or activation stage [4]. However, in later stages of biofilm formation, this connection was not statistically significant [58]. The QS signals, i.e., AHLs produced by Pseudomonas, Agrobacterium, and Aeromonas, significantly contribute to wastewater treatment [4]. AHLs also accelerate phenol degradation and its derivatives present in wastewater [59]. Hexadecane degradation is aided by the QS signals of Acinetobacter sp. DR1 [60]. The P. aeruginosa rhl QS system and catechol 2, 3-dioxygenase expression system are involved in benzoate, phenol, and phenanthrene degradation [61]. Aeromonas and Pseudomonas, the AHL-producing bacterial genera, are abundantly present in activated sludge and are also used for the purification of industrial and domestic wastewater. N-heptanoyl-L-homoserine lactone regulates the structure and metabolic activity of activated sludge in WWT [62]. Hexadecane is metabolized by the autoinducers produced by Acinetobacter sp. via QS. Desulfovibrio and other sulfate-reducing bacteria (SRB) are used in wastewater treatment containing Cu+2 [63]. Acidovorax sp., Pseudomonas sp., and Luteimonas sp. are used to accelerate the biodegradation of bisphenol A (BPA) in wastewater. The wastewater treatment systems for nitrogen metabolism have been reported to contain Bosea, Devosia Mezorhizobium, Paracocci, and Pseudoxanthomonas species [64,65].
EPS synthesis, biofilm development, organic pollutant biodegradation, and biofouling control in wastewater treatment have all been reported to be influenced by quorum sensing (QS) and quorum quenching (QQ), a technique of blocking the QS system and inhibiting gene expression (Table 1) [22]. With the advancement in molecular biology and analytical detection techniques, the formation of AHLs and AHL-alike molecules was observed in a variety of biological wastewater treatment systems (Table 2) [66,67,68,69,70]. Moreover, it was found that many activated sludges included both AHL-producing QS bacteria and AHL-degrading QQ bacteria [59,66,71,72,73]. AHL signals, impressively, can play a significant role in the biological wastewater treatment process, particularly in the areas of biofilm formation and maturation [74,75,76,77,78], microbial aggregation and stabilization [59], exoenzyme activity [62], sludge structure stability and granule formation [79,80]. Additionally, the beneficial effects of AHL-based QS regulation in the biodegradation of organic pollutants, such as phenol biodegradation, ammonium oxidation [59,68,81] anthranilate degradation, and denitrification, have also been discovered [82].

5. QS-Mediated Biofilm Regulation Methods in Wastewater Treatment Systems (WWTs)

Once it was discovered that quorum sensing has an influence on biofilm formation in wastewater treatment systems, researchers shifted their focus to how to regulate QS in WWTs so as to improve these systems’ working efficiencies [88]. Studies were carried out in search of QS regulation methods to optimize wastewater treatment systems (Table 3) [113,114,115]. In an experiment aimed at aquaculture wastewater treatment with biofilm, QS was promoted in the system by the addition of two AHL signaling molecules i.e., N-hexanoyl-homoserine lactone (C6-HSL) and N-3-oxo-octanoyl-homoserine-lactone (3-oxo-C8-HSL) [116]. The addition of AHLs had a positive effect on biofilms; it not only significantly increased biofilm biomass, but also helped in improving the overall internal environment of the system. In another study on QS regulated biofilm, conducted by Valle et al. (2004), it was found that with the addition of 2 μmol/L AHLs in a methanol wastewater treatment system, not only was the methanol decomposition rate increased, but also a positive change in bacterial diversity, community composition, and community function in the system was observed [59].
All QS signaling molecules have different effects, and thus, QS-based regulation methods are categorized into two groups: QS enrichment methods and QS inhibition methods [117].
Table
Table 3. QS regulatory systems and autoinducers present in both Gram-negative and Gram-positive bacteria.
Table 3. QS regulatory systems and autoinducers present in both Gram-negative and Gram-positive bacteria.
Type of MicrobeBacterial SpecieAI Molecule TypeQS Regulatory SystemRef.
Gram-negative bacteria [(LuxI/LuxR homologue) based regulator system]Erwinia carotovoraN-(3-oxooctanoyl)-HSLTraI/TraR[118]
Serratia liquefaciensN-butanoyl-HSLSwrI/SwrR[119]
Yersinia pseudotuberculosisN-octanoyl-HSL,
N-(3-oxohexanoyl)-HSL		YtbI/YtbR
YpsI/YpsR		[120,121]
Burkholderia cepaciaN-octanoyl-HSLCepI/CepR[24,122]
Halomonas anticariensisN-butanoyl-HSL, N-hexanoyl-HSL, N-octanoyl-HSL, N-dodecanoyl-HSL hanR/hanI[15,123]
Gram-positive bacteriaBacillus subtilisComX,
CSF (competence stimulating factor)		ComP/ComA[6]
Staphylococcus intermediusAIPAgrC/AgrA[124]
Streptococcus mutansCSP ComC)
,XIP (sigx inducing peptide) ComS)		ComD/ComE
ComR		[125,126]
Lactobacillus plantarumLamD558LamC/LamA[127,128]

5.1. QS Enrichment Methods

These methods simply help to increase the content of QS signaling molecules in the biofilms and thus help smoothen the overall operation of biological wastewater treatment systems [117]. There are three ways to enhance QS in WWTs: (i) addition of exogenous QS signaling molecules, (ii) increased synthesis of QS signaling molecules through addition of accelerators, and (iii) QS bacteria cultivation.

5.1.1. Addition of Exogenous QS Signaling Molecules

The addition of QS signaling molecules is the most well-known method for QS enhancement in WWTs that has direct control over QS levels and helps improve the bioreactor’s performance [58]. For instance, in a study, nitrogen transformation was successfully enhanced in an anaerobic ammonium oxidation process and moving bed biofilm reactor (MBBR) through the addition of exogenous C6-HSL and C8-HSL [129,130]. The addition of QS signaling molecules significantly improved the electrochemical reactor’s performance in organics removal. In microbial electrolysis cells (MECs) and microbial fuel cells (MFCs), power production capacity and electron transfer were found to have a stable increase with the addition of QS signaling molecules [62,113,131]. Disadvantages with this method are the high expense and instability caused by QQ bacteria [132].

5.1.2. Adding Accelerators for Synthesis of QS Signaling Molecules

The addition of accelerators is another method for QS enhancement in WWTs, where they help increase the synthesis of QS signaling molecules. Advantages of using this method are their low-cost, compared to the method of direct addition of QS signaling molecules, and their biggest flaw is their failure in the synthesis of QS signaling molecules, which is a complex process and may not be productive. Some of the reported accelerators either act as precursors for QS molecules or work in their release. For example, a prominent QS enhancer is boron, which forms a complex with 4,5-dihydroxy-2,3-pentanedione (DPD), acting as a precursor for AI-2 activation [133,134]. In bioelectrochemical fuel cells, this addition of boron has resulted in an increased potential of almost 15 mV [134].

5.1.3. QS Bacterial Cultivation

Another method that is more economical compared to direct addition of QS molecules or accelerators is the cultivation of QS bacteria, which are found in nature. In a study on leachates, Soler et al. (2018) isolated five QS bacterial strains out of a total of 99 bacterial strains [132]. While working on mature aerobic granular sludge, Zhang et al. (2020) used a supernatant of seven AHL-producing strains and added it to sequencing batch reactors [135]. He found an increase of 23%, 81%, and 27%, respectively, in concentrations of C6-HSL, C8-HSL, and N-(3- oxooctanoyl)-l-homoserine lactone (3OC8-HSL). Yong and Zhong, 2010 added P. aeruginosa (serves as pollutant degrader and AHL producer) to WWTs and found that it had a significant influence on the removal of organic carbon, nitrogen, and ammonia in the system and improved the overall performance of biological treatment systems [81]. The disadvantage of using this method is that these bacteria are more difficult to work with than other QS enhancement methods, may be washed out with excess biomass, and may be inhibited by competition with other bacteria in WWTs. In MBBR, the addition of Sphingomonas rubra sp. Nov (QS bacterium) had no significant effect on NH4+-N removal and COD. A similar scenario was also observed with the addition of Aeromonas sp. (an AHL producer), which caused a significant decrease in COD removal from 7% to 1%, from day 7 to day 40 [136,137].

5.2. QS Inhibition Methods

These methods aim to lower the concentration of QS signaling molecules. They either degrade QS signaling molecules, interfere with their functions, or inhibit their synthesis in biological treatment systems (Figure 4) [117]. QS inhibition can be achieved in four ways: (i) QS inhibitor addition, (ii) QQ bacteria cultivation, (iii) reactive oxygen species-based QS signaling molecules degradation, iv) enzyme-based QS signaling molecules degradation.

5.2.1. QS Inhibitor Addition

These inhibitors interfere with QS receptors or inactivate QS signaling molecules and are thus being used in WWTs [138,139,140]. Examples of such inhibitors are homoserine lactone-like TGK series, cladodionen, 3-amino2-oxazolidinone YXL-13, ε-polysine, gingerol, aporphinoid alkaloids, etc. [141,142,143,144,145,146,147,148,149,150]. A QS inhibitor, 4- hydroxy-3-methoxy benzaldehyde (Vanillin), when applied to reverse osmosis (RO) membrane, decreases biofilm formation by up to 45%. In MBR, the addition of 100 ug/L of QS inhibitor 3,3′,4′,5-tetrachlorosalicylanilide caused a 50% decline in biofilm formation and a 30% decrease in AI-2 concentration. They are easily synthesized and economical, with cheap operating costs [117].

5.2.2. QQ Bacterial Cultivation

A more common method than QS inhibitor addition is QQ bacterial strain cultivation for successful degradation of QS signaling molecules. Some examples of naturally isolated QQ bacteria that can rapidly degrade QS signaling molecules are Penicillium restrictum CBS 367.48, Rhodococcus sp. BH4, Pseudomonas sp. HS-18, and Bacillus licheniformis T-1 [97,151,152,153,154]. Among them, one of the most well-known QQ strains is Rhodococcus sp. BH4 [97,155]. Genetic engineering has also been employed in producing new and more potent QQ strains through plasmid transformation [156]. Just in a span of 30–60 s, the suspensions of Firmicutes and Betaproteobacteria at OD600 = 1.0 removed around 200 nM AHL [157]. It is expected that with further research on areas related to the isolation and evaluation of these QQ strains, more promising QS inhibition methods can be developed to be applied on a large scale [117,157].

5.2.3. Degrading QS Signaling Molecules by Production of Reactive Oxygen Species (ROS)

In recent years, reactive oxygen species (ROS) production has gained popularity as a new QS inhibition method. ROS mentioned here are hydroxyl radicals and superoxide [158,159]. In E. coli, Short-time UV-TiO2 photocatalysis was used to generate ROS, which then not only inactivated A1-2 produced by E. coli but also caused a reduction of 42.6% in biofilm biomass [160]. In MBR, biofouling was successfully mitigated by continuous application of UV photolysis or photocatalysis [159,161].

5.2.4. Degrading QS Signaling Molecules by Enzymes

The direct addition of enzymes for QS signaling molecule degradation is another new, emerging QS inhibition method. Many such enzymes have been studied so far; among them, enzymes for AHL degradation are the most studied. Acylase, deaminase, Lactonase, and decarboxylase are found to have the most capacity for AHL degradation in WWTs (Table 4) [103]. In MBR, levels of QS signaling molecules were reduced when Acylase (the most frequently used enzyme for AHL degradation) was applied [162].

6. Potential Applications of QS Regulated Biofilms for WWTs

6.1. Membrane Bioreactors (MBRs)

Membrane bioreactors (MBRs) have been widely employed in drinking water production, wastewater reclamation, and seawater desalination, due to their compact design process, and the high water quality they produce [168]. However, one of the most significant operational issues associated with MBRs is membrane biofouling, which sometimes causes permeate flux and a decrease in water quality. It may also increase operational expenses to meet the need for periodic membrane cleaning and replacement [169,170,171,172]. Membrane biofouling refers to the unwanted buildup of microorganisms on membrane surfaces as a result of the adherence, growth, and proliferation of living organisms [171,173]. Biofouling is rarely avoidable, because most of the time systems are not sterile, allowing microorganisms to reseed and regrow at the expense of biodegradable substances present in water, turning them into metabolic products and biomass. Hence, biofouling is more difficult to remove, as compared to the fouling of organic and inorganic substances, which can be removed in the majority of cases by effective pretreatment. Therefore, efficient methods of biofouling control in the membrane process are required [4]. Studies have demonstrated that the issue of membrane biofouling in MBRs is highly associated with the production of AHL signals during biofilm formation [75,174,175,176,177,178]. In a study by Yeon et al. (2009a), TLC chromatographic analysis of the MBR membrane biocake showed the existence of C6-HSL and C8-HSL autoinducers produced during the operation of MBRs and increased the transmembrane pressure [106]. The ability of several bacterial species found in MBRs, including Citrobacter, Enterobacter, Raoultella, Serratia, Pseudomonas, Aeromonas, and Klebsiella, to create AHL signals and control the development of biofilms on membrane surfaces was also documented [69]. According to those researches, AHL-based QS uniformly controls the development of biofilms, which then causes membrane biofouling in MBRs [94].
One of the best techniques for preventing membrane befouling is quorum quenching (QQ), a technique of blocking the QS system and inhibiting gene expression (Figure 5) [172].
According to quorum quenching principles, quorum sensing interference in bacteria prevents the establishment of desired phenotypes such as biofilms [178]. QQ solves the limitations of high-cost operation, less resource utilization, and inconvenient management of traditional antifouling methods such as membrane cleaning, membrane modification, tuning of liquor, etc. [172,179,180,181,182,183,184]. In addition, it also eliminates the use of antimicrobial agents, hence reducing the risk of multi-drug resistance development in the biofilms [178,185,186]. Researchers have identified several AHL-generating bacteria and isolated them to be employed in biofilm reactors for wastewater treatment. Li et al., 2007 isolated two AHL-producing bacterial strains when they used the biofilm method for the treatment of nitrobenzoic acid-containing wastewater [187]. In order to screen out 200 microorganisms that can produce AHLs, Lade et al., 2014 employed the reported strains Chromobacterium violaceum CV026 and Agrobacterium tumefaciens A136 in WWT [69]. The results obtained after performing 16S rRNA sequencing allowed the speculation that Aeromonas and Enterobacter sp. were the dominating microorganisms in the system. The presence of AHLs indicates the existence of QS in the biofilm process under natural conditions [88].

Hybrid MBR-Attached Growth MBR (AGMBR)

Although MBR is popular now, some obstacles have interfered with conventional MBR (CMBR) commercialization for wastewater treatment. One major obstacle is membrane fouling; some other issues are the limited and low removal of some emerging pollutants [188,189] and significant removal of nitrogen and phosphorus from treatment systems [190]. Researchers have developed a hybrid MBR named attached growth MBR (AGMBR), through the integration of CMBR with an attached growth process, to overcome these limitations of CMBRs [188]. In this hybrid MBR, pollutant removal is accomplished through several ways such as (i) activated sludge-mediated sorption or degradation, (ii) degradation through microbes attached to media, (iii) by sorption onto the media, (iv) degradation through attached biofilms, and (v) rejection by a membrane. It was found that the use of media in AGMBR can improve the overall performance of the system in terms of membrane filterability and mitigating membrane fouling through modifying sludge suspension characteristics, reducing the concentration of suspended solids, and enhancing the physical scouring effect of the suspended carriers [191,192,193]. AGMBR mitigated membrane fouling through bio-augmented carriers such as PVA gel beads, PVC carriers, and MPCs. All of these carriers either control or reduce membrane fouling by allowing less organic matter buildup on the membrane surface, which in turn limits microbial growth on surfaces and reduces EPS and SMP levels [194,195,196,197].
In AGMBR, activated carbon (AC) and polymeric carriers were used as conventional media [188,198,199]. It was found that with the use of AC, AGMBR (both aerobic and anaerobic) can remove >80–90% of COD and BOD5 from municipal or domestic wastewater, in comparison to single aerobic MBR or AnMBR. The overall use of conventional media allows AGMBR to have increased biomass retention, diverse microbial communities, and improved microbial activity, all of which help in increasing the removal of pollutants [193]. New media used in AGMBR include biochar and bio-augmented carriers (containing selected strains/mixed cultures). These aid in thick biofilm formation and in removing high nitrogen content and COD (>80%). It was observed that biochar addition in anaerobic AGMBR favors removal of NH4+-N through adsorption, while in aerobic AGMBR, it helps remove up to 100% NH4+-N [200,201]. Hybrid MBR with biochar has the ability to not only remove conventional pollutants, but also emerging pollutants that are highly toxic and can persist in water bodies for long periods. Examples of such pollutants are adsorbable organic halogens, micropollutants, and nonylphenol. Wastewater also has some other compounds (refractory compounds) that are carcinogenic and mutagenic in nature, such as long-chain hydrocarbons, nitrogenous heterocyclic compounds, polynuclear aromatic hydrocarbons, etc. All of these pollutants have a detrimental effect on human health and are a threat to the environment [202,203,204]. In AGMBR, in comparison to CMBR, better and far more improved removal of organics, nutrients, and micropollutants has been reported due to an increase in biomass concentration, improved microbial activity and/or diversity, and improved simultaneous nitrification and denitrification [205,206]. Though AGMBR has widespread applications in controlling membrane fouling and wastewater treatment, there is still much work to do, such as researching new media for better applications of AGMBR for pollutant removal, both conventional and emerging, or for pilot or full-scale applications [193].

6.2. Microbial Fuel Cells (MFCs)

These are bio-electrochemical systems that use biofilms as catalysts to convert chemical energy into electrical energy. They can generate electricity through low-grade biomass and even through wastewater [207]. They have a cathode chamber, an anaerobic anode chamber, a salt bridge, or a proton exchange membrane (PEM) that works as a separating unit between both chambers and only allow protons (H+) to pass to cathode from anode. In MFCs, the anode is the final electron acceptor, and bacteria get their energy through electron transfer to the anode from their central metabolic system. With the help of an external circuit, the electrons are conducted to the cathode, where they form water after combining H+ and oxygen. Not only pure but mixed bacterial cultures are also being employed for electricity generation in MFCs [208,209,210,211,212]. There are three ways by which extracellular electron transfer from bacteria to an anode can be accomplished in an MFC; (i) with the help of pili (electrically conductive), (ii) with the use of electron mediators (provided artificially or produced by microbes), and (iii) through direct outer membrane c-type mediated cytochrome transfer [5,213,214]. In the case of two-chamber conventional MFCs, in the anaerobic anode chamber, biofilms oxidize their organic or inorganic substrates, and electrons released during this process are sent to the electrode directly or through an electron mediator indirectly. Electricity is generated when electrical current flows in from an electrical circuit [215].
In P. aeruginosa, phenazines act as electron mediators and promote respiration with the electrode. In MFCs, current production by P. aeruginosa and QS are directly linked with the production of phenazine [216,217]. Other than controlling rhlI, LasR, a transcriptional regulator, regulates the pqsABCDE operon positively to produce PQS, another QS signal for P. aeruginosa. In contrast to this, phz, which controls the production of phenazine and helps in electron transfer to the anode, is controlled by pqs operon [207]. In a study, for QS overexpression, multi-copy broad-host plasmid pYC-rhlIR was transformed in strain CGMCC 1.860. The transformation resulted in phenazine overproduction and elimination of the above-mentioned compound. This newly transformed strain is 1.6 times more potent than the wild-type strain in producing current output. A limiting factor in P. aeruginosa mediated electricity production is that PQS-driven QS can inhibit anaerobic growth of not only P. aeruginosa, but some other co-culture species [218,219]. A new P. aeruginosa strain with defective PQS and overproduction of phenazine was constructed to solve this problem. It can not only anaerobically synthesize higher phenazine concentrations, but also generate five times more current density in comparison to its parent strain [215]. Further electrochemical studies showed a correlation between phenazines’ overproduction and current increase. Correspondingly, microbial electrochemical systems (MESs) were shown to be affected by AHLs. In microbial electrolysis cells (MECs), AHL addition regulated biofilm formation at anodes, which enhanced bioelectrochemical activities in MECs [113].
For example, addition of a short-chain AHL, i.e., 3-oxo-C6-HSL, in comparison to the addition of 3-oxo-C12-HSL, provided higher hydrogen yields, which were due to changes in the community structure of microbes in cathodic biofilms [220]. Short-chain ‘3-oxo-C6-HSL’ AHL addition reduces hydrogen scavengers and increases the electrochemically active population of bacteria, which in turn give rise to higher hydrogen yield and electron recovery. In another study, by inoculating P. aeruginosa PAO1 pure culture in MFCs, it was found that compared to wild type, AHL-deficient lasIrhlI mutant type showed less extracellular electron transfer. Interestingly, electricity production was restored to the levels of wild-type strains with exogenous C4-HSL addition [221].
Wastewater contains sufficient amounts of organic compounds that can be used as substrates by MFCs for electricity generation. Wastewater of many different types has been used in MFCs for side-by-side water treatment end electricity generation. Rather than removing waste from wastewater through chemical or physical means, MFCs are an alternative, environmentally friendly way to harness the power of microbes for wastewater treatment and production of electricity. Substrates used for pollutant removal and energy generation by MFCs include starch and food processing wastewater, chocolate industry wastewater, domestic wastewater, azo dyes containing textile wastewater, and mustard tuber wastewater. However, there are still some limitations associated with full-scale use of MFCs, such as low power density, membrane fouling, and high internal resistance of the reactor. These limitations have limited MFC application on a commercial scale [222].

6.3. Granular Sludge

Granular sludge is a particular type of biofilm that can be categorized into aerobic granular sludge (AGS) and anaerobic granular sludge (AnGS). All of the previous studies on granular sludge primarily studied the effect of fluctuating environmental conditions and physicochemical properties of sludge on microbial communities, hydrophobicity, EPS, surface charges, and the granulation process. However, in the sludge granulation process, regulation of QS on biofilms is also applied. The primary benefit of QS in flocculent granular sludge includes the increased production of EPS and ATP, which ultimately speed up the formation of granular sludge microbial communities. In granular sludge, the microbial communities consists of several species that perform a variety of metabolic tasks demonstrating the community level as a whole. Signaling molecules are the vital link that binds these communities together. Currently, the major signaling molecules in granular sludge systems are diffusible signaling molecules (DSF), intraspecific signaling molecules (AHL), and interspecific signaling molecules (AI-2) [88].

6.3.1. Aerobic Granular Sludge (AGS)

Aerobic granular sludge has gained extraordinary attention in the research field because of its superior settling ability, high biomass retention, outstanding anti-shock loading capability, small occupied footprint, and treatment efficiency as compared to conventional activated sludge. To cultivate aerobic granular sludge, activated sludge is used as a seed. AGS grows as a spherical form of biofilm with no carriers because of its self-immobilization property [88,223]. The pilot and full-scale use of AGS persuasively demonstrate the value of aerobic granulation technology in real-world settings [224]. Several potential factors, including organic loading rates, substrate composition, hydrodynamic shear force, settling time, seed sludge properties [225,226], starvation period, and sludge discharge affect aerobic granulation and have been studied [227,228,229]. During aerobic granulation, selection pressures are indispensable to achieve fast-settling aerobic granules while washing out the slow-settling flocs [229]. Moreover, the bacterial interactions and their coordinated behaviors also affect the aerobic granulation setting [230].
In 2006, for the first time, a report was published related to aerobic granulation and QS. In that report, AI-2 was detected in two genetically distinct bacterial co-culture strains forming aerobic granules [231]. Besides AI-2, AHLs were also detected in the cellular extracts and suspensions of AGS [230]. Extensive data are available online explaining the characteristics and different cultivation methods of AGS. However, the involved mechanism is not yet clear. The evidence for the vital role of QS in granule formation is increasing day by day. AHL displays a dense signaling molecule network within the granule interior and performs well in boosting the development of biofilms and microbial granulation [59]. Signaling molecules continue to promote the adhesion development and accumulation of suspended bacteria to form mature granules. They also aid in preserving the stability of granule structure and speed up granule formation. More signaling molecules are detected in mature granules as compared to smaller granules [88]. Hence, QS-based regulation may prove to be a novel technique to encourage AGS development and preserve granular stability, but there are still some challenges and knowledge gaps that need to be addressed.

6.3.2. Anaerobic Granular Sludge (AnGS)

Anaerobic granular sludge has a more complicated quorum sensing system than AGS and still lacks a relatively full regulation mechanism. AHL, AI-2, and DSF are the main research topics associated with the AnGS system. Ding et al. [231], reported 5.72 ± 1.56 pM/L as the initial total concentration of AHLs produced in a granular sludge system, of which 95% of the AHL concentration was composed of C4-HSL [231]. However, the C4-HSL concentration dramatically decreased with the development of AnGS, while the content of AI-2 remained stable [232,233,234]. Another study reported an increase in DSF concentration to 1.76 ± 0.18 nM/L from 0.66 ± 0.06 nM/L [235].
In AnGS, the granule particle size is influenced by AHL-based regulation. A large-sized particle has high biological activity, and its internal structure characterization based on its small diffusion area, porosity, low diffusivity, and macro void, facilitates improved production of biogas [236]. In contrast to this, the inoculation of exogenous AHL-producing and -quenching bacteria reduced the particle size in a study that hinted toward further investigation in this regard. This may have resulted due to the destruction of the original bacterial community structure as the additional strains did not dominate the system and showed less competition with local bacteria. Ding et al. [231] reported an increase in granular diameter via AI-2 regulation while reduced granule size due to DSF regulation [231].
Under neutral/weak alkaline conditions, by increasing the amount of AI-2 and reducing the amount of DSF in the system, the relative hydrophobicity and strength of the granular sludge will increase. This also facilitates granular sludge formation with large-size granules. However, if there is an imbalanced nitrogen supply, increasing the amount of AI-2 and reducing the amount of DSF in the system significantly reduces the particle strength and hydrophobicity of the sludge [231,237,238]. The findings of Ding’s study [231,237,238] further supported the notion that AI-2 can encourage the synthesis of EPS and increase the particle diameter of granular sludge. Additionally, AHLs might encourage Methanothrix development in the upflow anaerobic sludge bed reactor (UASB), which would greatly enhance sludge granulation and reactor operating efficiency. Exogenous AHLs play a significant role in regulation of EPS and microbial community structure, improving the performance of AnGS. Specific AHLs can increase the organic matter removal capacity and methanation ability in AnGS [239,240].

7. Conclusions and Future Perspectives

Biofilms are the aggregations of the same or different microbial communities, impregnated in a complex matrix and partitioned by a network of water channels. These are natural habitats in which microbes interact with each other by exchanging genetic material, metabolites and signaling molecules. Biofilm formation is a complex process regulated by QS. The control of biofilm formation has gained much attention in WWT. In order to improve and optimize biofilm control strategies, it is important to understand the factors that strongly influence biofilm formation. Genetic engineering techniques, such as metabolic engineering, omic based approaches, genome editing and bioinformatics approaches, have opened new avenues for biofilm-related wastewater treatment research. QS regulates EPS and biosurfactant synthesis, which can significantly contribute in waste water treatment. Understanding the complex QS mechanisms is difficult, because of the production of multiple signaling molecules. Hence, the determination of the factors that stimulate the emergence of QS is a major challenge. These factors may include gene expression patterns, cell-to-cell interaction, physiological properties and molecular level details of signaling molecules.
Although the utilization of QS for biological wastewater treatment has made great achievements in the field of WWT, there are still several problems yet to be addressed. Future research on biofilm-based wastewater treatment needs to cover several dimensions such as the evaluation of the risks associated with QS regulation, accurate estimation of QS level so that the interference caused by the coexistence of QQ and QS can be eliminated, evaluation of the efficacy of several QS inhibition or activation methods usually adopted in wastewater treatment, understanding the metabolism, distribution and fate of the QS signaling molecules produced during wastewater treatment, and changes in microbial community at the molecular level. The disturbance created by QQ in the understanding of QS should be eliminated by comprehensive and quantitative optimization for different types of wastewater bioreactors. The molecular tools, such as metagenomics and meta-transcriptomics, should be comprehensively adopted to understand the molecular level changes in QS-regulated biofilm during wastewater treatment. Most of the QS regulation-based studies of WWTs are not being conducted at a large scale, but at experimental levels in laboratories. Therefore, the mechanisms and effects of QS regulation strategies should also be explored on a large scale. Moreover, the QS approach, besides having several advantages, must have some negative impacts on the physiological behavior and structure of the biofilm. These impacts should also be studied for improvements in biological wastewater treatment by eco-friendly approaches using QS-regulated biofilms.

Author Contributions

Conceptualization, methodology, supervision, writing-review and editing, H.M.; conceptualization, visualization and writing-original draft preparation, S.S. (Sania Sahreen) and S.S. (Sundas Sharif); visualization, validation, V.H. and A.M.; supervision, writing-review and editing, K.I. All authors have read and agreed to the published version of the manuscript.

Funding

This study received no external funding.

Institutional Review Board Statement

Not applicable.

Informed Consent Statement

Not applicable.

Data Availability Statement

Not applicable.

Acknowledgments

This research paper is supported by the project “Increasing the impact of excellence research on the capacity for innovation and technology transfer within USAMVB Timișoara” code 6PFE, submitted in the competition Program 1—Development of the national system of research—development, Subprogram 1.2—Institutional performance, Institutional development projects—Development projects of excellence in RDI.

Conflicts of Interest

The authors declare no conflict of interest.

References

  1. Wimpenny, J.; Manz, W.; Szewzyk, U. Heterogeneity in biofilms. FEMS Microbial. Rev. 2000, 24, 661–671. [Google Scholar] [CrossRef]
  2. Costerton, J.W.; Stewart, P.S.; Greenberg, E.P. Bacterial biofilms: A common cause of persistent infections. Science 1999, 284, 1318–1322. [Google Scholar] [CrossRef] [PubMed]
  3. Sutherland, I.W. The biofilm matrix—An immobilized but dynamic microbial environment. Trends Microbiol. 2001, 9, 222–227. [Google Scholar] [CrossRef]
  4. Feng, L.; Wu, Z.; Yu, X. Quorum sensing in water and wastewater treatment biofilms. J. Environ. Biol. 2013, 34, 437. [Google Scholar] [PubMed]
  5. Singh, R.; Paul, D.; Jain, R.K. Biofilms: Implications in bioremediation. Trends Microbiol. 2006, 14, 389–397. [Google Scholar] [CrossRef] [PubMed]
  6. Balan, B.; Dhaulaniya, A.S.; Varma, D.A.; Sodhi, K.K.; Kumar, M.; Tiwari, M.; Singh, D.K. Microbial biofilm ecology, in silico study of quorum sensing receptor-ligand interactions and biofilm mediated bioremediation. Arch. Microbiol. 2021, 203, 13–30. [Google Scholar] [CrossRef]
  7. Mosharaf, M.K.; Tanvir, M.Z.H.; Haque, M.M.; Haque, M.A.; Khan, M.A.A.; Molla, A.H.; Alam, M.Z.; Islam, M.S.; Talukder, M.R. Metal-adapted bacteria isolated from wastewaters produce biofilms by expressing proteinaceous curli fimbriae and cellulose nanofibers. Front. Microbiol. 2018, 9, 1334. [Google Scholar] [CrossRef]
  8. Flemming, H.C. Sorption sites in biofilms. Water Sci. Technol. 1995, 32, 27. [Google Scholar] [CrossRef]
  9. Horn, H.; Morgenroth, E. Transport of oxygen, sodium chloride, and sodium nitrate in biofilms. Chem. Eng. Sci 2006, 61, 1347–1356. [Google Scholar] [CrossRef]
  10. Azeredo, J.; Azevedo, N.F.; Briandet, R.; Cerca, N.; Coenye, T.; Costa, A.R.; Desvaux, M.; Di Bonaventura, G.; Hébraud, M.; Jaglic, Z.; et al. Critical review on biofilm methods. Crit. Rev. Microbiol. 2017, 43, 313–351. [Google Scholar] [CrossRef] [Green Version]
  11. Mattei, M.R.; Frunzo, L.; D’acunto, B.; Pechaud, Y.; Pirozzi, F.; Esposito, G. Continuum and discrete approach in modeling biofilm development and structure: A review. J. Math. Biol. 2018, 76, 945–1003. [Google Scholar] [CrossRef] [PubMed]
  12. Nishitani, K.; Sutipornpalangkul, W.; de Mesy Bentley, K.L.; Varrone, J.J.; Bello-Irizarry, S.N.; Ito, H.; Matsuda, S.; Kates, S.L.; Daiss, J.L.; Schwarz, E.M. Quantifying the natural history of biofilm formation in vivo during the establishment of chronic implant-associated Staphylococcus aureus osteomyelitis in mice to identify critical pathogen and host factors. J. Orthop. Res. 2015, 33, 1311–1319. [Google Scholar] [CrossRef] [PubMed]
  13. Davey, M.E.; O’toole, G.A. Microbial biofilms: From ecology to molecular genetics. Microbiol. Mol. Biol. Rev. 2000, 64, 847–867. [Google Scholar] [CrossRef] [PubMed]
  14. Flemming, H.C.; Wingender, J.; Szewzyk, U.; Steinberg, P.; Rice, S.A.; Kjelleberg, S. Biofilms: An emergent form of bacterial life. Nat. Rev. Microbiol 2016, 14, 563–575. [Google Scholar] [CrossRef]
  15. Mangwani, N.; Shukla, S.K.; Kumari, S.; Das, S.; Rao, T.S. Effect of biofilm parameters and extracellular polymeric substance composition on polycyclic aromatic hydrocarbon degradation. RSC Adv. 2016, 6, 57540–57551. [Google Scholar] [CrossRef]
  16. Edwards, S.J.; Kjellerup, B.V. Applications of biofilms in bioremediation and biotransformation of persistent organic pollutants, pharmaceuticals/personal care products, and heavy metals. Appl. Microbiol. Biotechnol 2013, 97, 9909–9921. [Google Scholar] [CrossRef]
  17. Hall-Stoodley, L.; Costerton, J.W.; Stoodley, P. Bacterial biofilms: From the natural environment to infectious diseases. Nat. Rev. Microbiol 2004, 2, 95–108. [Google Scholar] [CrossRef]
  18. Varjani, S.J.; Gnansounou, E.; Pandey, A. Comprehensive review on toxicity of persistent organic pollutants from petroleum refinery waste and their degradation by microorganisms. Chemosphere 2017, 188, 280–291. [Google Scholar] [CrossRef]
  19. Terry, J.B.; Stephen, A.M.; Jagath, L.K.; Zusheng, L. Interactions between biofilms and the environment. FEMS Microbiol. Rev. 1997, 20, 291–303. [Google Scholar]
  20. Johnsen, A.R.; Karlson, U. Evaluation of bacterial strategies to promote the bioavailability of polycyclic aromatic hydrocarbons. Appl. Microbiol. Biotechnol. 2004, 63, 452–459. [Google Scholar] [CrossRef]
  21. Huang, H.; Peng, C.; Peng, P.; Lin, Y.; Zhang, X.; Ren, H. Towards the biofilm characterization and regulation in biological wastewater treatment. Appl. Microbiol. Biotechnol. 2019, 103, 1115–1129. [Google Scholar] [CrossRef] [PubMed]
  22. Chattopadhyay, I.; Usman, T.M.; Varjani, S. Exploring the role of microbial biofilm for industrial effluents treatment. Bioengineered 2022, 13, 6420–6440. [Google Scholar] [CrossRef] [PubMed]
  23. Gera, C.; Srivastava, S. Quorum-sensing: The phenomenon of microbial communication. Curr. Sci 2006, 90, 666–676. [Google Scholar]
  24. Miller, M.B.; Bassler, B.L. Quorum sensing in bacteria. Annu. Rev. Microbiol. 2001, 55, 165–199. [Google Scholar] [CrossRef] [PubMed]
  25. Mangwani, N.; Kumari, S.; Das, S. Bacterial biofilms and quorum sensing: Fidelity in bioremediation technology. Biotechnol. Genet. Eng. Rev. 2016, 32, 43–73. [Google Scholar] [CrossRef]
  26. Nealson, K.H.; Hastings, J.W. Bacterial bioluminescence: Its control and ecological significance. Microbiol. Rev. 1979, 43, 496–518. [Google Scholar] [CrossRef]
  27. Nealson, K.H.; Platt, T.; Hastings, J.W. Cellular control of the synthesis and activity of the bacterial luminescent system. J. Bacteriol. 1970, 104, 313–32231. [Google Scholar] [CrossRef] [PubMed]
  28. Zhang, W.; Li, C. Exploiting quorum sensing interfering strategies in gram-negative bacteria for the enhancement of environmental applications. Front. Microbiol. 2016, 6, 1535. [Google Scholar] [CrossRef]
  29. Shrout, J.D.; Chopp, D.L.; Just, C.L.; Hentzer, M.; Givskov, M.; Parsek, M.R. The impact of quorum sensing and swarming motility on Pseudomonas aeruginosa biofilm formation is nutritionally conditional. Mol. Microbiol. 2006, 62, 1264–1277. [Google Scholar] [CrossRef]
  30. Schuster, M.; Greenberg, E.P. A network of networks: Quorum-sensing gene regulation in Pseudomonas aeruginosa. Int. J. Med. Microbiol. 2006, 296, 73–81. [Google Scholar] [CrossRef]
  31. Bassler, B.L.; Losick, R. Bacterially speaking. Cell 2006, 125, 237–246. [Google Scholar] [CrossRef] [PubMed]
  32. Bassler, B.L. Small talk: Cell-to-cell communication in bacteria. Cell 2002, 109, 421–424. [Google Scholar] [CrossRef] [Green Version]
  33. Waters, C.M.; Bassler, B.L. Quorum sensing: Cell-to-cell communication in bacteria. Annu. Rev.Cell Dev. Biol. 2005, 21, 319–346. [Google Scholar] [CrossRef]
  34. Liao, N.Q.; Li, H.M. Conceivable bioremediation techniques based on quorum sensing. In Applied Mechanics and Materials; Trans Tech Publications Ltd.: Zurich, Switzerland, 2013; Volume 295, pp. 39–44. [Google Scholar]
  35. Von Bodman, S.B.; Willey, J.M.; Diggle, S.P. Cell-cell communication in bacteria: United we stand. J. Bacterial. 2008, 190, 4377–4391. [Google Scholar] [CrossRef] [PubMed]
  36. Pascale, G.; Sauriol, F.; Benhamou, N.; Bélanger, R.R.; Paulitz, T.C. Novel butyrolactones with antifungal activity produced by Pseudomonas aureofaciens strain 63–28. J. Antibiot. 1997, 50, 742–749. [Google Scholar] [CrossRef] [PubMed]
  37. Holden, M.T.; Ram Chhabra, S.; De Nys, R.; Stead, P.; Bainton, N.J.; Hill, P.J.; Manefield, M.; Kumar, N.; Labatte, M.; England, D.; et al. Quorum-sensing cross talk: Isolation and chemical characterization of cyclic dipeptides from Pseudomonas aeruginosa and other gram-negative bacteria. Mol. Microbiol 1999, 33, 1254–1266. [Google Scholar] [CrossRef]
  38. Lee, J.H.; Lee, J. Indole as an intercellular signal in microbial communities. FEMS Micbiol. Rev. 2010, 34, 426–444. [Google Scholar] [CrossRef]
  39. Deng, Y.; Wu, J.E.; Tao, F.; Zhang, L.H. Listening to a new language: DSF-based quorum sensing in Gram-negative bacteria. Chem. Rev. 2011, 111, 160–173. [Google Scholar] [CrossRef]
  40. Wang, J.; Quan, C.; Wang, X.; Zhao, P.; Fan, S. Extraction, purification and identification of bacterial signal molecules based on N-acyl homoserine lactones. Microb. Biotechnol. 2011, 4, 479–490. [Google Scholar] [CrossRef]
  41. Watson, W.T.; Minogue, T.D.; Val, D.L.; Von Bodman, S.B.; Churchill, M.E. Structural basis and specificity of acyl-homoserine lactone signal production in bacterial quorum sensing. Mol. Cell 2002, 9, 685–694. [Google Scholar] [CrossRef]
  42. Parsek, M.R.; Greenberg, E.P. Acyl-homoserine lactone quorum sensing in gram-negative bacteria: A signaling mechanism involved in associations with higher organisms. Proc. Natl. Acad. Sci. USA 2000, 97, 8789–8793. [Google Scholar] [CrossRef] [PubMed]
  43. Kjelleberg, S.; Molin, S. Is there a role for quorum sensing signals in bacterial biofilms? Curr. Opin. Microbiol. 2002, 5, 254–258. [Google Scholar] [CrossRef]
  44. Mangwani, N.; Dash, H.R.; Chauhan, A.; Das, S. Bacterial quorum sensing: Functional features and potential applications in biotechnology. Microb. Physiol. 2012, 22, 215–227. [Google Scholar] [CrossRef] [PubMed]
  45. Biswa, P.; Doble, M. Production of acylated homoserine lactone by Gram-positive bacteria isolated from marine water. FEMS Microbiol. Lett. 2013, 343, 34–41. [Google Scholar] [CrossRef] [PubMed]
  46. Paliwal, V.; Puranik, S.; Purohit, H.J. Integrated perspective for effective bioremediation. Appl. Biochem. Biotechnol. 2012, 166, 903–924. [Google Scholar] [CrossRef]
  47. Dunny, G.M.; Leonard, B.A. Cell-cell communication in gram-positive bacteria. Annu. Rev. Microbiol. 1997, 51, 527. [Google Scholar] [CrossRef]
  48. Novick, R.P. Autoinduction and signal transduction in the regulation of staphylococcal virulence. Mol. Microbiol. 2003, 48, 1429–1449. [Google Scholar] [CrossRef]
  49. Williams, P. Quorum sensing, communication and cross-kingdom signalling in the bacterial world. Microbiology 2007, 153, 3923–3938. [Google Scholar] [CrossRef]
  50. Wuster, A.; Babu, M.M. Conservation and evolutionary dynamics of the agr cell-to-cell communication system across firmicutes. J. Bacterial. 2008, 190, 743–746. [Google Scholar] [CrossRef]
  51. Hegde, M.; Englert, D.L.; Schrock, S.; Cohn, W.B.; Vogt, C.; Wood, T.K.; Manson, M.D.; Jayaraman, A. Chemotaxis to the quorum-sensing signal AI-2 requires the Tsr chemoreceptor and the periplasmic LsrB AI-2-binding protein. J. Bacteriol 2011, 193, 768–773. [Google Scholar] [CrossRef]
  52. Henke, J.M.; Bassler, B.L. Three parallel quorum-sensing systems regulate gene expression in Vibrio harveyi. J. Bacteriol 2004, 186, 6902–6914. [Google Scholar] [CrossRef] [PubMed]
  53. Xavier, K.B.; Bassler, B.L. Interference with AI-2-mediated bacterial cell–cell communication. Nature 2005, 437, 750–753. [Google Scholar] [CrossRef] [PubMed] [Green Version]
  54. Shrout, J.D.; Nerenberg, R. Monitoring bacterial twitter: Does quorum sensing determine the behavior of water and wastewater treatment biofilms? Environ. Sci. Technol. 2012, 46, 1995–2005. [Google Scholar] [PubMed]
  55. Song, X.N.; Cheng, Y.Y.; Li, W.W.; Li, B.B.; Sheng, G.P.; Fang, C.Y.; Wang, Y.K.; Li, X.Y.; Yu, H.Q. Quorum quenching is responsible for the underestimated quorum sensing effects in biological wastewater treatment reactors. Bioresour. Technol. 2014, 171, 472–476. [Google Scholar] [CrossRef]
  56. Dobretsov, S.; Teplitski, M.; Paul, V. Mini-review: Quorum sensing in the marine environment and its relationship to biofouling. Biofouling 2009, 25, 413–427. [Google Scholar] [CrossRef]
  57. Escudié, R.; Cresson, R.; Delgenès, J.P.; Bernet, N. Control of start-up and operation of anaerobic biofilm reactors: An overview of 15 years of research. Water Res. 2011, 45, 1–10. [Google Scholar] [CrossRef]
  58. Hu, H.; He, J.; Liu, J.; Yu, H.; Tang, J.; Zhang, J. Role of N-acyl-homoserine lactone (AHL) based quorum sensing on biofilm formation on packing media in wastewater treatment process. RSC Adv. 2016, 6, 11128–11139. [Google Scholar] [CrossRef]
  59. Valle, A.; Bailey, M.J.; Whiteley, A.S.; Manefield, M. N-acyl-L-homoserine lactones (AHLs) affect microbial community composition and function in activated sludge. Environ. Microbiol. 2004, 6, 424–433. [Google Scholar] [CrossRef]
  60. Kang, Y.S.; Park, W. Contribution of quorum-sensing system to hexadecane degradation and biofilm formation in Acinetobacter sp. strain DR1. J. Appl. Microbiol. 2010, 109, 1650–1659. [Google Scholar] [CrossRef]
  61. Yong, Y.C.; Zhong, J.J. Regulation of aromatics biodegradation by rhl quorum sensing system through induction of catechol meta-cleavage pathway. Bioresour. Technol. 2013, 136, 761–765. [Google Scholar] [CrossRef]
  62. Chong, G.; Kimyon, O.; Rice, S.A.; Kjelleberg, S.; Manefield, M. The presence and role of bacterial quorum sensing in activated sludge. Microb. Biotechnol. 2012, 5, 621–633. [Google Scholar]
  63. Miran, W.; Jang, J.; Nawaz, M.; Shahzad, A.; Jeong, S.E.; Jeon, C.O.; Lee, D.S. Mixed sulfate-reducing bacteria-enriched microbial fuel cells for the treatment of wastewater containing copper. Chemosphere 2017, 189, 134–142. [Google Scholar]
  64. Cydzik-Kwiatkowska, A.; Zielińska, M. Microbial composition of biofilm treating wastewater rich in bisphenol A. J. Environ. Sci. Health Part A 2018, 53, 385–392. [Google Scholar]
  65. De Beer, D.M.; Botes, M.; Cloete, T.E. The microbial community of a biofilm contact reactor for the treatment of winery wastewater. J. Appl. Microbiol 2018, 124, 598–610. [Google Scholar]
  66. Morgan-Sagastume, F.; Boon, N.; Dobbelaere, S.; Defoirdt, T.; Verstraete, W. Production of acylated homoserine lactones by Aeromonas and Pseudomonas strains isolated from municipal activated sludge. Can. J. Microbiol. 2005, 51, 924–933. [Google Scholar]
  67. Liu, J.; Nguyen, D.; Paice, M. Aerobic granule formation in a sequencing batch reactor treating newsprint effluent under low phosphate conditions. Water Sci. Technol. 2010, 62, 2571–2578. [Google Scholar]
  68. De Clippeleir, H.; Defoirdt, T.; Vanhaecke, L.; Vlaeminck, S.E.; Carballa, M.; Verstraete, W.; Boon, N. Long-chain acylhomoserine lactones increase the anoxic ammonium oxidation rate in an OLAND biofilm. Appl. Microbiol. Biotechnol. 2011, 90, 1511–1519. [Google Scholar]
  69. Lade, H.; Paul, D.; Kweon, J.H. Isolation and molecular characterization of biofouling bacteria and profiling of quorum sensing signal molecules from membrane bioreactor activated sludge. Int. J. Mol. Sci. 2014, 15, 2255–2273. [Google Scholar]
  70. Li, Y.; Lv, J.; Zhong, C.; Hao, W.; Wang, Y.; Zhu, J. Performance and role of N-acyl-homoserine lactone (AHL)-based quorum sensing (QS) in aerobic granules. J. Environ. Sci. 2014, 26, 1615–1621. [Google Scholar]
  71. Cheong, W.S.; Lee, C.H.; Moon, Y.H.; Oh, H.S.; Kim, S.R.; Lee, S.H.; Lee, C.H.; Lee, J.K. Isolation and identification of indigenous quorum quenching bacteria, Pseudomonas sp. 1A1, for biofouling control in MBR. Ind. Eng. Chem. Res. 2013, 52, 10554–10560. [Google Scholar]
  72. Oh, H.S.; Kim, S.R.; Cheong, W.S.; Lee, C.H.; Lee, J.K. Biofouling inhibition in MBR by Rhodococcus sp. BH4 isolated from real MBR plant. Appl. Microbiol. Biotechnol. 2013, 97, 10223–10231. [Google Scholar]
  73. Yong, Y.C.; Zhong, J.J. Impacts of quorum sensing on microbial metabolism and human health. Future Trends Biotechnol. 2012, 131, 25–61. [Google Scholar]
  74. Eberl, L.; Winson, M.K.; Sternberg, C.; Stewart, G.S.; Christiansen, G.; Chhabra, S.R.; Bycroft, B.; Williams, P.; Molin, S.; Givskov, M. Involvement of N-acyl-l-homoserine lactone autoinducers in controlling the multicellular behaviour of Serratia liquefaciens. Mol. Microbiol. 1996, 20, 127–136. [Google Scholar]
  75. Davies, D.G.; Parsek, M.R.; Pearson, J.P.; Iglewski, B.H.; Costerton, J.W.; Greenberg, E.P. The involvement of cell-to-cell signals in the development of a bacterial biofilm. Science 1998, 280, 295–298. [Google Scholar]
  76. Lynch, M.J.; Swift, S.; Kirke, D.F.; Keevil, C.W.; Dodd, C.E.; Williams, P. The regulation of biofilm development by quorum sensing in Aeromonas hydrophila. Environ. Microbiol. 2002, 4, 18–28. [Google Scholar]
  77. Labbate, M.; Queck, S.Y.; Koh, K.S.; Rice, S.A.; Givskov, M.; Kjelleberg, S. Quorum sensing-controlled biofilm development in Serratia liquefaciens MG1. J. Bacteriol. 2004, 186, 692–698. [Google Scholar]
  78. Parsek, M.R.; Greenberg, E.P. Sociomicrobiology: The connections between quorum sensing and biofilms. Trends Microbiol. 2005, 13, 27–33. [Google Scholar]
  79. Ren, T.T.; Yu, H.Q.; Li, X.Y. The quorum-sensing effect of aerobic granules on bacterial adhesion, biofilm formation, and sludge granulation. Appl. Microbiol. Biotechnol. 2010, 88, 789–797. [Google Scholar]
  80. Tan, C.H.; Koh, K.S.; Xie, C.; Tay, M.; Zhou, Y.; Williams, R.; Ng, W.J.; Rice, S.A.; Kjelleberg, S. The role of quorum sensing signalling in EPS production and the assembly of a sludge community into aerobic granules. ISME J. 2014, 8, 1186–1197. [Google Scholar]
  81. Yong, Y.C.; Zhong, J.J. N-acylated homoserine lactone production and involvement in the biodegradation of aromatics by an environmental isolate of Pseudomonas Aeruginosa. Process Biochem. 2010, 45, 1944–1948. [Google Scholar]
  82. Toyofuku, M.; Nomura, N.; Fujii, T.; Takaya, N.; Maseda, H.; Sawada, I.; Nakajima, T.; Uchiyama, H. Quorum sensing regulates denitrification in Pseudomonas aeruginosa PAO1. J. Bacteriol. 2007, 189, 4969–4972. [Google Scholar]
  83. Jørgensen, K.S.; Pauli, A.S.L. Polyphosphate accumulation among denitrifying bacteria in activated sludge. Anaerobe 1995, 1, 161–168. [Google Scholar] [CrossRef]
  84. Enya, J.; Shinohara, H.; Yoshida, S.; Tsukiboshi, T.; Negishi, H.; Suyama, K.; Tsushima, S. Culturable leaf-associated bacteria on tomato plants and their potential as biological control agents. Microbial. Ecol. 2007, 53, 524–536. [Google Scholar]
  85. Matsumiya, Y.; Wakita, D.; Kimura, A.; Sanpa, S.; Kubo, M. Isolation and characterization of a lipid-degrading bacterium and its application to lipid-containing wastewater treatment. J. Biosci Bioeng. 2007, 103, 325–330. [Google Scholar]
  86. Wattanaphon, H.T.; Kerdsin, A.; Thammacharoen, C.; Sangvanich, P.; Vangnai, A.S. A biosurfactant from Burkholderia cenocepacia BSP3 and its enhancement of pesticide solubilization. J. Appl. Microbiol. 2008, 105, 416–423. [Google Scholar]
  87. Chugani, S.; Greenberg, E.P. LuxR homolog-independent gene regulation by acyl-homoserine lactones in Pseudomonas aeruginosa. Proc. Natl. Acad. Sci. USA 2010, 107, 10673–10678. [Google Scholar]
  88. Hu, H.; Luo, F.; Liu, Y.; Zeng, X. Function of quorum sensing and cell signaling in wastewater treatment systems. Water Sci. Technol 2021, 83, 515–531. [Google Scholar]
  89. Niu, C.; Clemmer, K.M.; Bonomo, R.A.; Rather, P.N. Isolation and characterization of an autoinducer synthase from Acinetobacter baumannii. J. Bacteriol. 2008, 190, 3386–3392. [Google Scholar]
  90. Gaddy, J.A.; Actis, L.A. Regulation of Acinetobacter baumannii biofilm formation. Future Microbiol. 2009, 4, 273–278. [Google Scholar]
  91. Clemmer, K.M.; Bonomo, R.A.; Rather, P.N. Genetic analysis of surface motility in Acinetobacter baumannii. Microbiology 2011, 157, 2534. [Google Scholar]
  92. Juretschko, S.; Loy, A.; Lehner, A.; Wagner, M. The microbial community composition of a nitrifying-denitrifying activated sludge from an industrial sewage treatment plant analyzed by the full-cycle rRNA approach. Syst. Appl. Microbiol. 2002, 25, 84–99. [Google Scholar] [CrossRef] [PubMed]
  93. Burton, E.O.; Read, H.W.; Pellitteri, M.C.; Hickey, W. Identification of acyl-homoserine lactone signal molecules produced by Nitrosomonas europaea strain Schmidt. Appl. Environ. Microbiol. 2005, 71, 4906–4909. [Google Scholar] [CrossRef] [PubMed]
  94. Huang, J.; Shi, Y.; Zeng, G.; Gu, Y.; Chen, G.; Shi, L.; Hu, Y.; Tang, B.; Zhou, J. Acyl-homoserine lactone-based quorum sensing and quorum quenching hold promise to determine the performance of biological wastewater treatments: An overview. Chemosphere 2016, 157, 137–151. [Google Scholar] [CrossRef] [PubMed]
  95. Leadbetter, J.R.; Greenberg, E.P. Metabolism of acyl-homoserine lactone quorum-sensing signals by Variovorax paradoxus. J. Bacteriol. 2000, 182, 6921–6926. [Google Scholar] [CrossRef] [PubMed]
  96. Huang, J.J.; Han, J.I.; Zhang, L.H.; Leadbetter, J.R. Utilization of acyl-homoserine lactone quorum signals for growth by a soil pseudomonad and Pseudomonas aeruginosa PAO1. Appl. Environ. Microbiol. 2003, 69, 5941–5949. [Google Scholar] [CrossRef]
  97. Oh, H.S.; Yeon, K.M.; Yang, C.S.; Kim, S.R.; Lee, C.H.; Park, S.Y.; Han, J.Y.; Lee, J.K. Control of membrane biofouling in MBR for wastewater treatment by quorum quenching bacteria encapsulated in microporous membrane. Environ. Sci. Technol. 2012, 46, 4877–4884. [Google Scholar] [CrossRef] [PubMed]
  98. Kim, S.R.; Oh, H.S.; Jo, S.J.; Yeon, K.M.; Lee, C.H.; Lim, D.J.; Lee, C.H.; Lee, J.K. Biofouling control with bead-entrapped quorum quenching bacteria in membrane bioreactors: Physical and biological effects. Env. Sci. Technol. 2013, 47, 836–842. [Google Scholar] [CrossRef]
  99. Ouyang, Y.; Hu, Y.; Huang, J.; Gu, Y.; Shi, Y.; Yi, K.; Yang, Y. Effects of exogenous quorum quenching on microbial community dynamics and biofouling propensity of activated sludge in MBRs. Biochem. Eng. J. 2020, 157, 107534. [Google Scholar] [CrossRef]
  100. Kim, S.R.; Lee, K.B.; Kim, J.E.; Won, Y.J.; Yeon, K.M.; Lee, C.H.; Lim, D.J. Macroencapsulation of quorum quenching bacteria by polymeric membrane layer and its application to MBR for biofouling control. J. Membr. Sci. 2015, 473, 109–117. [Google Scholar] [CrossRef]
  101. Cheong, W.S.; Kim, S.R.; Oh, H.S.; Lee, S.H.; Yeon, K.M.; Lee, C.H.; Lee, J.K. Design of quorum quenching microbial vessel to enhance cell viability for biofouling control in membrane bioreactor. J. Microbiol. Biotechnol. 2014, 24, 97–105. [Google Scholar] [CrossRef]
  102. Ochiai, S.; Morohoshi, T.; Kurabeishi, A.; Shinozaki, M.; Fujita, H.; Sawada, I.; Ikeda, T. Production and degradation of N-acylhomoserine lactone quorum sensing signal molecules in bacteria isolated from activated sludge. Biosci. Biotechnol. Biochem. 2013, 77, 2436–2440. [Google Scholar] [CrossRef] [PubMed] [Green Version]
  103. Siddiqui, M.F.; Rzechowicz, M.; Harvey, W.; Zularisam, A.W.; Anthony, G.F. Quorum sensing based membrane biofouling control for water treatment: A review. J. Water Process. Eng. 2015, 7, 112–122. [Google Scholar] [CrossRef]
  104. Ponnusamy, K.; Paul, D.; Kim, Y.S.; Kweon, J.H. 2(5H)-Furanone: A prospective strategy for biofouling-control in membrane biofilm bacteria by quorum sensing inhibition. Braz. J. Microbiol. 2010, 41, 227–234. [Google Scholar] [CrossRef]
  105. Kim, S.; Lee, S.; Hong, S.; Oh, Y.; Kweon, J.; Kim, T. Biofouling of reverse osmosis membranes: Microbial quorum sensing and fouling propensity. Desalination 2009, 247, 303–315. [Google Scholar] [CrossRef]
  106. Yeon, K.M.; Cheong, W.S.; Oh, H.S.; Lee, W.N.; Hwang, B.K.; Lee, C.H.; Beyenal, H.; Lewandowski, Z. Quorum sensing: A new biofouling control paradigm in a membrane bioreactor for advanced wastewater treatment. Environ. Sci. Technol. 2008, 43, 380–385. [Google Scholar] [CrossRef]
  107. Kumari, A.; Pasini, P.; Daunert, S. Detection of bacterial quorum sensing N-acyl homoserine lactones in clinical samples. Anal. Bioanal. Chem. 2008, 391, 1619–1627. [Google Scholar] [CrossRef]
  108. Huang, S.; Zhang, H.; Ng, T.C.A.; Xu, B.; Shi, X.; Ng, H.Y. Analysis of N-Acy-L-homoserine lactones (AHLs) in wastewater treatment systems using SPE-LLE with LC-MS/MS. Water Res. 2020, 177, 115756. [Google Scholar] [CrossRef]
  109. Rothballer, M.; Uhl, J.; Kunze, J.; Schmitt-Kopplin, P.; Hartmann, A. Detection of the bacterial quorum-sensing signaling molecules N-acyl-homoserine lactones (HSL) and N-acyl-homoserine (HS) with an enzyme-linked immunosorbent assay (ELISA) and via ultrahigh-performance liquid chromatography coupled to mass spectrometry (UHPLC-MS). In Quorum Sensing; Humana Press: New York, NY, USA, 2018; pp. 61–72. [Google Scholar]
  110. Wang, J.; Ding, L.; Li, K.; Schmieder, W.; Geng, J.; Xu, K.; Zhang, Y.; Ren, H. Development of an extraction method and LC–MS analysis for N-acylated-l-homoserine lactones (AHLs) in wastewater treatment biofilms. J. Chromatogr. B 2017, 1041, 37–44. [Google Scholar] [CrossRef]
  111. Neumann, A.; Patzelt, D.; Wagner-Döbler, I.; Schulz, S. Identification of new N-acylhomoserine lactone signalling compounds of Dinoroseobacter shibae DFL-12T by overexpression of luxi genes. ChemBioChem 2013, 14, 2355–2361. [Google Scholar] [CrossRef]
  112. Maddela, N.R.; Sheng, B.; Yuan, S.; Zhou, Z.; Villamar-Torres, R.; Meng, F. Roles of quorum sensing in biological wastewater treatment: A critical review. Chemosphere 2019, 221, 616–629. [Google Scholar] [CrossRef]
  113. Liu, W.; Cai, W.; Ma, A.; Ren, G.; Li, Z.; Zhuang, G.; Wang, A. Improvement of bioelectrochemical property and energy recovery by acylhomoserine lactones (AHLs) in microbial electrolysis cells (MECs). J. Power Source 2015, 284, 56–59. [Google Scholar] [CrossRef]
  114. Peng, P.; Huang, H.; Ren, H.; Ma, H.; Lin, Y.; Geng, J.; Xu, K.; Zhang, Y.; Ding, L. Exogenous N-acyl homoserine lactones facilitate microbial adhesion of high ammonia nitrogen wastewater on biocarrier surfaces. Sci. Total Environ. 2018, 624, 1013–1022. [Google Scholar] [CrossRef] [PubMed]
  115. Liu, L.; Ji, M.; Wang, F.; Tian, Z.; Wang, T.; Wang, S.; Wang, S.; Yan, Z. Insight into the short-term effect of fulvic acid on nitrogen removal performance and N-acylated-L-homoserine lactones (AHLs) release in the anammox system. Sci. Total Environ. 2020, 704, 135285. [Google Scholar] [CrossRef] [PubMed]
  116. Sun, J. Study on Quorum Sensing of Biofilm Treatment in Aquaculture Wastewater. Ph.D. Thesis, Ocean University of China, Qingdao, China, 2012. [Google Scholar]
  117. Sun, Z.; Xi, J.; Yang, C.; Cong, W. Quorum sensing regulation methods and their effects on biofilm in biological waste treatment systems: A review. Front. Environ. Sci. Eng. 2022, 16, 87. [Google Scholar] [CrossRef]
  118. Zaitseva, Y.V.; Popova, A.A.; Khmel, I.A. Quorum sensing regulation in bacteria of the family Enterobacteriaceae. Russ. J. Genet. 2014, 50, 323–340. [Google Scholar] [CrossRef]
  119. Remuzgo-Martínez, S.; Lázaro-Díez, M.; Mayer, C.; Aranzamendi-Zaldumbide, M.; Padilla, D.; Calvo, J.; Marco, F.; Martínez-Martínez, L.; Icardo, J.M.; Otero, A.; et al. Biofilm formation and quorum-sensing-molecule production by clinical isolates of Serratia liquefaciens. Appl. Environ. Microbiol. 2015, 81, 3306–3315. [Google Scholar] [CrossRef]
  120. Guan, J.; Xiao, X.; Xu, S.; Gao, F.; Wang, J.; Wang, T.; Song, Y.; Pan, J.; Shen, X.; Wang, Y. Roles of RpoS in Yersinia pseudotuberculosis stress survival, motility, biofilm formation and type VI secretion system expression. J. Microbiol. 2015, 53, 633–642. [Google Scholar] [CrossRef]
  121. Wiechmann, A. Quorum Sensing and the Regulation of Multicellular Behaviour in Yersinia pseudotuberculosis. Ph.D. Thesis, University of Nottingham, Nottingham, UK, 2016. [Google Scholar]
  122. Ganesh, P.S.; Vishnupriya, S.; Vadivelu, J.; Mariappan, V.; Vellasamy, K.M.; Shankar, E.M. Intracellular survival and innate immune evasion of Burkholderia cepacia: Improved understanding of quorum sensing-controlled virulence factors, biofilm, and inhibitors. Microbiol. Immunol 2020, 64, 87–98. [Google Scholar] [CrossRef]
  123. Llamas, I.; Quesada, E.; Martínez-Cánovas, M.J.; Gronquist, M.; Eberhard, A.; Gonzalez, J.E. Quorum sensing in halophilic bacteria: Detection of N-acyl-homoserine lactones in the exopolysaccharide-producing species of Halomonas. Extremophiles 2005, 9, 333–341. [Google Scholar] [CrossRef]
  124. Ji, G.; Pei, W.; Zhang, L.; Qiu, R.; Lin, J.; Benito, Y.; Lina, G.; Novick, R.P. Staphylococcus intermedius produces a functional agr autoinducing peptide containing a cyclic lactone. J. Bacteriol. 2005, 187, 3139–3150. [Google Scholar] [CrossRef]
  125. Mashburn-Warren, L.; Morrison, D.A.; Federle, M.J. A novel double-tryptophan peptide pheromone controls competence in Streptococcus spp. via an Rgg regulator. Mol. Microbiol. 2010, 78, 589–606. [Google Scholar] [CrossRef] [PubMed] [Green Version]
  126. Shanker, E.; Federle, M.J. Quorum sensing regulation of competence and bacteriocins in Streptococcus pneumoniae and mutans. Genes 2017, 8, 15. [Google Scholar] [CrossRef] [PubMed]
  127. Fujii, T.; Ingham, C.; Nakayama, J.; Beerthuyzen, M.; Kunuki, R.; Molenaar, D.; Sturme, M.; Vaughan, E.; Kleerebezem, M.; De Vos, W. Two homologous Agr-like quorum-sensing systems cooperatively control adherence, cell morphology, and cell viability properties in Lactobacillus plantarum WCFS1. J. Bacteriol. 2008, 190, 7655–7665. [Google Scholar] [CrossRef]
  128. Rizzello, C.G.; Filannino, P.; Di Cagno, R.; Calasso, M.; Gobbetti, M. Quorum-sensing regulation of constitutive plantaricin by Lactobacillus plantarum strains under a model system for vegetables and fruits. Appl. Environ. Microbiol. 2014, 80, 777–787. [Google Scholar] [CrossRef] [PubMed]
  129. Zhang, J.; Li, J.; Zhao, B.H.; Zhang, Y.C.; Wang, X.J.; Chen, G.H. Long-term effects of N-acyl-homoserine lactone-based quorum sensing on the characteristics of ANAMMOX granules in high-loaded reactors. Chemosphere 2019, 218, 632–642. [Google Scholar] [CrossRef]
  130. Huang, H.; Fan, X.; Peng, P.; Peng, C.; Gao, Y.; Zhang, X.; Ren, H. Two birds with one stone: Simultaneous improvement of biofilm formation and nitrogen transformation in MBBR treating high ammonia nitrogen wastewater via exogenous N-acyl homoserine lactones. Chem. Eng. J. 2020, 386, 124001. [Google Scholar] [CrossRef]
  131. Monzon, O.; Yang, Y.; Li, Q.; Alvarez, P.J. Quorum sensing autoinducers enhance biofilm formation and power production in a hypersaline microbial fuel cell. Biochem. Eng. J. 2016, 109, 222–227. [Google Scholar] [CrossRef]
  132. Soler, A.; Arregui, L.; Arroyo, M.; Mendoza, J.A.; Muras, A.; Álvarez, C.; García-Vera, C.; Marquina, D.; Santos, A.; Serrano, S. Quorum sensing versus quenching bacterial isolates obtained from MBR plants treating leachates from municipal solid waste. Int. J. Environ. Health Res. 2018, 15, 1019. [Google Scholar] [CrossRef]
  133. Chen, X.; Schauder, S.; Potier, N.; Van Dorsselaer, A.; Pelczer, I.; Bassler, B.L.; Hughson, F.M. Structural identification of a bacterial quorum-sensing signal containing boron. Nature 2002, 415, 545–549. [Google Scholar] [CrossRef]
  134. Cevik, E.; Tombuloglu, H.; Anıl, I.; Senel, M.; Sabit, H.; AbdulAzeez, S.; Borgio, J.F.; Barghouthi, M. Direct electricity production from Microalgae Choricystis sp. and investigation of the boron to enhance the electrogenic activity. Int. J. Hydrogen Energy 2020, 45, 11330–11340. [Google Scholar] [CrossRef]
  135. Zhang, B.; Li, W.; Guo, Y.; Zhang, Z.; Shi, W.; Cui, F.; Lens, P.N.; Tay, J.H. A sustainable strategy for effective regulation of aerobic granulation: Augmentation of the signaling molecule content by cultivating AHL-producing strains. Water Res. 2020, 169, 115193. [Google Scholar] [CrossRef]
  136. Wang, J.; Liu, Q.; Ma, S.; Hu, H.; Wu, B.; Zhang, X.X.; Ren, H. Distribution characteristics of N-acyl homoserine lactones during the moving bed biofilm reactor biofilm development process: Effect of carbon/nitrogen ratio and exogenous quorum sensing signals. Bioresour. Technol. 2019, 289, 121591. [Google Scholar] [CrossRef]
  137. Gao, M.; Liu, Y.; Liu, Z.; Li, H.; Zhang, A. Strengthening of aerobic sludge granulation by the endogenous acylated homoserine lactones-secreting strain Aeromonas sp. A-L3. Biochem. Eng. J. 2019, 151, 107329. [Google Scholar] [CrossRef]
  138. Yates, E.A.; Philipp, B.; Buckley, C.; Atkinson, S.; Chhabra, S.R.; Sockett, R.E.; Goldner, M.; Dessaux, Y.; Cámara, M.; Smith, H.; et al. N-acylhomoserine lactones undergo lactonolysis in a pH-, temperature-, and acyl chain length-dependent manner during growth of Yersinia pseudotuberculosis and Pseudomonas Aeruginosa. Infect. Immun. 2002, 70, 5635–5646. [Google Scholar] [CrossRef]
  139. Teplitski, M.; Mathesius, U.; Rumbaugh, K.P. Perception and degradation of N-acyl homoserine lactone quorum sensing signals by mammalian and plant cells. Chem. Rev. 2011, 111, 100–116. [Google Scholar] [CrossRef]
  140. Kalia, V.C. Quorum sensing inhibitors: An overview. Biotechnol. Adv. 2013, 31, 224–245. [Google Scholar] [CrossRef]
  141. Al-Shabib, N.A.; Husain, F.M.; Rehman, M.T.; Alyousef, A.A.; Arshad, M.; Khan, A.; Khan, J.M.; Alam, P.; Albalawi, T.A.; Shahzad, S.A.; et al. Food color ‘Azorubine’interferes with quorum sensing regulated functions and obliterates biofilm formed by food associated bacteria: An in vitro and in silico approach. Saudi. J. Biol. Sci 2020, 27, 1080–1090. [Google Scholar] [CrossRef]
  142. Alibi, S.; Selma, W.B.; Ramos-Vivas, J.; Smach, M.A.; Touati, R.; Boukadida, J.; Navas, J.; Mansour, H.B. Anti-oxidant, antibacterial, anti-biofilm, and anti-quorum sensing activities of four essential oils against multidrug-resistant bacterial clinical isolates. Curr. Res.Transl. Med. 2020, 68, 59–66. [Google Scholar] [CrossRef]
  143. Brown, M.M.; Kwiecinski, J.M.; Cruz, L.M.; Shahbandi, A.; Todd, D.A.; Cech, N.B.; Horswill, A.R. Novel peptide from commensal Staphylococcus simulans blocks methicillin-resistant Staphylococcus aureus quorum sensing and protects host skin from damage. Antimicrob. Agents Chemother. 2020, 64, e00172-20. [Google Scholar] [CrossRef]
  144. Cheng, W.J.; Zhou, J.W.; Zhang, P.P.; Luo, H.Z.; Tang, S.; Li, J.J.; Deng, S.M.; Jia, A.Q. Quorum sensing inhibition and tobramycin acceleration in Chromobacterium violaceum by two natural cinnamic acid derivatives. Appl. Microbiol. Biotechnol. 2020, 104, 5025–5037. [Google Scholar] [CrossRef]
  145. Di Marco, N.I.; Pungitore, C.R.; Lucero-Estrada, C.S.M. Aporphinoid alkaloids inhibit biofilm formation of Yersinia enterocolitica isolated from sausages. J. Appl. Microbiol. 2020, 129, 1029–1042. [Google Scholar] [CrossRef]
  146. Li, T.; Sun, X.; Chen, H.; He, B.; Mei, Y.; Wang, D.; Li, J. Methyl anthranilate: A novel quorum sensing inhibitor and anti-biofilm agent against Aeromonas sobria. Food. Microbiol. 2020, 86, 103356. [Google Scholar] [CrossRef]
  147. Parmar, P.; Shukla, A.; Rao, P.; Saraf, M.; Patel, B.; Goswami, D. The rise of gingerol as anti-QS molecule: Darkest episode in the LuxR-mediated bioluminescence saga. Bioorg. Chem. 2020, 99, 103823. [Google Scholar] [CrossRef]
  148. Qin, X.; Thota, G.K.; Singh, R.; Balamurugan, R.; Goycoolea, F.M. Synthetic homoserine lactone analogues as antagonists of bacterial quorum sensing. Bioorg. Chem. 2020, 98, 103698. [Google Scholar] [CrossRef]
  149. Shen, C.; Islam, M.T.; Masuda, Y.; Honjoh, K.I.; Miyamoto, T. Transcriptional changes involved in inhibition of biofilm formation by ε-polylysine in Salmonella Typhimurium. Appl. Microbiol. Biotechnol. 2020, 104, 5427–5436. [Google Scholar] [CrossRef]
  150. Wang, M.; Zhao, L.; Wu, H.; Zhao, C.; Gong, Q.; Yu, W. Cladodionen is a potential quorum sensing inhibitor against Pseudomonas aeruginosa. Mar. Drugs 2020, 18, 205. [Google Scholar] [CrossRef]
  151. Chen, B.; Peng, M.; Tong, W.; Zhang, Q.; Song, Z. The quorum quenching bacterium Bacillus licheniformis T-1 protects zebrafish against Aeromonas hydrophila infection. Probiotics Antimicrob. Proteins 2020, 12, 160–171. [Google Scholar] [CrossRef]
  152. Maddela, N.R.; Meng, F. Discrepant roles of a quorum quenching bacterium (Rhodococcus sp. BH4) in growing dual-species biofilms. Sci. Total Environ. 2020, 713, 136402. [Google Scholar] [CrossRef]
  153. Wang, H.; Liao, L.; Chen, S.; Zhang, L.H. A quorum quenching bacterial isolate contains multiple substrate-inducible genes conferring degradation of diffusible signal factor. Appl. Environ. Microbiol. 2020, 86, e02930-19. [Google Scholar] [CrossRef]
  154. Fakhri, H.; Shahi, A.; Ovez, S.; Aydin, S. Bioaugmentation with immobilized endophytic Penicillium restrictum to improve quorum quenching activity for biofouling control in an aerobic hollow-fiber membrane bioreactor treating antibiotic-containing wastewater. Ecotoxicol. Environ. Saf 2021, 210, 111831. [Google Scholar] [CrossRef]
  155. Oh, H.S.; Lee, C.H. Origin and evolution of quorum quenching technology for biofouling control in MBRs for wastewater treatment. J. Membr. Sci. 2018, 554, 331–345. [Google Scholar] [CrossRef]
  156. Oh, H.S.; Tan, C.H.; Low, J.H.; Rzechowicz, M.; Siddiqui, M.F.; Winters, H.; Kjelleberg, S.; Fane, A.G.; Rice, S.A. Quorum quenching bacteria can be used to inhibit the biofouling of reverse osmosis membranes. Water Res. 2017, 112, 29–37. [Google Scholar] [CrossRef]
  157. Gül, B.Y.; Koyuncu, I. Assessment of new environmental quorum quenching bacteria as a solution for membrane biofouling. Process Biochem. 2017, 61, 137–146. [Google Scholar]
  158. Lee, K.; Yu, H.; Zhang, X.; Choo, K.H. Quorum sensing and quenching in membrane bioreactors: Opportunities and challenges for biofouling control. Bioresour. Technol. 2018, 270, 656–668. [Google Scholar]
  159. Zhang, X.; Lee, K.; Yu, H.; Mameda, N.; Choo, K.H. Photolytic quorum quenching: A new anti-biofouling strategy for membrane bioreactors. J. Chem. Eng. 2019, 378, 122235. [Google Scholar] [CrossRef]
  160. Xiao, X.; Zhu, W.W.; Liu, Q.Y.; Yuan, H.; Li, W.W.; Wu, L.J.; Li, Q.; Yu, H.Q. Impairment of biofilm formation by TiO2 photocatalysis through quorum quenching. Environ. Sci. Technol. 2016, 50, 11895–11902. [Google Scholar] [CrossRef]
  161. Mehmood, C.T.; Waheed, H.; Tan, W.; Xiao, Y. Photocatalytic quorum quenching: A new antifouling and in-situ membrane cleaning strategy for an external membrane bioreactor coupled to UASB. J. Environ. Chem. Eng. 2021, 9, 105470. [Google Scholar] [CrossRef]
  162. Jiang, W.; Xia, S.; Liang, J.; Zhang, Z.; Hermanowicz, S.W. Effect of quorum quenching on the reactor performance, biofouling and biomass characteristics in membrane bioreactors. Water Res. 2013, 47, 187–196. [Google Scholar] [CrossRef]
  163. Romero, M.; Martin-Cuadrado, A.B.; Roca-Rivada, A.; Cabello, A.M.; Otero, A. Quorum quenching in cultivable bacteria from dense marine coastal microbial communities. FEMS Microbiol. Ecol. 2011, 75, 205–217. [Google Scholar] [CrossRef]
  164. Chowdhary, P.K.; Keshavan, N.; Nguyen, H.Q.; Peterson, J.A.; González, J.E.; Haines, D.C. Bacillus megaterium CYP102A1 oxidation of acyl homoserine lactones and acyl homoserines. Biochemistry 2007, 46, 14429–14437. [Google Scholar] [CrossRef]
  165. Roy, V.; Fernandes, R.; Tsao, C.Y.; Bentley, W.E. Cross species quorum quenching using a native AI-2 processing enzyme. ACS Chem. Biol. 2010, 5, 223–232. [Google Scholar] [CrossRef]
  166. Cho, K.W.; Lee, H.S.; Rho, J.R.; Kim, T.S.; Mo, S.J.; Shin, J. New lactone-containing metabolites from a marine-derived bacterium of the genus Streptomyces. J. Nat. Prod. 2001, 64, 664–667. [Google Scholar]
  167. Chan, K.G.; Atkinson, S.; Mathee, K.; Sam, C.K.; Chhabra, S.R.; Cámara, M.; Koh, C.L.; Williams, P. Characterization of N-acylhomoserine lactone-degrading bacteria associated with the Zingiber officinale (ginger) rhizosphere: Co-existence of quorum quenching and quorum sensing in Acinetobacter and Burkholderia. BMC Microbiol. 2011, 11, 51. [Google Scholar]
  168. Visvanathan, C.; Aim, R.B.; Parameshwaran, K. Membrane separation bioreactors for wastewater treatment. Crit. Rev. Env. Sci. Technol. 2000, 30, 1–48. [Google Scholar]
  169. Miura, Y.; Watanabe, Y.; Okabe, S. Membrane biofouling in pilot-scale membrane bioreactors (MBRs) treating municipal wastewater: Impact of biofilm formation. Environ. Sci. Technol. 2007, 41, 632–638. [Google Scholar]
  170. Mahendran, B.; Lin, H.; Liao, B.; Liss, S.N. Surface properties of biofouled membranes from a submerged anaerobic membrane bioreactor after cleaning. J. Environ. Eng. 2011, 137, 504–513. [Google Scholar]
  171. Guo, W.; Ngo, H.H.; Li, J. A mini-review on membrane fouling. Bioresour. Technol. 2012, 122, 27–34. [Google Scholar]
  172. Malaeb, L.; Le-Clech, P.; Vrouwenvelder, J.S.; Ayoub, G.M.; Saikaly, P.E. Do biological-based strategies hold promise to biofouling control in MBRs? Water Res. 2013, 47, 5447–5463. [Google Scholar]
  173. Liu, C.X.; Zhang, D.R.; He, Y.; Zhao, X.S.; Bai, R. Modification of membrane surface for anti-biofouling performance: Effect of anti-adhesion and anti-bacteria approaches. J. Membr. Sci. 2010, 346, 121–130. [Google Scholar]
  174. Stuckey, D.C. Recent developments in anaerobic membrane reactors. Bioresour. Technol. 2012, 122, 137–148. [Google Scholar]
  175. Ren, T.T.; Li, X.Y.; Yu, H.Q. Effect of N-acy-l-homoserine lactones-like molecules from aerobic granules on biofilm formation by Escherichia coli K12. Bioresour. Technol. 2013, 129, 655–658. [Google Scholar]
  176. Kim, H.W.; Oh, H.S.; Kim, S.R.; Lee, K.B.; Yeon, K.M.; Lee, C.H.; Kim, S.; Lee, J.K. Microbial population dynamics and proteomics in membrane bioreactors with enzymatic quorum quenching. Appl. Microbiol. Biotechnol. 2013, 97, 4665–4675. [Google Scholar]
  177. Kim, M.; Lee, S.; Park, H.D.; Choi, S.I.; Hong, S. Biofouling control by quorum sensing inhibition and its dependence on membrane surface. Water Sci. Technol. 2012, 66, 1424–1430. [Google Scholar] [CrossRef]
  178. Lade, H.; Paul, D.; Kweon, J.H. Quorum quenching mediated approaches for control of membrane biofouling. Int. J. Biol. Sci. 2014, 10, 550. [Google Scholar] [CrossRef]
  179. Xu, H.; Liu, Y. Control and cleaning of membrane biofouling by energy uncoupling and cellular communication. Environ. Sci. Technol. 2011, 45, 595–601. [Google Scholar]
  180. Huang, J.H.; Guo, S.H.; Zeng, G.M.; Xiong, Y.L.; Zhang, D.M.; Tang, X.J.; Xie, G.X. Prediction of fouling resistance and permeate flux in cross-flow micellar-enhanced ultrafiltration (MEUF). Colloids Surf. A Physicochem. Eng. Asp. 2012, 401, 81–89. [Google Scholar]
  181. Huang, J.; Liu, L.; Zeng, G.; Li, X.; Peng, L.; Li, F.; Jiang, Y.; Zhao, Y.; Huang, X. Influence of feed concentration and transmembrane pressure on membrane fouling and effect of hydraulic flushing on the performance of ultrafiltration. Desalination 2014, 335, 1–8. [Google Scholar]
  182. Huang, J.; Peng, L.; Zeng, G.; Li, X.; Zhao, Y.; Liu, L.; Li, F.; Chai, Q. Evaluation of micellar enhanced ultrafiltration for removing methylene blue and cadmium ion simultaneously with mixed surfactants. Sep. Purif. Technol. 2014, 125, 83–89. [Google Scholar] [CrossRef]
  183. Jeong, S.; Rice, S.A.; Vigneswaran, S. Long-term effect on membrane fouling in a new membrane bioreactor as a pretreatment to seawater desalination. Bioresour. Technol. 2014, 165, 60–68. [Google Scholar]
  184. Liang, S.; Xiao, K.; Wu, J.; Liang, P.; Huang, X. Mechanism of membrane filterability amelioration via tuning mixed liquor property by pre-ozonation. J. Membr. Sci. 2014, 454, 111–118. [Google Scholar]
  185. Davies, D. Understanding biofilm resistance to antibacterial agents. Nat. Rev. Drug Discov. 2003, 2, 114–122. [Google Scholar] [PubMed]
  186. Hook, A.L.; Chang, C.Y.; Yang, J.; Luckett, J.; Cockayne, A.; Atkinson, S.; Mei, Y.; Bayston, R.; Irvine, D.J.; Langer, R.; et al. Combinatorial discovery of polymers resistant to bacterial attachment. Nat. Biotechnol. 2012, 30, 868–875. [Google Scholar]
  187. Li, M.Y.; Lu, P.; Zhang, J.; Xu, J.L.; Li, S.P. Isolation and biofilm forming capacity of quorum sensing factor bacterium. China Environ.Sci. 2007, 27, 194–198. [Google Scholar]
  188. Alvarino, T.; Torregrosa, N.; Omil, F.; Lema, J.M.; Suarez, S. Assessing the feasibility of two hybrid MBR systems using PAC for removing macro and micropollutants. J. Environ. Manag. 2017, 203, 831–837. [Google Scholar]
  189. Asif, M.B.; Ren, B.; Li, C.; Maqbool, T.; Zhang, X.; Zhang, Z. Powdered activated carbon–membrane bioreactor (PAC-MBR): Impacts of high PAC concentration on micropollutant removal and microbial communities. Sci. Total Environ. 2020, 745, 141090. [Google Scholar]
  190. Khan, S.J.; Ahmad, A.; Nawaz, M.S.; Hankins, N.P. Membrane fouling and performance evaluation of conventional membrane bioreactor (MBR), moving biofilm MBR and oxic/anoxic MBR. Water Sci. Technol. 2014, 69, 1403–1409. [Google Scholar]
  191. Radnia, H.; Ghoreyshi, A.A.; Younesi, H.; Najafpour, G.D. Adsorption of Fe (II) ions from aqueous phase by chitosan adsorbent: Equilibrium, kinetic, and thermodynamic studies. Desalin. Water Treat. 2012, 50, 348–359. [Google Scholar]
  192. Deng, L.; Guo, W.; Ngo, H.H.; Zhang, J.; Liang, S.; Xia, S.; Zhang, Z.; Li, J. A comparison study on membrane fouling in a sponge-submerged membrane bioreactor and a conventional membrane bioreactor. Bioresour. Technol. 2014, 165, 69–74. [Google Scholar]
  193. Deng, L.; Guo, W.; Ngo, H.H.; Zhang, X.; Chen, C.; Chen, Z.; Cheng, D.; Ni, S.Q.; Wang, Q. Recent advances in attached growth membrane bioreactor systems for wastewater treatment. Sci. Total Environ. 2022, 808, 152123. [Google Scholar]
  194. Juntawang, C.; Rongsayamanont, C.; Khan, E. Entrapped cells-based-anaerobic membrane bioreactor treating domestic wastewater: Performances, fouling, and bacterial community structure. Chemosphere 2017, 187, 147–155. [Google Scholar]
  195. Juntawang, C.; Rongsayamanont, C.; Khan, E. Fouling characterization in entrapped cells-based-membrane bioreactor treating wastewater. Sep. Purif. Technol. 2017, 175, 321–329. [Google Scholar] [CrossRef]
  196. Ng, K.K.; Shi, X.; Ong, S.L.; Lin, C.F.; Ng, H.Y. An innovative of aerobic bio-entrapped salt marsh sediment membrane reactor for the treatment of high-saline pharmaceutical wastewater. Chem. Eng. J. 2016, 295, 317–325. [Google Scholar]
  197. Zhang, Z.; Liu, S.; Miyoshi, T.; Matsuyama, H.; Ni, J. Mitigated membrane fouling of anammox membrane bioreactor by microbiological immobilization. Bioresour. Technol. 2016, 201, 312–318. [Google Scholar] [CrossRef]
  198. Chaiprapat, S.; Thongsai, A.; Charnnok, B.; Khongnakorn, W.; Bae, J. Influences of liquid, solid, and gas media circulation in anaerobic membrane bioreactor (AnMBR) as a post treatment alternative of aerobic system in seafood industry. J. Membr. Sci 2016, 509, 116–124. [Google Scholar] [CrossRef]
  199. Zhang, S.; Zuo, X.; Xiong, J.; Ma, C.; Hu, B. Effect of powdered activated carbon dosage on sludge properties and membrane bioreactor performance in a hybrid MBR-PAC system. Environ. Technol. 2019, 40, 1156–1165. [Google Scholar] [CrossRef]
  200. Zhang, W.; Liu, X.; Wang, D.; Jin, Y. Effects of bamboo charcoal on fouling and microbial diversity in a flat-sheet ceramic membrane bioreactor. Bioresour. Technol. 2017, 243, 1020–1026. [Google Scholar] [CrossRef]
  201. Xia, T.; Gao, X.; Wang, C.; Xu, X.; Zhu, L. An enhanced anaerobic membrane bioreactor treating bamboo industry wastewater by bamboo charcoal addition: Performance and microbial community analysis. Bioresour. Technol. 2016, 220, 26–33. [Google Scholar]
  202. Lim, M.; Ahmad, R.; Guo, J.; Tibi, F.; Kim, M.; Kim, J. Removals of micropollutants in staged anaerobic fluidized bed membrane bioreactor for low-strength wastewater treatment. Process Saf. Environ. Prot. 2019, 127, 162–170. [Google Scholar] [CrossRef]
  203. Wang, Y.K.; Pan, X.R.; Sheng, G.P.; Li, W.W.; Shi, B.J.; Yu, H.Q. Development of an energy-saving anaerobic hybrid membrane bioreactors for 2-chlorophenol-contained wastewater treatment. Chemosphere 2015, 140, 79–84. [Google Scholar] [CrossRef]
  204. Xiao, Y.; Yaohari, H.; Araujo, C.D.; Sze, C.C.; Stuckey, D.C. Removal of selected pharmaceuticals in an anaerobic membrane bioreactor (AnMBR) with/without powdered activated carbon (PAC). Chem. Eng. J. 2017, 321, 335–345. [Google Scholar] [CrossRef]
  205. Nguyen, T.T.; Bui, X.T.; Luu, V.P.; Nguyen, P.D.; Guo, W.; Ngo, H.H. Removal of antibiotics in sponge membrane bioreactors treating hospital wastewater: Comparison between hollow fiber and flat sheet membrane systems. Bioresour. Technol. 2017, 240, 42–49. [Google Scholar] [CrossRef] [PubMed]
  206. Zhang, W.; Tang, B.; Bin, L. Research progress in biofilm-membrane bioreactor: A critical review. Ind. Eng. Chem. Res. 2017, 56, 6900–6909. [Google Scholar] [CrossRef]
  207. Anburajan, P.; Kim, Y.; Rice, S.A.; Oh, H.S. Bacterial signaling and signal responses as key factors in water and wastewater treatment. J. Water Process. Eng. 2021, 44, 102434. [Google Scholar] [CrossRef]
  208. Zhang, T.; Cui, C.; Chen, S.; Yang, H.; Shen, P. The direct electrocatalysis of Escherichia coli through electroactivated excretion in microbial fuel cell. Electrochem. Commun. 2008, 10, 293–297. [Google Scholar] [CrossRef]
  209. Hassan, S.H.A.; Kim, Y.S.; Oh, S.-E. Power generation from cellulose using mixed and pure cultures of cellulose-degrading bacteria in a microbial fuel cell. Enzyme Microb. Technol. 2012, 51, 269–273. [Google Scholar] [CrossRef] [PubMed]
  210. Liu, M.; Yuan, Y.; Zhang, L.-X.; Zhuang, L.; Zhou, S.-G.; Ni, J.-R. Bioelectricity generation by a Gram-positive Corynebacterium sp. strain MFC03 under alkaline condition in microbial fuel cells. Bioresour. Technol. 2010, 101, 1807–1811. [Google Scholar] [CrossRef]
  211. Ren, Z.; Steinberg, L.M.; Regan, J.M. Electricity production and microbial biofilm characterization in cellulose-fed microbial fuel cells. Water Sci. Technol. 2008, 58, 617–622. [Google Scholar] [CrossRef]
  212. Rezaei, F.; Xing, D.; Wagner, R.; Regan, J.M.; Richard, T.L.; Logan, B.E. Simultaneous cellulose degradation and electricity production by Enterobacter cloacae in a microbial fuel cell. Appl. Environ. Microbiol. 2009, 75, 3673–3678. [Google Scholar] [CrossRef]
  213. Topare, N.S.; Attar, S.J.; Manfe, M.M. Sewage/wastewater treatment technologies: A review. Sci. Rev. Chem. Commun. 2011, 1, 18–24. [Google Scholar]
  214. O’Toole, G.; Kaplan, H.B.; Kolter, R. Biofilm formation as microbial development. Annu. Rev. Microbiol. 2000, 54, 49–79. [Google Scholar] [CrossRef]
  215. Wang, V.B.; Chua, S.L.; Cao, B.; Seviour, T.; Nesatyy, V.J.; Marsili, E.; Kjelleberg, S.; Givskov, M.; Tolker-Nielsen, T.; Song, H.; et al. Engineering PQS biosynthesis pathway for enhancement of bioelectricity production in Pseudomonas aeruginosa microbial fuel cells. PLoS ONE 2013, 8, e63129. [Google Scholar] [CrossRef] [PubMed] [Green Version]
  216. Rabaey, K.; Boon, N.; Hofte, M.; Verstraete, W. Microbial phenazine production enhances electron transfer in biofuel cells. Environ. Sci. Technol. 2005, 39, 3401–3408. [Google Scholar] [CrossRef] [PubMed]
  217. Venkataraman, A.; Rosenbaum, M.; Arends, J.B.A.; Halitschke, R.; Angenent, L.T. Quorum sensing regulates electric current generation of Pseudomonas aeruginosa PA14 in bioelectrochemical systems. Electrochem. Commun. 2010, 12, 459–462. [Google Scholar] [CrossRef]
  218. Toyofuku, M.; Nomura, N.; Kuno, E.; Tashiro, Y.; Nakajima, T.; Uchiyama, H. Influence of the Pseudomonas quinolone signal on denitrification in Pseudomonas aeruginosa. J. Bacteriol. 2008, 190, 7947–7956. [Google Scholar] [CrossRef] [PubMed]
  219. Toyofuku, M.; Nakajima-Kambe, T.; Uchiyama, H.; Nomura, N. The effect of a cell-to-cell communication molecule, Pseudomonas quinolone signal (PQS), produced by P. aeruginosa on other bacterial species. Microbes Environ. 2010, 25, 1–7. [Google Scholar] [CrossRef]
  220. Cai, W.; Zhang, Z.; Ren, G.; Shen, Q.; Hou, Y.; Ma, A.; Deng, Y.; Wang, A.; Liu, W. Quorum sensing alters the microbial community of electrode-respiring bacteria and hydrogen scavengers toward improving hydrogen yield in microbial electrolysis cells. Appl. Energy 2016, 183, 1133–1141. [Google Scholar] [CrossRef]
  221. Yang, Y.; Zhou, H.; Mei, X.; Liu, B.; Xing, D. Dual-edged character of quorum sensing signaling molecules in microbial extracellular electron transfer. Front. Microbiol. 2018, 9, 1924. [Google Scholar] [CrossRef]
  222. Seow, T.W.; Lim, C.K.; Nor, M.H.M.; Mubarak, M.F.M.; Lam, C.Y.; Yahya, A.; Ibrahim, Z. Review on wastewater treatment technologies. Int. J. Appl. Environ. Sci. 2016, 11, 111–126. [Google Scholar]
  223. Pronk, M.; de Kreuk, M.K.; de Bruin, B.; Kamminga, P.; Kleerebezem, R.; van Loosdrecht, M.C.M. Full scale performance of the aerobic granular sludge process for sewage treatment. Water Res. 2015, 84, 207–217. [Google Scholar] [CrossRef]
  224. Wagner, J.; Weissbrodt, D.G.; Manguin, V.; da Costa, R.H.; Morgenroth, E.; Derlon, N. Effect of particulate organic substrate on aerobic granulation and operating conditions of sequencing batch reactors. Water Res. 2015, 85, 158–166. [Google Scholar] [CrossRef]
  225. Sheng, G.P.; Li, A.J.; Li, X.Y.; Yu, H.Q. Effects of seed sludge properties and selective biomass discharge on aerobic sludge granulation. Chem. Eng. J. 2010, 160, 108–114. [Google Scholar] [CrossRef]
  226. Devlin, T.R.; di Biase, A.; Kowalski, M.; Oleszkiewicz, J.A. Granulation of activated sludge under low hydrodynamic shear and different wastewater characteristics. Bioresour. Technol. 2017, 224, 229–235. [Google Scholar] [CrossRef] [PubMed]
  227. Liu, Y.; Wang, Z.W.; Qin, L.; Liu, Y.Q.; Tay, J.H. Selection pressuredriven aerobic granulation in a sequencing batch reactor. Appl. Microbiol. Biotechnol. 2005, 67, 26–32. [Google Scholar] [CrossRef] [PubMed]
  228. Zou, J.; Tao, Y.; Li, J.; Wu, S.; Ni, Y. Cultivating aerobic granular sludge in a developed continuous-flow reactor with two-zone sedimentation tank treating real and low-strength wastewater. Bioresour. Technol. 2017, 247, 776–783. [Google Scholar] [CrossRef]
  229. Chen, H.; Li, A.; Cui, D.; Wang, Q.; Wu, D.; Cui, C.; Ma, F. N-Acyl-homoserine lactones and autoinducer-2-mediated quorum sensing during wastewater treatment. Appl. Microbiol. Biotechnol. 2018, 102, 1119–1130. [Google Scholar] [CrossRef] [PubMed]
  230. Jiang, H.; Tay, J.; Maszenan, A.M.; Tay, S.T.-L. Enhanced phenol biodegradation and aerobic granulation by two coaggregating bacterial strains. Env. Sci. Technol. 2006, 40, 6137–6142. [Google Scholar] [CrossRef]
  231. Ding, Y.; Feng, H.; Huang, W.; Shen, D.; Wang, M. A sustainable method for effective regulation of anaerobic granular sludge: Artificially increasing the concentration of signal molecules by cultivating a secreting strain. Bioresour. Technol. 2015, 196, 273–278. [Google Scholar] [CrossRef]
  232. Song, X.; Qiu, H.; Xiao, X.; Cheng, Y.; Li, W.; Sheng, G.; Li, X.; Yu, H. Determination of autoinducer-2 in biological samples by high-performance liquid chromatography with flfluorescence detection using pre-column derivatization. J. Chromatogr. A 2014, 1361, 162–168. [Google Scholar] [CrossRef]
  233. Servinsky, M.D.; Terrell, J.L.; Tsao, C.Y.; Wu, H.C.; Quan, D.N.; Zargar, A.; Allen, P.C.; Byrd, C.M.; Sund, C.J.; Bentley, W.E. Directed assembly of a bacterial quorum. ISME J. 2016, 10, 158–169. [Google Scholar] [CrossRef]
  234. Zhao, J.; Quan, C.; Jin, L.; Chen, M. Production, detection and application perspectives of quorum sensing autoinducer2 in bacteria. J. Biotechnol. 2018, 268, 53–60. [Google Scholar] [CrossRef]
  235. Wang, L.H.; He, Y.; Gao, Y.; Wu, J.E.; Dong, Y.H.; He, C.; Wang, S.X.; Weng, L.X.; Xu, J.L.; Tay, L.; et al. A bacterial cell-cell communication signal with cross-kingdom structural analogues. Mol. Microbiol. 2004, 51, 903–912. [Google Scholar] [CrossRef] [PubMed]
  236. Wu, J.; Afridi, Z.U.R.; Cao, Z.; Zhang, Z.; Poncin, S.; Li, H.; Zuo, J.; Wang, K. Size effect of anaerobic granular sludge on biogas production: A micro scale study. Bioresour. Technol. 2016, 202, 165–171. [Google Scholar] [CrossRef] [PubMed]
  237. Ding, Y.; Feng, H.; Huang, W.; Li, N.; Zhou, Y.; Wang, M.; Zhang, X.; Shen, D. The effect of quorum sensing on anaerobic granular sludge in different pH conditions. Biochem. Eng. J. 2015, 103, 270–276. [Google Scholar] [CrossRef]
  238. Ding, Y.; Feng, H.; Zhao, Z.; Shen, D.; Wang, M.; Zhou, Y. The effect of quorum sensing on mature anaerobic granular sludge in unbalanced nitrogen supply. Water Air Soil Pollut. 2016, 227, 334. [Google Scholar] [CrossRef]
  239. Li, L.; Zheng, M.; Ma, H.; Gong, S.; Ai, G.; Liu, X.; Li, J.; Wang, K.; Dong, X. Significant performance enhancement of a UASB reactor by using acyl homoserine lactones to facilitate the long filaments of Methanosaeta harundinacea 6Ac. App. Microbiol. Biotechnol. 2015, 99, 6471–6480. [Google Scholar] [CrossRef]
  240. Lv, L.; Li, W.; Zheng, Z.; Li, D.; Zhang, N. Exogenous acylhomoserine lactones adjust community structures of bacteria and methanogens to ameliorate the performance of anaerobic granular sludge. J. Hazard. Mater. 2018, 354, 72–80. [Google Scholar] [CrossRef]
Ijms 23 09751 g001 550
Figure 1. Schematic diagram of various steps involved in the biofilm formation process.
Figure 1. Schematic diagram of various steps involved in the biofilm formation process.
Ijms 23 09751 g001
Ijms 23 09751 g002 550
Figure 2. Schematic diagram of various techniques used for biofilm characterization.
Figure 2. Schematic diagram of various techniques used for biofilm characterization.
Ijms 23 09751 g002
Ijms 23 09751 g003 550
Figure 3. Typical QS signaling pathways. (A) AHL pathway seen in Gram-negative bacteria, (B) AIP pathway seen in Gram-positive bacteria, (C) AI-2 pathway seen in both Gram-negative and Gram-positive bacteria.
Figure 3. Typical QS signaling pathways. (A) AHL pathway seen in Gram-negative bacteria, (B) AIP pathway seen in Gram-positive bacteria, (C) AI-2 pathway seen in both Gram-negative and Gram-positive bacteria.
Ijms 23 09751 g003
Ijms 23 09751 g004 550
Figure 4. AHL degradation pathways. (1) AHL synthesis blockage, (2) AHL inactivation, (3) interference with AHL signal receptor.
Figure 4. AHL degradation pathways. (1) AHL synthesis blockage, (2) AHL inactivation, (3) interference with AHL signal receptor.
Ijms 23 09751 g004
Ijms 23 09751 g005 550
Figure 5. Diagrammatic representation of the difference between quorum sensing and quorum quenching.
Figure 5. Diagrammatic representation of the difference between quorum sensing and quorum quenching.
Ijms 23 09751 g005
Table
Table 1. QS and QQ bacteria involved in wastewater treatment.
Table 1. QS and QQ bacteria involved in wastewater treatment.
TypeBacteriaSignal TypeQS/QQ-Related ActivitiesTreatment ProcessesWastewater TypeRef.
Quorum sensing bacteriaSphingomonas paucimobilis--EBPR aerobic-anaerobic process/conventional aerobic activated sludge processMunicipal or industry wastewater[83,84]
Burkholderia sp. DW2–1CepI/CepRBiosurfactant production-Municipal or industry wastewater[85,86]
B. cenocepacia BSP3
AeromonasAHL, AI-2Biofilm formation--[54]
A. hydrophilaC4-HSL, C6-HSL, AI-2Biofilm developmentActivated sludge processMunicipal wastewater[66,76]
Pseudomona aeruginosa PAON-decanoyl-L-HSL (C10HSL)Anthranilate biodegradation in waste water--[87]
Xanthomonas sp.DSFEPS productionActivated sludge-[88]
P. aeruginosaRhlI/RhlRDegradation of phenol-Industrial and municipal wastewater[22]
Vibrio sp.AI-2, AHKBiofilm formation, virulence factor production--[54]
Ac. baumannii strain M23- hydroxy C12-HSLBiofilm formation and development, surface motility-Municipal or industry wastewater[83,89,90,91]
Pseudomonas sp.C4-HSL, C6-HSL, oxo-C12-HSL, PQSBiofilm formation and development; virulence factor production; EPS production; interspecies competition; denitrificationActivated sludge-[83,88]
Nitrosomonas europaeaC6-HSL, C8-HSL C10-HSL-Activated sludge processIndustrial wastewater[92,93]
P. putidaC4-HSL,Biofilm formationActivated sludge process Municipal wastewater[94]
Quorum quenching bacteriaVariovorax paradoxus strain VAI-CC4-HSL, C6-HSL C8-HSL, C10-HSL C12-HSL 3-oxo-C6-HSLDegrade other species AHLsActivated sludge process Industrial wastewater[92,95,96]
Rhodococcus sp. BH4C6-HSL, C8-HSL C10-HSL, C12-HSL 3-oxo-C6-HSL 3-oxo-C8-HSL 3-oxo-C10-HSL 3-oxo-C12-HSLInhibit biofilm formation in MBRReal MBR plant Municipal wastewater[72,97,98,99,100]
Acinetobacter sp. strain Ooi24C10-HSL -Activated sludge process Unknown[94]
Pseudomonas sp. 1A1C6-HSL,C8- HSL C10-HSL, C12-HSL 3-oxo-C8- HSL 3-oxo-C10- HSL 3-oxo-C12- HSLInhibit biofilm formation in MBRLab-scale MBR/activated sludge processMunicipal wastewater[71,101,102]
Not available = ‘‘-‘’.
Table
Table 2. Techniques for autoinducer detection, identification and characterization in wastewater treatment systems.
Table 2. Techniques for autoinducer detection, identification and characterization in wastewater treatment systems.
Technique EmployedApplicationsAdvantagesLimitationsRef.
Bacterial biosensorsC. violacum CV026Detects AHLs by producing purple colored pigment violacein Simple bioassayUnable to detect any of the three hydroxyl derivatives, no information on AHLs’ structure and concentrations[103]
A. tumefaciens A136 &
A. tumefaciens NTL4		Produces blue spots on TLC plates or Petri dishes upon detection of AHLs A fast biosensor for AHL screeningNot capable of detecting N-butanoyl-homoserine lactone, no information on AHLs’ structure and concentrations[94,103]
LuminescenceBeta-Glo Assay System (Promega, Madison, WI, USA) based AHL quantification techniqueSimple, easy, and fast bioassayNA[72]
TLCPartial characterization and structure identification of AHLsEasy, fast, and cheap method for determining preliminary structure information, can be coupled with biosensor or sulfuric acidTLC alone is enough to determine the complete structure of AHLs[104,105,106]
HPLCCan detect a large no. of AHLsSimple and fast technique for AHLs’ qualitative and quantitative analysisUnable to provide an AHL-specific structure.[103]
HPLC–MS/MSUsed for quantification of various AHLsProvides rapid AHL quantificationNA[107]
LC–MSAble to determine AHL structure, can be coupled with HPLC Can quantify very small amounts of AHLs—down to picomoles Some qualitative information and chromophores are needed for operation[72,103]
SPE-LLE with LC-MS/MSDetection and trace analysis of AHLs in wastewaterCan identify and quantify AHL trace levels in wastewater systemsNA[108]
ELISAQuantitative detection of AHLs and their degradation productsRapid, cheap, and sensitive method, needs low amounts of sample (<1 mL)NA[109]
HLB and UE coupled with UPLC-MS/MSAHL detectionRobust and sensitive method for AHL detection in wastewaterNA[110]
UHPLC-MSAHL detection and quantificationIndependent of the sample matrix, can detect low concentrations of AHLsNA[109]
IRIdentifies functional groupsSimple, cheap, easy, and versatile Sample preparation needs extra care[40]
NMRUsed in AHL structure determinationCan detect fine details of structural componentsTime-consuming and costly[111]
GC-MS, NanoLC-MS/MS, MALDI-MS, and magnetic molecularly imprinted polymer nanoparticles based electrochemical sensorAHL detection and characterizationProvides accurate details on AHL structure and characterizationNA[94,112]
Legend: TLC—thin layer chromatography; HPLC—high-performance liquid chromatography; HPLC–MS/MS—LC-MS—liquid chromatography–mass spectrometry; SPE-LLE—solid phase extraction—liquid–liquid extraction; LC-MS/MS—liquid chromatography—tandem mass spectrometry; ELISA—enzyme-linked immunosorbent assay; HLB—hydrophilic–lipophilic balanced sorbent; UE—ultrasonic extraction; UHPLC-MS—ultrahigh-performance liquid chromatography coupled to mass spectrometry; IR—infrared; NMR—nuclear magnetic resonance; GC-MS—gas chromatography-mass spectrometry; NanoLC-MS/MS—nanoscale liquid chromatography coupled to tandem mass spectrometry; MALDI-MS—matrix assisted laser desorption/ionization.
Table
Table 4. Major naturally existing quorum quenching enzymes used in wastewater treatment.
Table 4. Major naturally existing quorum quenching enzymes used in wastewater treatment.
QQ EnzymeSource OrganismMechanism of ActionRef.
AHL-acylaseTenacibaculum discolor strain 20 J,AHL degradation[163]
Hyphamonas sp. DG895C4HSL and 3OC12-HSL[103]
AHL-oxidaseBacillus megateriumC4HSL and 3OC12HSL[164]
AI-2 kinase (LsrK)Escherichia coli, other enteric bacteriaDegradation of AI-2[112,165]
LactonesStreptomycetes spp.Mimics AHL signals[166]
AHL-oxidoreductaseBurkholderia strain GG43OC6HSL[167]
AHL-lactonaseHalomonas sp. strain 33AHL degradation[163]
Bacillus cereusAHL degradation[103]
Publisher’s Note: MDPI stays neutral with regard to jurisdictional claims in published maps and institutional affiliations.

Share and Cite

MDPI and ACS Style

Sahreen, S.; Mukhtar, H.; Imre, K.; Morar, A.; Herman, V.; Sharif, S. Exploring the Function of Quorum Sensing Regulated Biofilms in Biological Wastewater Treatment: A Review. Int. J. Mol. Sci. 2022, 23, 9751. https://doi.org/10.3390/ijms23179751

AMA Style

Sahreen S, Mukhtar H, Imre K, Morar A, Herman V, Sharif S. Exploring the Function of Quorum Sensing Regulated Biofilms in Biological Wastewater Treatment: A Review. International Journal of Molecular Sciences. 2022; 23(17):9751. https://doi.org/10.3390/ijms23179751

Chicago/Turabian Style

Sahreen, Sania, Hamid Mukhtar, Kálmán Imre, Adriana Morar, Viorel Herman, and Sundas Sharif. 2022. "Exploring the Function of Quorum Sensing Regulated Biofilms in Biological Wastewater Treatment: A Review" International Journal of Molecular Sciences 23, no. 17: 9751. https://doi.org/10.3390/ijms23179751

Note that from the first issue of 2016, this journal uses article numbers instead of page numbers. See further details here.

Article Metrics

Back to TopTop