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Article

Biofouling Removal from Membranes Using Nonthermal Plasma

by
Irena Maliszewska
1 and
Tomasz Czapka
2,*
1
Department of Organic and Medicinal Chemistry, Faculty of Chemistry, Wroclaw University of Science and Technology, 50-370 Wroclaw, Poland
2
Department of Electrical Engineering Fundamentals, Faculty of Electrical Engineering, Wroclaw University of Science and Technology, 50-370 Wroclaw, Poland
*
Author to whom correspondence should be addressed.
Energies 2020, 13(17), 4318; https://doi.org/10.3390/en13174318
Submission received: 17 July 2020 / Revised: 14 August 2020 / Accepted: 19 August 2020 / Published: 20 August 2020
(This article belongs to the Section K: State-of-the-Art Energy Related Technologies)
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Abstract

:
An essential aspect of wastewater treatment systems based on membranes is fouling, which leads to a decrease in their performance and durability. The membrane biofouling is directly related to the deposition of biological particles (e.g., microorganisms in the form of biofilm) on the membrane surface. The objective of the study was to investigate the possibility of using nonthermal plasma for membrane treatment to overcome the biofouling problem. The removal of biological cells from the membrane surface was performed in a dielectric barrier discharge (DBD) plasma. The biofoulant (i.e., activated sludge) on the surface of membranes was treated with plasma for 3–10 min, corresponding to a plasma dose of 13–42 J cm−2. Results of biofouling removal studies indicated that the process was very efficient (i.e., lethal effect was also observed) and dependent on the type of membrane and exposure time to the nonthermal plasma. Moreover, investigations of the influence of plasma treatment on extracellular polymeric substances of biofilms have confirmed the possibility of using plasma in the process of protein release from biological structures, which results in their destruction. It seems that plasma technologies can be part of the so-called hybrid methods of removing biological contamination of membranes used in wastewater treatment.

Graphical Abstract

1. Introduction

The issue of water purity is urgent because of its impact on the ecosystem as well as human and animal health. Water used in homes, industries, and companies is released back into the environment in great volumes. Unfortunately, water in the form of wastewater contains significant amounts of harmful compounds (e.g., chemical, biological, heavy metals, etc.), and therefore needs to be treated to improve its quality to the required safety level.
Water management is becoming increasingly challenging and several wastewater treatment methods have emerged in recent decades [1]. The separation of materials through a membrane depends on pore and molecule size, and water treatment procedures use different types of membranes [2]. Most membranes are produced from hydrophobic synthetic organic polymers (e.g., polysulfone, polyethersulfone, polyethylene, polypropylene) [3,4]. The hydrophobicity of membranes is a disadvantage contributing to their fouling. In general, membrane fouling is triggered by deposition and accumulation of inorganic and organic molecules (i.e., microbial cells) on the filter membrane resulting in complete blocking of the pores [5]. Biofouling is a comprehensive, dynamic, and fairly slow process involving various biological mechanisms that have not been fully understood yet [6,7]. Biofouling is considered to be the “Achilles heel” of wastewater treatment using membrane procedures, because microorganisms can reproduce over time and cleaning protocols cause additional operating costs [8].
The effects of extracellular polymeric substances (EPS) on membrane fouling have received increasing attention in recent years [9,10]. It is well known that biofilm culture is enclosed in a matrix of hydrated EPS that create its environment. For most of the biofilm, the microorganisms are less than 10% of dry matter, whereas the extracellular matrix (mainly produced by the organisms themselves) may be over 90% [11]. An extracellular matrix consists of various biomolecules such as polysaccharides, proteins, nucleic acids and lipids [12]. They establish the structural and functional integrity of microbiological biofilms and contribute to the organization of the biofilm community [13]. Moreover, these substances significantly affect the mechanical stability of biofilms [14].
The accumulation of EPS on the surface of membranes reduce their permeability. The deposited material forms a gel layer by crosslinking with the membrane surface [15]. This layer provides a nutrient-rich environment that is ideal for the further binding of microbial cells. It can, therefore, be concluded that the estimation of cell mortality on the membrane surface is not a sufficient indicator to assess the effectiveness of the nonthermal plasma in the biofouling removal process. Carbohydrates have been identified as one of the main components of EPS, but the complexity of these molecules and unique combinations of monomers result in difficulties in their quantification. We assumed that the destruction of EPS expressed as the concentration of protein released into the water from the surface of the membrane with the fouling layer after plasma treatment can be an additional criterion for assessing the effectiveness of biofouling destruction. It was confirmed that the membrane with biofilm cells layer subjected to the ultrasonic bath for 5 min was a positive control and the concentration of protein released from the membrane into the water after this treatment was considered as 100%.
The conventional anti-fouling strategy is based on dosing feed water continuously with biocides. Chlorine is the most commonly employed disinfectant in water and wastewater treatment. In some scenarios, chlorine is not suitable for membrane treatment since the most commercially accessible polymeric membranes are sensitive to chlorine [16]. Furthermore, ozone is efficient in the inactivation of bacteria, viruses, and protozoa [17]. However, owing to its instability, ozone must be produced on-site. It should be emphasized that ozone can form in the treated water mutagenic and carcinogenic factors such as bromate [18]. In water treatment, the frequent use of non-oxidizing biocides (e.g., formaldehyde, glutaraldehyde, and quaternary ammonium compounds) may result in a decrease in the sensitivity of microorganisms to the applied biocides [19]. Similarly, UV radiation has been used for many years to disinfect water and treat wastewater. Moreover, UV radiation is an effective physical process that inactivates bacteria, viruses [20], and degrades macromolecules to smaller fragments. However, the relatively high cost of this method and problems in dose optimization and monitoring have mainly reduced its applications to minor and automated systems [21]. Membrane cleaning is also carried out by physical methods. Physical methods include hydraulic, pneumatic, and mechanical cleaning, as well as the use of electric fields [22,23,24,25]. The drawback of physical processes is the usage of harmful chemicals such as acids, bases, oxidants, and surfactants [5].
A very promising method of wastewater treatment is the application of nonthermal plasma (NTP) produced by various types of electrical discharges [26,27,28]. Plasma technologies belong to the so-called advanced oxidation processes (AOPs). Advanced oxidation processes (AOPs) are novel techniques that apply energy (e.g., electrical or chemical) to the reaction area to form highly reactive species that initiate many physical and chemical processes. Nowadays, plasma technologies—as one of the AOPs—are of great interest due to their excellent performance and high energy efficiency in environmental applications.
In general, plasma can be considered as an electrically neutral medium in the gaseous phase, consisting of electrons, ions, and neutral particles. The characteristic features of plasma are its ionization degree and high electrical conductivity. NTP at atmospheric pressure is successfully used for gas cleaning (e.g., decomposition of volatile organic compounds), surface treatment of materials, enhancing of chemical reactions, biological applications (e.g., sterilization process), and in plasma medicine (e.g., wound healing, cancer therapy) [29,30,31,32].
In the process of wastewater processing, the plasma can be used in many different ways. The main methods utilized for the treatment of water (including wastewater) are plasma injection, remote, indirect, and direct plasma technologies. The individual methods are differentiated by the location of plasma formation (i.e., directly, near or far from the treated liquid medium) and by the impact of individual particles present in the plasma (i.e., electrons, ions, excited species, and neutral atoms or molecules), which are specified by their different chemical properties. As a result of plasma interaction with the treated object (i.e., solid material, gas, liquid) many chemical reactions such as ionization, excitation, dissociation, attachment, and detachment may occur separately or simultaneously. To improve energy and water treatment efficiency, the combination of plasma technology with catalysts has become very popular [33,34].
An other way of using nonthermal plasma in water treatment technologies is to alter membranes with anti-fouling features. It is known that plasma significantly affects the surface of polymeric materials without changing their bulk properties. NTP processing of polymers results in essential changes in their surface properties (i.e., chemical and physical), especially surface energy, wettability, adhesion, catalytic performance, gas absorption, and so on. The plasma treatment of polymer surface is now widely used in many applications, e.g., in the textile industry, electronics production, printing technologies for packaging materials and plastic bonding processes [35,36]. The usage of plasma for processing gas separation membranes is already known and modified membranes exhibit high permeability and selectivity of gas separation [37,38]. The membrane modification, similarly to biomaterials, is carried out employing two different plasma processes, i.e., plasma polymerization and direct plasma interaction with the membrane material [39,40]. However, the utilization of NTP to alter the properties of membranes used in wastewater systems is still a new approach and is not well described. The methods of membrane modification (e.g., chemical and using NTP) aiming at limiting the process of fouling are presented in [39,41].
The purpose of this paper is to present the possibility of using nonthermal plasma for membrane cleaning to overcome the biofouling problem in wastewater treatment. The essential novelty of the work is to specify the level of plasma dose necessary to inactivate bacterial cells from the activated sludge.

2. Materials and Methods

2.1. Microorganisms and Culture Conditions

The activated sludge was collected from the municipal sewage treatment plant. This activated sludge was diluted 100 times and supplemented with synthetic sewage consisted of (g/L tap water): peptone, 0.1; yeast extract, 0.01; NaCl, 0.05; KH2PO4, 0.02; NaHCO3, 0.075; MgSO4 × 7H20, 0.07; and CaCl2, 0.025.

2.2. Membranes

Polyamide (PA) and cellulose acetate (CA) membranes were obtained from Sterlitech Corporation (USA). The studied membranes were cut into squares with an area of 4.0 cm2. Each membrane was sterilized for two hours in 70% EtOH, followed by two washing steps using sterile deionized (DI) water to remove the remaining EtOH. The membranes were stored in sterile H2O at 4 °C for further use.

2.3. Adhesion Formation

The static experiments were carried out using activated sludge as a biofoulant (see Figure 1). The initial adhesion was performed in a culture vessel by an incubation time of 4 h, at 20 °C using a rotary shaker (100 rpm). To avoid sedimentation of the microorganisms on the membrane, the membrane was placed in a vertical position (Figure 1). After 4 h of incubation, the membrane was removed from activated sludge, rinsed twice with sterile distilled water, and placed in a new vessel with 5 mL of sterile distilled water.

2.4. Biofilm Formation

The initial adhesion was performed following the method described above. After 4 h of incubation, the membrane was removed from activated sludge, rinsed twice with distilled sterile water and placed in a new vessel containing 5 mL of the synthetic sewage. The biofilm was formed on the surface on the membrane for 24 or 72 h at room temperature. The membrane was then washed twice with sterile distilled water and placed in a new vessel with 5 mL of sterile distilled water.

2.5. Studies on the Effectiveness of Removing of Biofouling by Nonthermal Plasma

The removal of biofouling was carried out using a DBD plasma reactor. Nonthermal plasma was generated in the air at atmospheric pressure. The membranes were placed on the grounded electrode and the high voltage electrode was approximately 4 mm above the treated sample. The biofoulant on the surface of membranes was treated with the plasma for 3, 5, 7, and 10 min. Discharge power density in the experiment was constant and equal to 70 mW cm−2 (i.e., calculated from a charge-voltage Lissajous plot). The effectiveness of biofouling removal was quantified based on the percentage of surviving microbial population and the percentage of EPS destroyed. The plasma dose during the tests was given by:
Plasma   dose   [ J   cm − 2 ] = P · t S ,
where P is the discharge power (i.e., from Lissajous plot), t is treatment time, and S is the membrane surface.

2.6. Quantification of Cell Viability

The membranes with fouling layer (i.e., before and after nonthermal plasma treatment) were placed in 5 mL of water and treated with an ultrasound bath (SONOREX Digital 10P, Bandelin Electronic GmbH & Co. KG, Berlin, Germany) for 5 min. The viability of the microorganisms in the harvested suspension was tested using MTT (3-(4,5-dimethylthiazol-2-yl)-2,5-diphenyltetrazolium bromide, a tetrazole) assay. The percentage of surviving microbial population obtained by MTT assay was calculated as:
Cell   viability   [ % ] = A − B C − B · 100 ,
where A is the average absorbance for treated membranes (adhesive/biofilm cells and plasma treatment), B is the average absorbance for control membranes (no adhesive/biofilm cells, no plasma treatment), and C is the average absorbance for untreated membranes (adhesive/biofilm cells, no plasma treatment).

2.7. Extraction and Evaluation of Extracellular Polymers from Biofilms

The membrane with a fouling layer after nonthermal plasma treatment was placed in 5 mL of water and incubated at room temperature for 5 min with vigorous shaking (140 rpm). Then, the membrane was taken out from the water and added to NaCl with the final concentration of 1.5 M [42]. This suspension was centrifuged (500× g; 5 min) without any incubation period. The obtained supernatant was harvested as an EPS fraction. The concentration of proteins in the isolated EPS fraction was determined by the Lowry method [43]. Bovine serum albumin (BSA) was used as a standard.
The positive control was the membrane with a fouling layer after 5 min of ultrasonic bath treatment. The efficiency of nonthermal plasma treatment in removing EPS from the surface of the membrane, estimated with the Lowry method was given by:
Destroyed   ( removed )   EPS   [ % ] = A − C B − C · 100 ,
where A represents the average concentration of protein extracted from membranes with biofilm cells after nonthermal plasma treatment, B represents the average concentration of protein extracted from membranes with biofilm cells after 5 min of an ultrasonic bath, and C represents the average concentration of protein extracted from membranes with biofilm cells without any treatment (i.e., biofilm cells, no plasma or ultrasonic bath).

2.8. SEM Studies

For SEM studies, all samples were fixed in 2.5% glutaraldehyde for 24 h at 4 °C. Then the samples were washed three times with 0.1M sodium phosphate at pH 7. The material was then dried in a series of graduated ethanol (from 40% to 100%) and deposited on the grids covered with carbon tape, air-dried, and coated with a thin gold layer. The surface topography of the samples was evaluated by scanning electron microscopy (Quanta 250, FEI).

2.9. The Fluorescence Microscopy

A biofilm covering the membrane was analyzed using fluorescence microscopy. Samples before and after plasma treatment were exposed to SYTOX® Green cell stain (ThermoFisher Scientific, Waltham, MA, USA) and incubated at room temperature in the dark for 15 min. Biofilm imaging was carried out using an Olympus 60BX light microscope.

2.10. Statistical Analysis

All tests were performed in three repetitions. Statistical analyses were carried out using STATISTICA data analysis software (version 10.0) and Excel. Quantitative variables were determined by the arithmetic mean of standard deviation, median or maximum/min (range), and 95% confidence interval. The statistical significance of the differences between the two groups was established using the Student’s t-test. In all calculations, a p-value of 0.05 was assumed as the limit value.

3. Results and Discussion

Activated sludge is a suspension of heterotrophic bacteria and protozoa. This flocculent suspension contains microorganisms capable of carrying oxidation of organic compounds, nitrification, denitrification, or having the ability to accumulate phosphorus. Biofouling of the membrane by activated sludge remains a key problem influencing the efficiency and economical performance of membrane separation bioreactors in wastewater treatment technologies. The activated sludge properties responsible for membrane fouling comprise components such as inorganic matter, mixed liquid suspended solids, extracellular polymers (EPS), microbial metabolites products, and microbial communities [44]. The intensive development of the activated sludge, especially overgrowth of filamentous bacteria, may lead to severe membrane fouling [45]. Formation of biofilm by microorganisms on the membrane surface involves several specific stages: reversible and irreversible cell attachment to the surface, displacement of reversibly bonded cells on the surface, and triggering of microcolony formation, maturation, differentiation, and eventually dissolution and dispersion of the biofilm [46]. The binding of microbial cells to the membrane surface is the initial phase of membrane biofouling [7]. Electrokinetic and hydrophobic interactions play the main role in this process [8]. An essential function in biofilm formation is assigned to extracellular polymeric substances, which are released by microorganisms, inducing microorganisms to colonize the membrane surface [17].
Our research focused on determining the efficiency of the nonthermal plasma in removing biofouling from the membrane surface at various stages of biofilm development by activated sludge. The DBD plasma reactor with a flat-parallel electrode configuration was used as shown in Figure 2. The electrical discharges were generated between two electrodes (i.e., with the electrode area of 120 cm2) covered by a dielectric layer with the area and the thickness equal to 140 cm2 and 0.1 cm, respectively. The sample was placed between the electrodes before the plasma treatment. A pulse modulated alternating current (37 kHz) power supply (Dora Electronics Equipment, Poland) was connected to electrodes of the plasma reactor to energize air operated as a processing gas at atmospheric pressure with no flow. An output voltage and a discharge power were constant and equal to 5.5 kV and 8.4 W (i.e., corresponding to 70 mW cm−2), respectively. Based on the measured discharge power and the plasma treatment time, it was possible to determine the energy density (i.e., plasma dose) used to remove biofouling from the membrane surface. The maximum energy density used in the tests was 42 J cm−2.
The efficiency of the nonthermal plasma in membrane cleaning was determined as: (i) the highest cell mortality obtained and (ii) the plasma treatment time necessary to achieve the cell mortality rate of 50% (lethal dose 50; LD50) and (iii) the percentage of destroyed EPS.
Taking into account the importance of the initial attachment of cells to the surface of the membrane, the efficiency of nonthermal plasma in destroying viable microbial cells forming fouling after 4-h contact of the activated sludge with membranes was determined. The results of the experiment are shown in Figure 3.
As can be seen, the removal efficiency of adherent cells was plasma dose-dependent, and the lethal effect (i.e., a number of viable cells was below detection level) was obtained after 10 min of plasma treatment and it corresponds to a plasma dose of 42 J cm−2 for PA membrane. In the case of the CA membrane, this effect was achieved after 7 min of exposure to nonthermal plasma which corresponds to a dose of ~29 J cm−2. It is noteworthy that a three-minute plasma treatment of adherent cells, which corresponds to an energy density of ~13 J cm−2, results in a mortality of 92% and 93% for PA and CA membranes, respectively. The estimated plasma treatment times required to achieve 50% mortality of cells (LD50) attached to the tested membrane surface (i.e., after 4 h of incubation of activated sludge) were 69 s (~5 J cm−2) and 55 s (~4 J cm−2) for PA and CA membranes, respectively.
The adherence of microbes to the surface is a first and necessary step in the formation of a membrane biofilm. In the presented experiment, a quite important membrane effect was found. Removal of a significant number of viable cells from the surface of the polyamide membrane required a higher energy dose (a longer plasma treatment time). Our experiments showed that this phenomenon is related to the fact that the polyamide membrane has a higher biofouling tendency (see Supplementary Information; Figure S1). After 4 h of incubation with the activated sludge, a higher metabolic activity of cells (on membrane surface) as an indicator of their viability, compared to the CA membrane, was observed.
The adhesion of bacteria of one species to the membrane surface has been extensively studied, and the factors influencing this process are well understood [5]. However, the phenomenon that occurs in our experiment is much more complex, as species may additionally interact with each other. It is well known that activated sludge is a very complex community and its composition is influenced by many different factors [13]. Different species occur in the activated sludge, and each species group has its habitat and niche. By disturbing the homeostasis in habitat (introducing the membrane), some species can bind to this new habitat and display their preferred membrane-bound life form. It has previously been described that the microbial community on the surface of the membrane is very different from those in the suspended biomass [14]. Thus, at this stage of our study, it is suggested that some species present in the activated sludge (culture vessel) had a high affinity for the polyamide membrane.
The next step of our research was to assess the efficiency of nonthermal plasma in destroying the biofilm culture formed on the surface after 24-h incubation of the membranes with activated sludge. It can be considered that 24-h cell proliferation in specific zones results in the formation of structures called microcolonies that can control the mature biofilm [47]. The effect of nonthermal plasma on the destruction of viable cells forming fouling is presented in Figure 4. The obtained results showed again that the plasma-cleaning efficiency was plasma dose-dependent and the best results were obtained after 10-min treatment, which corresponds to the plasma dose of 42 J cm−2 (Figure 4). The mortality rate of biofilm culture reached 92% and 95% for the PA and CA membranes, respectively. The lowest plasma dose used in the test (~13 J cm−2; three-minute treatment) resulted in cell mortality of 27% and 30% for PA and CA membranes, respectively. The calculated plasma treatment times to achieve 50% cell mortality were 314 s (~22 J cm−2) and 288 s (~20 J cm−2) for PA and CA membranes, respectively. Similarly to the results described above, the removal of 24-h biofouling from the surface of the PA membrane required a higher dose of energy. This phenomenon is related to the number of viable cells forming a biofilm on the surface of the PA membrane (see Supplementary Information; Figure S1).
The last experimental series included the removal of a 72-h biological layer from the surface of the membranes by the nonthermal plasma. The results of the measurements are shown in Figure 5. Similarly to the results described above, this cleaning process was dependent on the type of membrane and exposure time to the nonthermal plasma. Ten minutes of plasma treatment of the surface of PA and CA membranes resulted in 81% and 76% mortality of biofilm culture. Three minutes of membrane exposure to plasma (~13 J cm−2) caused only 20% and 13% cell mortality. The membrane surfaces (i.e., depending on the type of material) were required to be plasma-treated for 341 s (~24 J cm−2) and 381 s (~27 J cm−2) to achieve cell mortality rate of 50%.
In the case of a 72-h biofilm, it was observed that the removal of biofouling from the CA membrane requires a higher dose of energy. This time, our results showed that the number of viable cells in the biofilm on the PA membrane was lower than those on the cellulose acetate membrane (see Supplementary Information; Figure S1). These results may suggest that the microbial community that forms biofouling on the two types of membranes may be different. This suggestion can be confirmed by slightly different structures of the biological layers shown in the SEM images (Figure 6). The obtained results confirmed that bacterial adherence to the polymer membrane is a dynamic process. It is known that bacteria (either as single cells or clusters) can actively (or passively) leave the biofilm by a process termed “dispersion” or “dissolution.” It cannot be excluded that in the case of a 72-h biofilm formed on the surface of the PA membrane, this phenomenon may occur.
Moreover, the different nature of the dependence of cell viability on plasma dose was observed (Figure 3, Figure 4 and Figure 5). This phenomenon may be due to the different dynamics of processes occurring during the interaction of plasma with bacteria cells. It should be emphasized that the number of cells was different depending on the time of biofilm formation (i.e., contact of membranes with the activated sludge).
Based on the results obtained, it was found that both polyamide and cellulose acetate membranes are excellent materials for microbial adhesion and biofouling. Our results are consistent with Ridgway and Safarik’s previous observations [48]. These authors showed that polyamide membranes fed with pre-treated municipal wastewater are subject to faster and more intense biological fouling than cellulose acetate membranes. Besides, the resulting biofilm is more strongly attached to the polyamide surface, which reduces the effectiveness of chemical cleaning.
The results of the cleaning process using nonthermal plasma cannot be compared with those obtained by other authors due to the lack of such data. Sonication is one of the methods often applied to clean membranes. Sonication is based on using high energy, ultrasonic impulses to target and dispose materials from the surface. The efficiency of membrane treatment by a single method of deionized (DI) water backwashing, sonication, chemical cleaning, or a combined method (i.e., chemicals, sonication and backwashing) was studied by Lim and Bai [49]. The obtained results showed that none of the individual methods successfully cleaned the membrane, and DI water proved to be the least effective method of biofouling removal. Xu et al. [50] used ultrasonic equipment to control membrane contamination in an anaerobic membrane bioreactor. Four groups of ultrasonic parameters have been tested for effectiveness in controlling membrane fouling. The ultrasonic power intensity of 0.18 W cm−2 and the time of 3 min h−1 (i.e., operate 3 min for each hour) were considered as optimal. Ruiz et al. [51] applied sonication at low power (15 W) with various frequencies (i.e., from 20 to 40 kHz) for the cleaning of fluorinated polyvinylidene membrane. The best control of transmembrane pressure was achieved at 20 kHz without significantly affecting membrane integrity.
The results of the effect of nonthermal plasma on EPS are presented in Table 1. These studies can help assess the destruction process of bacterial biofilms formed on the membrane surface. It should be noted that the production of EPS is the maturation stage of the biofilm formation that binds cells together on the surface [52]; therefore, our experiments were carried out only for biofilms growing for 24 and 72 h. The results collected in Table 1 showed that the concentration of proteins released into the water after exposure of the fouling membrane to the nonthermal plasma was time-dependent, but most proteins were released during the first 5 min of the process. As can be seen in Table 1, a five-minute treatment of biofilms formed for 24 h on the surface of polyamide and cellulose acetate membranes with nonthermal plasma caused a detachment of 65 ± 2% and 69 ± 3% of the total protein considered as an extracellular matrix component. After 10 min of plasma treatment, the cleaning effect was increased by approx. 20%, resulting in the removal of 82 ± 2% and 86 ± 2% proteins from the surface of the membranes tested. A five-minute treatment of the surface of the PA membrane incubated with activated sludge for 72 h released 63 ± 3% of total biofilm proteins into the water. In the case of a membrane made of cellulose acetate, under the same experimental conditions, it was observed that 71 ± 2% of total proteins, recognized as the EPS component, were removed. As expected, the longer treatment time for mature biofilm using the nonthermal plasma resulted in more efficient EPS removal, because 85 ± 3% and 90 ± 2% of total proteins were detected in water for PA and CA membranes, respectively.
Extracellularly secreted proteins determine the microbial attachment process to different solid surfaces [53]. Proteins are accumulated on the cell surface and after the secretion process to the external environment, these molecules may be adsorbed on contact surfaces [54]. This layer of adsorbed proteins can transform the solid/medium phase into a gel-like area with which other specific polymers of the bacterial surface can interact [55]. During more advanced phases of the microbial colonization process, the in situ secretion of extracellular proteins might also be observed. This leads to the intensification of the microbial attachment process by anchoring the single cells on the contact surface [56]. It should be noticed that it is unclear how long the cells within the biofilm matrix excretes these molecules [57].
It is known that EPS is an irreversible foulant but it can be removed from the surface of the membrane by specific enzymes (i.e., proteases and polysaccharides) and thus prevent biofilm formation [58,59,60,61]. Enzymatic cleaning has disadvantages that limit its large scale application. These limitations are: (i) dependence of enzyme activity on pH, temperature and salt concentration; (ii) high costs of enzyme production, and (iii) the difficulty of recovering the enzyme from the aqueous medium [62]. Moreover, EPS usually consists of a mixture of macromolecules, so its removal from the surface of the membrane required several enzymes [63].
It should be noticed that mature biofilm was persistent and difficult to eliminate also by chemical cleaning [64]. Rapid regrowth of the microbes attached to the surface was observed and therefore more frequent chemical cleaning is inevitable leading to the increased consumption of chemical cleaning agents and increased wastewater production. Frequent chemical cleaning also shortens the life of the membrane [65].
The SEM micrographs of the tested membranes after 24-h contact with the activated sludge (left photos) and the same membranes after 10 min of plasma treatment (right photos) are presented in Figure 6. It seems that the structure of the biofilms formed on the studied membranes is slightly different. More biological material has adhered to the surface of the polyamide membrane. This observation can be direct evidence that polyamide membranes are better in terms of microbial adhesion and biofouling than cellulose acetate membranes.
As can be seen, the nonthermal plasma is extremely effective in removing biofilm formed on the polymeric surface. Only a slight contamination of the membranes is visible. Moreover, no damage to the membranes was found after plasma treatment.
Our results showed that the fluorescence microscopy was an effective tool to prove the influence of nonthermal plasma treatment on bacteria cells. Fluorescence microscopy images of a biofilm formed on a cellulose acetate (CA) membrane before and after 10-min nonthermal plasma treatment are shown in Figure 7. SYTOX Green stain was used for a microbial viability assessment. It was previously described that SYTOX Green stain is a high-nucleic acid compound, which does not penetrate through the membranes of living cells, and at the same time easily enters cells with plasma-damaged membranes [66]. Thus, nonviable cells are accessible to SYTOX Green and appear green. The obtained images indicated that the number of nonviable cells (for both membranes) correlated with the time of the exposure to nonthermal plasma (data not shown). High cell mortality after 5–10 min (corresponding to 21–42 J cm−2) of the plasma treatment was especially visible.
It is documented that the use of nonthermal plasma does not involve harmful chemical substances and it seems to be an interesting technique of cleaning the surface of membranes used in wastewater treatment. Moreover, the results demonstrated by Hong et al. showed that plasma treatment not only inactivates the biofilm but also inhibits biofilm re-growth after surgery [67]. The authors re-cultured plasma-treated biofilms of Streptococcus mutans and observed interesting changes in the physiological activity of these bacteria. The obtained results of crystal violet (CV) staining, biofilm sludge production, and quantitative assessment of genomic DNA showed that the number of recovered bacteria in plasma-treated biofilms was significantly reduced. It is reported that it is very difficult to completely prevent biofilm recovery after removal of treatments, and therefore the plasma inhibition of biofilm recovery may be crucial for the effective control of the deposition and accumulation of different molecules and living cells on the filter membrane.

4. Conclusions

The fouling process caused by microorganisms has, unfortunately, great potential to reduce the operating efficiency and durability of membranes. Thus, contaminated membranes need to be cleaned to maintain their required properties. The efficiency of the biofouling removal can be significantly increased by the appropriate plasma dose. Comparing the results of membrane decontamination tests, it can be concluded that plasma treatment exhibits the highest biofouling removal efficiency for short membrane surface contact times (i.e., regardless of the membrane type) with bacterial cells.
According to the research on the influence of plasma on extracellular polymeric substances, it can be observed that the amount of proteins released from tested biofilms depends on the time of biofilm formation and the type of membrane on which the biofilm is located.
The proposed method of plasma cleaning of membranes covered with biological contaminants seems to be very attractive from the economic point of view. Taking into account the energy consumption of the process, it can be concluded that the cost of treatment of 1 square centimeter of a membrane with nonthermal plasma was 1.2 × 10−5 of the energy cost that is set in the EU at a level of 0.16 Euro per kWh for non-household users. The provided data indicate that there is a great potential for the application of a nonthermal plasma in wastewater treatment plants (WWTPs).
The presented studies have confirmed the great possibilities of using nonthermal plasma in the process of membrane cleaning and limiting the biofouling process. It appears that there is a reasonable opportunity to apply plasma in the so-called membrane reactors. Membrane bioreactors (or membrane biological reactors, MBRs) are widely used in wastewater treatment processes linking a membrane process (e.g., microfiltration or ultrafiltration) and a biological process (e.g., the activated sludge). The membrane bioreactor (MBR) has become an effectively integrated technology for the treatment of municipal and industrial wastewater. The main disadvantage limiting the extended use of MBRs is the contamination of the membranes (i.e., fouling), which substantially affects the performance and lifetime of the membranes, and consequently leads to an increase in maintenance and operating costs. Our aim was to apply the plasma method of limiting the biofouling process appearing in a system containing membranes to maintain their initial filtration properties. Plasma can ensure that the high efficiency of membranes is maintained over a long period in MBRs.
Considerably more work involving studies on modifications of the structure of the membranes caused by nonthermal plasma treatment is required. These efforts are currently in progress.

Supplementary Materials

The following are available online at https://www.mdpi.com/1996-1073/13/17/4318/s1, Figure S1: The colonization of polyamide membrane (PA) and cellulose acetate membrane (CA) by microbes of the activated sludge. Average ± SD of three independent experiments are shown.

Author Contributions

Conceptualization, I.M.; methodology, I.M. and T.C.; validation, I.M. and T.C.; formal analysis, I.M. and T.C.; investigation, I.M. and T.C.; resources, I.M. and T.C.; writing—original draft preparation, I.M. and T.C.; writing—review and editing, I.M. and T.C.; visualization, T.C.; funding acquisition, I.M. and T.C. All authors have read and agreed to the published version of the manuscript.

Funding

This research received no external funding. This work was financed by a statutory activity subsidy from the Polish Ministry of Science and Higher Education (PMSHE) for the Department of Organic and Medicinal Chemistry and Department of Electrical Engineering Fundamentals of Wroclaw University of Science and Technology.

Conflicts of Interest

The authors declare no competing financial interest.

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Figure 1. Schematic diagram of the system for testing the adhesion process with activated sludge.
Figure 1. Schematic diagram of the system for testing the adhesion process with activated sludge.
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Figure 2. DBD plasma reactor: schematic view of the DBD configuration (A), a model of the plasma reactor (B), electrical discharges (i.e., nonthermal plasma) in the reactor (C).
Figure 2. DBD plasma reactor: schematic view of the DBD configuration (A), a model of the plasma reactor (B), electrical discharges (i.e., nonthermal plasma) in the reactor (C).
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Figure 3. The effect of nonthermal plasma on the destruction of viable microbial cells forming fouling after 4-h contact of the activated sludge with: (A) polyamide membrane (PA); (B) cellulose acetate membrane (CA).
Figure 3. The effect of nonthermal plasma on the destruction of viable microbial cells forming fouling after 4-h contact of the activated sludge with: (A) polyamide membrane (PA); (B) cellulose acetate membrane (CA).
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Figure 4. The effect of nonthermal plasma on the destruction of viable microbial cells forming fouling after 24-h contact of the activated sludge with: (A) polyamide membrane (PA); (B) cellulose acetate membrane (CA).
Figure 4. The effect of nonthermal plasma on the destruction of viable microbial cells forming fouling after 24-h contact of the activated sludge with: (A) polyamide membrane (PA); (B) cellulose acetate membrane (CA).
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Figure 5. The effect of nonthermal plasma on the destruction of viable microbial cells forming fouling after 24-h contact of the activated sludge with: (A) polyamide membrane (PA); (B) cellulose acetate membrane (CA).
Figure 5. The effect of nonthermal plasma on the destruction of viable microbial cells forming fouling after 24-h contact of the activated sludge with: (A) polyamide membrane (PA); (B) cellulose acetate membrane (CA).
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Figure 6. SEM images of cellulose acetate (A) and polyamide (B) membranes: after 24 h contact with the activated sludge (left) and after 10 min of the non-thermal plasma treatment (right).
Figure 6. SEM images of cellulose acetate (A) and polyamide (B) membranes: after 24 h contact with the activated sludge (left) and after 10 min of the non-thermal plasma treatment (right).
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Figure 7. Fluorescence microscopy images of a biofilm formed on a cellulose acetate (CA) membrane before (A) and after 10-min nonthermal plasma treatment (B). Images obtained at a magnification of 20.
Figure 7. Fluorescence microscopy images of a biofilm formed on a cellulose acetate (CA) membrane before (A) and after 10-min nonthermal plasma treatment (B). Images obtained at a magnification of 20.
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Table
Table 1. The protein released from PA/CA membranes into the water after the nonthermal plasma treatment [%].
Table 1. The protein released from PA/CA membranes into the water after the nonthermal plasma treatment [%].
Time of Treatment/Energy Dose (J cm−2)Biofilm Cells (24 h)Biofilm Cells (72 h)
% of the Total Proteins Detected in Water
3/~1340 ± 2/45 ± 248 ± 2/49 ± 3
5/2165 ± 2/69 ± 363 ± 3/71 ± 2
7/~2974 ± 3/79 ± 279 ± 3/84 ± 2
10/~4282 ± 2/86 ± 285 ± 3/90 ± 2

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Maliszewska, I.; Czapka, T. Biofouling Removal from Membranes Using Nonthermal Plasma. Energies 2020, 13, 4318. https://doi.org/10.3390/en13174318

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Maliszewska I, Czapka T. Biofouling Removal from Membranes Using Nonthermal Plasma. Energies. 2020; 13(17):4318. https://doi.org/10.3390/en13174318

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Maliszewska, Irena, and Tomasz Czapka. 2020. "Biofouling Removal from Membranes Using Nonthermal Plasma" Energies 13, no. 17: 4318. https://doi.org/10.3390/en13174318

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