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Recent Advances in Biotechnologies for the Treatment of Environmental Pollutants Based on Reactive Sulfur Species

State Key Laboratory of Urban Water Resource and Environment, School of Environment, Harbin Institute of Technology, Harbin 150090, China
College of Biological Engineering, Beijing Polytechnic, Beijing 100176, China
Department of Chemical Engineering, National Taiwan University, Taipei 106, Taiwan
Author to whom correspondence should be addressed.
Antioxidants 2023, 12(3), 767;
Received: 21 February 2023 / Revised: 19 March 2023 / Accepted: 20 March 2023 / Published: 21 March 2023
(This article belongs to the Special Issue Reactive Sulfur Species in Microorganisms)


The definition of reactive sulfur species (RSS) is inspired by the reactivity and variable chemical valence of sulfur. Sulfur is an essential element for life and is a part of global geochemical cycles. Wastewater treatment bioreactors can be divided into two major categories: sulfur reduction and sulfur oxidation. We review the origins of the definition of RSS and related biotechnological processes in environmental management. Sulfate reduction, sulfide oxidation, and sulfur-based redox reactions are key to driving the coupled global carbon, nitrogen, and sulfur co-cycles. This shows the coupling of the sulfur cycle with the carbon and nitrogen cycles and provides insights into the global material−chemical cycle. We also review the biological classification and RSS metabolic mechanisms of functional microorganisms involved in the biological processes, such as sulfate-reducing and sulfur-oxidizing bacteria. Developments in molecular biology and genomic technologies have allowed us to obtain detailed information on these bacteria. The importance of RSS in environmental technologies requires further consideration.

1. Introduction

Hydrogen sulfide from violent movements of the Earth’s crust (e.g., volcanic eruptions) provided the energy, reducing power, and material basis for the origin of life about 3.8 billion years ago [1,2]. The ensuing anoxygenic and oxygenic photosynthesis led the Earth into an era known as the “great oxidation event” (GOE) [3]. The hypothesis of “ox-tox” is that early living organisms evolved antioxidant defense systems (e.g., superoxide dismutase, catalase, peroxiredoxins, thioredoxin, and glutaredoxin) to counteract the abundance of oxygen [4]. Sulfide-based biochemical reactions persist in modern times, not as a primary source of energy, but as a regulator of metabolism and signaling. This basis to create, regulate, and maintain life activities is redox reactions, such as photosynthesis and respiration [2].
Reactive oxygen species (ROS), reactive nitrogen species (RNS), and reactive nitrogen oxides (RNOS) are highly oxidizing, destroying redox-sensitive proteins and enzymes and attacking membranes and DNA [5]. Anti-oxidation is a core topic in physiological and biochemical research, and the attention of researchers has shifted from oxygen to sulfur. Sulfur-containing materials are generally considered to exist naturally as antioxidants (e.g., hydrogen sulfide and glutathione). The definition of reactive sulfur species (RSS) emerged in 2001 and research has focused on physiological, biochemical, and protein molecular functions. Previous reviews described the active chemical properties and physiological effects of RSS [6,7]. The sulfur cycle is an important part of global geochemical cycles (Figure 1) [8,9], but what role does RSS play in the field of environmental technology?
In this review, we detail the relationship between RSS and pollutants, environmental technologies, and metabolic mechanisms. The review emphasizes the prevalence and importance of RSS in environmental technologies and provides an outlook on application prospects and future development of RSS.

2. RSS Definition and Relationship with Environmental Management

2.1. Origins and Definition of RSS

Giles et al. first defined RSS by presenting it as an oxidative-stress product and juxtaposing it with ROS, RNS, and RNOS [10]. Later, Brannan and Gruhlke amended the definition of RSS to “sulfur-containing molecules capable of oxidizing or reducing the oxidative reactive activity of biological macromolecules under physiological conditions” [11,12]. This definition does not include environmental microorganisms. This is because, for many simple chemoautotrophic microorganisms, the source of energy for survival is inorganic matter or sunlight. In these cases, in addition to hydrogen sulfide, inorganic reduced sulfur substances, such as elemental sulfur (S0), can serve as an electron donor or electron acceptor for growth. From this perspective, S0 has properties similar to those of RSS, which is susceptible to oxidation or reduction by biological processes. We suggest that RSS should be defined more broadly to include sulfur-containing molecules which are bioavailable and susceptible to redox reactions. The chemical valence states of the sulfur atoms in the typical sulfur-containing compounds are summarized in Table 1. This review is particularly focused on sulfide, S0, polysulfide, sulfur dioxide, and sulfate.

2.2. Relationship between RSS and Environmental Pollutant Management

Sulfur is the 10th most common element in the universe, the 15th most common element in the Earth’s crust, and the 7th most common element in biology [13]. Its main forms are pyrite (FeS2) and gypsum (CaSO4) in the ground and free sulfate in the ocean. It has a valence state of −2 to +6, and is more stable at even numbers. H2S (−2), the most reduced form of sulfur, is characterized by a rotten-egg odor, typical of RSS. In aqueous environments, it exhibits properties of a dibasic weak acid. Despite the similarity to H2O, the transmembrane behavior is different, with H2S in the ionic form of HS by simple free diffusion [14,15]. The anaerobic environment is favorable for the generation and aggregation of H2S. With anthropogenic intervention, sulfide-containing wastewater is often observed in industrial plant wastewater, e.g., petrochemical plants, tanneries, synthetic fiber manufacturers, or coal gasification power plants. Therefore, the release of H2S into the environment, as dissolved sulfide in wastewater or as H2S in flue gases, is controlled for environmental protection.
S0 is one of the major sulfur pools in the global sulfur cycle. Chemically generated S0 has low water solubility (5 μg/L, 25 °C), with the bio-generated form being hydrophilic and more bioavailable [16]. As a non-corrosive solid that is environmentally friendly and easy to handle and transport, S0 is pursued as a target for sulfur-containing pollution treatment. Its commercial value exceeds that of sulfuric acid, even though both can be used in chemical processes and fertilizer production [17].
Polysulfides (RSnR, RSnH, H2Sn; n ≥ 2), highly reactive chemical intermediates, often accompany the oxidation of sulfides and the bioavailability of sulfur, and are also typical of RSS [18]. The hypothetical polysulfide generation process is shown in Figure 2 [19]. Similar to S0, polysulfides can act as both electron acceptors and electron donors. Polysulfides, rather than hydrogen sulfide, play an important role in intracellular antioxidation, persulfide modification, and signaling [20,21,22]. S0 and polysulfides are important as intermediate products of the global sulfur cycle in different sulfur reservoirs and isotope fractionations.
SO2(+4) is a toxic, colorless, environmental pollutant. It has a wide range of sources, such as coal-fired processes in power plants, incinerators, and boilers. The dispersion of sulfur dioxide gas into the atmosphere causes photochemical smog, acid rain, stratospheric ozone depletion, and fine particulate matter, causing serious harm to ecosystems and corroding the metal components of industrial equipment [23]. Efforts have focused on the development of qualified technologies to eliminate SO2 from coal-combustion flue gas. Flue-gas exhaust contains some CO, nitrogen oxides (NOX), and small amounts of O2 in addition to SO2 [24]. Developing technologies for integrated methods of treating multiple greenhouse gases remains a global priority.
Sulfate (+6), one of the main forms of sulfur in nature, is a type of secondary pollutant due to its anaerobic reduction products [25]. Sulfate-laden wastewater is characterized by a long latent period and is difficult to treat. Wastewater with high untreated sulfate levels causes acidification of surface and groundwater, damage to soil structure, and reduction of crop yield [26]. High sulfate concentrations lead to off-flavors (>400 mg L−1) and diarrhea (1000–1200 mg L−1) [27]. The development of high-sulfate wastewater treatment technologies with solid elemental sulfur as a recovery target is important.

3. RSS-Related Bioprocesses for the Treatment of Environmental Pollutants

A central issue in wastewater treatment is nitrogen removal [28]. Excess nitrogen causes eutrophication, has a toxic effect on aquatic plants and animals, and contaminates drinking water sources [29]. Biological denitrification stands out for its low operating costs and environmental friendliness. In this process, both autotrophic and heterotrophic bacteria play roles separately or together. The SANI (sulfate reduction−autotrophic denitrification−nitrification integrated) process is successful in practical municipal wastewater treatment, especially in terms of energy and sludge reduction (Figure 3) [30]. We review wastewater treatment mediated by sulfur-containing substances, categorized by main sulfur species, focusing on the main functional microorganisms, functional genes, and metabolic mechanisms. In addition to the SANI process, other types of reactors, such as membrane reactors and elemental sulfur packed-bioreactor, are covered. Some of the treatment processes that involve exhaust gas treatment are also discussed.

3.1. Sulfur-Reduction-Based Biological Treatment

3.1.1. Sulfate-Reduction Bioreactors

Sulfate can be used as an alternative terminal electron acceptor under anaerobic conditions, except for oxygen, nitrate, Mn (IV), and Fe (III), which provide higher energy yields. Therefore, sulfate reduction is not only an important part of the global sulfur cycle but is also applied in wastewater treatment. The use of sulfate-reducing bacteria (SRB) for the treatment of high-sulfate wastewater is appropriate, given the potential threat of excessive sulfate emissions to the environment. To the best of our knowledge, the sulfate respiration of SRB relies on a variety of electron donors, such as formate, acetate, butyrate, and H2, with sulfide as the end product [31,32]. Sulfate-reduction bioreactors are used in single or multi-stage systems for full-depth treatment of wastewater, depending on the purpose of the treatment.
Bio-sulfate-reduction technology for the removal and recovery of valuable metals is critical [33]. Metallic wastewater from acid mine drainage (AMD) and heavy industries, such as metallurgy and steel manufacturing, has low pH and COD (chemical oxygen demand), high sulfate, and high heavy metals [34]. The advantages of using SRB to precipitate metals include (1) SRB have a broad spectrum of pH adaptability and can perform sulfate reduction at low pH to produce sulfides, (2) high sensitivity of sulfide precipitation reactions and high recoverability, and (3) low cost. Treatment of antimony (Sb) mine drainage is regarded as a priority by regulators, and sulfate-reduction bioreactors have great potential for Sb removal [35]. Up to 98.3% antimony removal is achieved in SRB reactors with Fe(II) participation, and soluble Sb(V) is reduced to Sb(III) and precipitated as pyroxene (Sb2S3) [36]; a typical strain of SRB enriched therein is Desulfovibrio sp. Macroscopically, SRB utilizes the organic compounds in wastewater to provide electrons for sulfate reduction, which results in the production of sulfides that combine with metal ions to form insoluble precipitates. These reactions can be expressed by two equations:
2CH2O + SO42− + 2H+ → H2S + 2CO2 + 2H2O
H2S + M2+ → MS + 2H+
where M is a metal, e.g., Mn, Pb, Cu, Cd, or Ni. Sulfate reduction is an alkalinity-producing process that is advantageous in biologically neutralizing acidic wastewater and for ecological restoration. The major problems associated with the anaerobic treatment of high-sulfate wastewater are related to the production of sulfides. In addition to the precipitation of metals, sulfide can also be used as a feedstock for subsequent bioreactors. Sulfide oxidation used for wastewater treatment is summarized in Section 3.2.
Besides AMD wastewater, sulfate-reduction biotechnology is applied to other types of wastewater, such as antibiotic-containing pharmaceutical or phenol-containing paper-mill wastewater. Ciprofloxacin (CIP) is a fluoroquinolone antibiotic that is widely used in human and animal manufacturing. It has strong antibacterial effects in the treatment of human tuberculosis and urinary tract and respiratory tract infections, as well as in animal husbandry and farming [37]. Jia et al. found that sulfate-reduction biotechnology has great potential to treat wastewater containing CIP [38]. At low concentrations CIP is adsorbed by secreting extracellular polymeric substances (EPS), thus avoiding the toxic effects of antibiotics on microorganisms—with increasing CIP concentrations, CIP-resistant Desulfobacter are enriched. The CIP biodegradation pathway dependent on cytochrome P450 enzymes and acetylases was validated in an SRUSB (sulfate-reducing up-flow sludge bed) reactor [39].
Other examples are phenols and their derivatives present in wastewater from textile, paper, plastic, and cosmetic industries, as well as in industrial phenol leaks and exhaust gases from construction and renovation [40]. Because of their toxicity and carcinogenicity, phenol substances may cause pollution, which has attracted widespread attention from the scientific community and the public. Anaerobic treatment of phenol-containing wastewater is mostly performed in UASB (up-flow anaerobic sludge blanket) reactors [41]. Guo et al. achieved up to 90% phenol removal using a UASB reactor based on sulfate reduction [42]. Sequencing 16s DNA showed that Clostridium spp. and Desulfotomaculum spp. were the major phenol-degrading bacteria. Dephosphorylation and acidification are known to be the main pathways of phenol biodegradation [43].

3.1.2. Sulfate-Reducing Bacteria (SRB) and Molecular Mechanisms

Sulfate-reducing bacteria, an artificial taxonomic designation according to function, comprise a diverse group of anaerobic microorganisms with a wide range of fermentation-product metabolism capabilities [44,45]. SRB are distributed in more than 220 species in 60 genera of five phyla of bacteria and two divisions of archaea [46,47]. Bacteria taxa include Desulfovibrio, Desulfotomaculum, and Desulfosporomus in phylum Firmicutes, Thermodesulfovibrio of phylum Nitrospira, and Thermodesulfobacterium. For archaea, the euryarchaeota genus Archaeoglobus and the two crenarchaeotal genera Thermocladium and Caldivirga are dominant. The dominant SRB vary in different bioreactors. For example, in an expanded granular sludge bed (EGSB) reactor capable of carbon, nitrogen, and sulfur co-removal operated by Chen, the dominant strain of SRB was Desulfomicrobium sp. [48]. Desulfomicrobiaceae and Desulfobulbaceae are the two dominant SRB taxa in sulfate-reduction and organic-matter-removal units [49]. Two new species were defined in the sulfate-reducing ammonia anaerobic oxidation (SRAO) process, Anammoxoglobus sulfate and Bacillus benzoevorans, which possess the ability to simultaneously eliminate ammonia and sulfate [50].
Regardless of the environment or bioreactor, a common set of dissimilatory sulfate-reduction pathways (also called ‘‘sulfate respiration’’) are shared by functional SRB as shown in Figure 4 [51,52,53]. Sulfate is taken up from the environment via sulfate transporters and activated by the enzyme ATP sulfurylase (Sat) to form adenosine-5′-phosphosulfate (APS). Then APS is reduced to sulfite through adenylyl-sulfate reductase (Apr), which accepts electrons from the electron transport complex (ETC) in the membrane. The dissimilatory (bi)sulfite reductase (DSR) complex further reduces the (bi)sulfite to H2S, which diffuses passively out of cell membranes. Besides the dissimilatory sulfate-reduction pathway, there is an assimilatory sulfate pathway in SRB [54,55]. Both share the same initial step of sulfate activation by ATP—the difference is that assimilatory sulfate reduction requires the transfer of phosphate to adenosine-5′-phosphate sulfate (APS) by adenylate kinase to produce phosphoryl adenosine-5′-phosphate sulfate (PAPS). This continues to be decomposed by NADPH2 to produce SO32− and, finally, a cysteine is formed from SO32− by sulfite reductase.
The enzymatic reaction of sulfate reduction is reversible due to the intermediate products and substrate concentrations. This explains sulfur isotope fractionation [56,57]. Genes dsrA and dsrB are regarded as the characteristic key functional genes of SRB, and they have been used to investigate the distribution and abundance of SRB in colonies [58]. Specific inhibition of sulfate reduction by molybdate or selenate has been experimentally demonstrated, and this has been used to study the contribution of different electron donors to sulfate reduction [59].
In addition to temperature and pH, two basic physicochemical indicators that directly affect the activity of SRB substrate carbon supply are to be considered for sulfate-reduction biotechnology: (1) SRB are mostly heterotrophic in metabolism and (2) different types of SRB utilize different carbon sources [44]. Therefore, the provision of suitable carbon sources is of significance to improve the efficiency of SRB reactors. Scientific research mostly uses a single carbon-source culture, but it is expensive. In large-scale applications, such as industrial wastewater treatment, alternative efficient and inexpensive carbon source supplies must be considered. Mixing multiple carbon sources is common. Steel slag, sugarcane bagasse, fruit and vegetable wastewater, and sugar by-products have been introduced as cheap carbon sources [60,61]. In anaerobic wastewater treatment, methanogenic bacteria compete with sulfate-reducing bacteria for hydrogen and acetic acid (both are prerequisites for methane formation and electron donors for sulfate reduction) [62,63]. Providing suitable reaction conditions and controlling the activity of methanogenic bacteria are also important to improve sulfate-reducing bioreactors [64].

3.1.3. S0-Based Reduction Bioreactors

Sulfur-packed bioreactors have significant advantages in treating both high-rate COD wastewater and low C/N ratio domestic wastewater by avoiding high activated-sludge yields [65,66]. Sulfur-packed bioreactors can be categorized into two major types according to the electron valence change of sulfur. One is as electron acceptors, mainly used in the treatment of high-organic-carbon wastewater and hazardous metal-laden wastewater [65,67]. The other is as electron donors for in-depth denitrification of drinking-water resources and wastewater with a low C/N ratio (see Section 3.2.3) [68]. These technologies provide a more cost-effective solution to the environmental problems in current wastewater treatment.
The S0-based reduction bioreactor is an efficient anaerobic wastewater treatment process that reduces sludge production and avoids the excess activated sludge problem commonly faced by wastewater plants [69]. A laboratory-scale sulfur-reducing anaerobic fluidized bed (SRAFB) reactor built by Zhang et al. achieved high organic removal rates with a sludge yield of only 16% (VSS per kg COD) [70]. Sulfide in the effluent can be recovered by micro-aeration biological treatment, an internal sulfur cycling process (ISC). An ISC system achieved 94% removal at 300 mg/L COD after 200 days of continuous operation, and 76% recovery of sulfide in the effluent was recovered in the form of elemental sulfur after 200 days of continuous operation [71].
Emerging sulfur-reduction biotechnology requires only two electrons for the sulfidation of elemental sulfur, theoretically reducing organic consumption by 75%. Sulfur reduction can reduce organic carbon by 66–80% compared to sulfate reduction when producing equivalent amounts of sulfide [67]. Li et al. performed a pilot-scale sulfur reduction bioreactor to handle practical domestic wastewater, coupling Cu-laden electroplating wastewater treatment [72]. The results achieved 99% removal of Cu2+, indicating that sulfur reduction is a sustainable sulfide generation technology with great potential for application.
Mercury and arsenate removal is also critical for S0-based reduction bioreactors. Arsenite (III) is more mobile and toxic than arsenate (V) and both are culprits of arsenic contamination in groundwater. Sulfide precipitation is the ideal means of biological arsenic removal [73]. Because sulfate reduction is alkali-producing, the by-product thioarsenite (As(OH)S22−) is produced [74]. Therefore, sulfur-reduction technology under acidic conditions is considered a prospective alternative because it produces large amounts of sulfide while minimizing pH increases. Sun et al. verified that an S0-based reduction bioreactor could produce high sulfide yields (0.42 ± 0.2 kg S/m3-d) under acidic conditions (pH~4.3) while achieving 99% removal of arsenite without the formation of soluble thioarsenite [75].
2H3AsO3 + 3HS → As2S3 + 3H2O + 3OH
H3AsO3 + HS + 2H+ → AsS + 3H2O
As2S3 + HS + 3OH → 2As(OH)S22− + H2O
Sulfur-reduction technology also has the potential for treating mercury (II) in aqueous environments. Mercury (II) is highly toxic and can be removed by the formation of insoluble precipitates with biogenic sulfides. Sulfate reduction, however, does not achieve desired mercury removal because SRB promotes the production of the more toxic methylmercury (MeHg) in the presence of organic matter and sulfate [76]. Wang et al. performed successive experiments on mercury-laden wastewater and found that the use of S0-based reduction bioreactors completely removed mercury (II) (up to 50 mg/L) without forming neurotoxic MeHg [77]. However, the causes and mechanisms for no by-product MeHg production in this process are not clear.
Sulfur-packed bioreactors have also been used in flue-gas treatment. SO2 has high solubility (11.29 g SO2/100 g H2O), whereas NO, which is the major component of NOx, does not (0.00618 g NO/100 g H2O). The traditional physical−chemical desulfurization and denitrification approach is wet flue-gas desulfurization (WFGD) for SO2 removal with selective catalytic reduction (SCR) of nitrogen oxides [23]. Reducing substances produced during wastewater treatment, such as ammonia, nitric oxide, and hydrogen sulfide, have been shown to act as reducing agents for flue-gas desulfurization and denitrogenation. Sun et al. developed a simultaneous catalytic desulfurization and denitrogenation (SCDD) technology based on sulfur cycling [78]. This technology takes the organic matter in wastewater as an electron donor and obtains high-rate sulfide by biological sulfur reduction; the resulting low-cost reductant (hydrogen sulfide) removes 90% of SO2 and NO from the flue gas, and the end product was elemental sulfur that was non-toxic and had economic recovery value.
Polysulfides have been found to participate in and accelerate the sulfur reduction in S0-based reduction bioreactors. As a product of the nucleophilic attack of sulfur hydrogen ions on elemental sulfur, polysulfides are a key intermediate in sulfur reduction and they enhance the bioavailability of sulfur. Polysulfides were also found by Zhang et al. in their laboratory-scale, sulfur-reducing anaerobic fluidized bed (SRAFB) bioreactor for wastewater treatment [70]. The small initial amount of sulfide promoted the production of polysulfide, which accelerated the reduction of elemental sulfur, forming a polysulfide-mediated self-accelerating chain reaction. Qiu et al. suggested that a novel polysulfide-involved SADN (PiSADN) process achieved a high rate of autotrophic nitrate removal [79]. In this process, sulfur disproportionation is considered to be the key to driving PiSADN, where disproportionation generates sulfides, which, in turn, promote the formation of polysulfides.
HS + (n − 1) S0 → Sn2− + H+
4S0 + 4H2O → SO42− + 3HS + 5H+
ΔG0 = 240.2 kJ/mol

3.1.4. Sulfur-Reducing Bacteria (S0RB) and Molecular Mechanisms

Elemental sulfur reduction to sulfide coupled with inorganic phosphorylation of ADP is known as sulfur respiration [80]. Since the discovery of sulfur respiration in Desulfuromonas acetoxidans, more bacteria that can catalyze elemental sulfur reduction have been discovered. Sulfur-reducing bacteria (S0RB) are distributed in both archaea and bacteria and have a wide range of habitats in nature, from extremely acidic hot seawater to superheated seafloor vents [80,81]. Because of this, the metabolism of S0RB exhibits high variability (Table 2).
There are at least two known mechanisms of sulfur respiration in S0RB (Figure 5) [96]. One is found in Wolinella succinogenes, in which the [NiFe]-hydrogenase (HydABC) oxidizes H2 and transfers electrons via methyl quinone to the periplasmic membrane-bound polysulfide reductase, PsrABC [80]. PsrA is responsible for polysulfide reduction to H2S, PsrB is an [FeS] electron transfer protein, and PsrC is a quinone-containing membrane anchor. In addition, a polysulfide transferase (Sud) protein is thought to be involved in the acquisition of sulfides from protons and sulfur. The other is the NAD(P)H elemental sulfur reductase (Nsr) that uses elemental sulfur as a substrate directly, rather than polysulfides, to reduce elemental sulfur by oxidizing NAD(P)H and releasing H2S [96].

3.2. Sulfur-Oxidation-Based Biological Treatment

3.2.1. Sulfide-Oxidation Bioreactors

Sulfide is highly reductive and serves as an energy source for some chemoautotrophic microorganisms. It is found in many scenarios, such as anaerobic treatment effluent of sulfate-laden wastewater, sulfidogenic treatment of acid mine drainage, petroleum refining industries, and pharmaceutical wastewater [34,37]. In the geochemical cycle, sulfide is re-oxidized back to sulfate via various oxidants, such as oxygen, nitrate, Mn (IV), Fe (III), and other chemical oxidants or bio-oxidizers, such as reductive sulfur substances oxidizing bacteria (SOB), through different sulfur intermediates (polysulfide, elemental sulfur, sulfite, thiosulfate, etc.). The degree of sulfide oxidation depends on the number of available chemical oxidants (e.g., oxygen and nitrate) and the species of SOB [62]. SOB is a group of microorganisms that utilize reduced sulfur substances (sulfide, elemental sulfur, or thiosulfate) and whose oxidation products are higher-valence sulfur-containing substances or sulfates. Due to the diversity of their nutrient metabolism types, they have long been used in wastewater treatment [97]. Practical wastewater systems contain organic carbon, nitrate nitrogen, and ammonia nitrogen in different concentrations, besides sulfurous substances. Therefore, various simultaneous desulfurization and denitrification technologies have been developed to deal with sulfurous wastewater pollution [98].
Denitrifying functional microorganisms are classified into two main groups depending on the electron donor. Processes using organic material are called heterotrophic denitrification (HD) and those using inorganic materials (e.g., Fe2+, Mn2+, H2, S2−, and S0) are called autotrophic denitrification (AD). The former has the advantage of rapid denitrification but disadvantages include sludge production, N2O emissions, and exogenous supplemental carbon sources. AD decreases sludge yield but has a long start-up period and slow bacterial growth [99]. The choice of autotrophic or heterotrophic denitrification, or a combination, depends on the type of wastewater being treated.
Autotrophic denitrification technology with sulfide as an alternative electron donor is applied to the desulfurization of biogas and denitrification of low C/N ratio wastewater. This can avoid the exogenous addition of carbon sources, and the intermediate oxidation product (elemental sulfur) is not a secondary pollutant and has economic value [100]. Therefore, the final treatment of sulfur-containing wastewater is often targeted at elemental sulfur. As shown in Figure 3, AD is the core technology unit in the SANI system, in which sulfide and nitrate are synchronously converted by microorganisms into sulfate and N2, thus achieving the goal of harmless and resourceful wastewater.
Biogas, a biomass energy source, has many advantages, such as high combustion value, simple preparation, sufficient raw materials, and low pollution; however, the formation of hydrogen sulfide as a by-product is inevitable [101]. Although the concentration of H2S is low, it will have a strong corrosive effect on metal pipes, instruments, internal combustion engines, etc. Moreover, it will produce SO2 after combustion, which will cause pollution. Therefore, desulfurization is an essential part of biogas purification [102,103]. The coupling of biogas desulfurization with deep denitrification of wastewater is increasingly common.
Similar to sulfur-containing wastewater treatment, biodesulfurization uses SOB to convert H2S in biogas into elemental sulfur or sulfate. Wang et al. proposed a new process using autotrophic denitrification coupled with biogas desulfurization [104]. The process uses H2S in biogas as the electron donor for wastewater denitrification and achieves deep nitrogen removal from wastewater and simultaneous purification of biogas without an additional carbon source. Even if the N/S parameters change, the removal rate of elemental nitrogen in the effluent can reach 100% and the removal rate of hydrogen sulfide remains above 91%.
The combination of autotrophs and heterotrophs has significant advantages in wastewater treatment, such as increasing the stability of the reactor network, compensating for insufficient organic carbons, and minimizing sludge yields. On this basis, integrated autotrophic heterotrophic denitrification (IAHD) is proposed for the treatment of organic wastewater containing nitrogen and sulfide, i.e., simultaneous carbon, nitrogen, and sulfur removal. Reyes-Avila et al. achieved simultaneous removal of nitrate (to N2), sulfide (to S0), and carbon (acetate to CO2) in a continuously stirred tank reactor (CSTR) using an incubated autotrophic heterotrophic symbiotic system [105]. The maximum removal rates were 0.209 kg N m−3 d−1, 0.294 kg S m−3 d−1, and 0.303 kg C m−3 d−1. Chen et al. used an EGSB to achieve high rates of bioconversion in synthetic wastewater, at loading rates of 3.0 kg S m−3 d−1, 1.45 kg N m−3 d−1, and 2.77 kg Ac m−1 d−1 [106]. Zhang et al. investigated the contribution of autotrophic and heterotrophic bacteria in an IAHD system and found that Thiobacillus was the key autotrophic desulfurization and denitrification bacterium at low sulfide levels, while other heterotrophic bacteria, such as Azoarcus and Pseudomonas, functioned at high sulfide concentrations [107].
Huang et al. achieved 78% recovery using a UASB reactor while ensuring 100% carbon, nitrogen, and sulfur co-removal [108]. Further, they developed a compact, biofilm-forming, membrane-filtration reactor (BfMFR) aimed at the rapid separation of the generated elemental sulfur from the biofilm by membrane filtration [109]. The high sulfur generation efficiency (98% on average) was stably maintained with feed water concentrations of 115, 120, and 100 mg/L for acetic acid, nitrate, and sulfide. Researchers found that the genera Thauera, Arcobacter, Pseudomonas, Azoarcus, Ochrobactrum, Alkiflexus, and Thiobacillus were prevalent and they were the core genera of denitrification desulfurization system [109].

3.2.2. Sulfide-Oxidation Bacteria (SOB) and Molecular Mechanisms

The biological oxidation of sulfides is an ancient metabolic mode and a common chemical reaction in extreme environments such as volcanoes and hot springs. The microorganisms that dominate these oxidation reactions are diverse and include various trophic groups of bacteria and archaea. Table 3 summarizes the taxonomy, nutrient types, and enzymes of several representative SOBs [110,111,112,113,114].
Colorless sulfur bacteria include Paracoccus, Hyphomicrrobium, Alcaligenes, Pseudomonas, Ochrobactrum, and Hydrogenobacter. Thiobacillus denitrificans is the most well-studied chemoautotrophic sulfide-oxidizing bacterium, capable of sulfide oxidation under aerobic and anaerobic conditions [127]. Primary sulfide-oxidation pathways include the sulfide−quinone oxidoreductase (SQR/PDO/ST) system, flavin cytochrome c dehydrogenase (FCSD), and Sox multi-enzyme oxidation system. Among them, SQR and FCSD are the dominant types of sulfide oxidases (Figure 6). There are six SQR systems distributed in animals, plants, and microorganisms [111,128]. SQR relies on its cofactor FAD to oxidize sulfide to zero-valent sulfur, and the resulting electrons enter the respiratory chain via coenzyme Q or methyl naphthoquinone on cell membranes. The resulting zero-valent sulfur reacts spontaneously with GSH in the presence of a suitable receptor (e.g., GSH) to form glutathione persulfide (GSSH), which is then oxidized to sulfite by persulfide dioxygenase (PDO) [129]. The zero-valent sulfur is temporarily bound to the conserved cysteine of SQR in the absence of a suitable receptor, and as the sulfide is oxidized; the zero-valent sulfur bound to SQR is eventually shed as S8. By contrast, FCSD is a heterologous flavoprotein dimer formed by the binding of two c-type cytochrome subunits encoded by the fccA and fccB genes, which are generally found in the microbial periplasmic space [130]. FCSD differs from the electron acceptor of SQR in that it uses cytochrome c as an electron acceptor to oxidize sulfide to zero-valent sulfur. The FCSD system is thought to be useful in areas of low sulfide concentration and, therefore, SQR is generally considered to be the primary sulfide-oxidation system (especially in high sulfide environments) [131]. Therefore, sqr, fccA, fccB, pdo, and sox are often queried as key characteristic genes or proteins in the distribution and diversity analysis of SOB.
The optimization of reactor operating parameters, such as temperature, pH, HRT, N/S ratio, and C/N ratio of the influent, directly affects the operating effectiveness of denitrification sulfide removal [132]. The rate of microbial-catalyzed sulfide oxidation is several orders of magnitude higher than chemical oxidation [133,134]. Researchers have demonstrated that microaerobic conditions (DO in the range of 0.2–1 mg L−1) can improve the sulfide tolerance of functional bacteria, promote the efficiency of biodesulfurization, and increase the elemental sulfur yield [135,136,137]. Macrogenomic results show that micro-oxygen promoted the abundance of genes responsible for sulfide metabolism (sqr, glpE (a typical sulfotransferase gene in Escherichia coli), pdo, sox, and cysK (Figure 4)) [138]. The formation of polysulfides is inevitable during the oxidation of sulfides [139].

3.2.3. S0-Based Oxidation Bioreactors

S0-based oxidation bioreactors are primarily applied for the intensive denitrification of low C/N ratio wastewater or groundwater for economic reasons. More importantly, sulfur autotrophic denitrification (SADN) emits less N2O than heterotrophic denitrification [140]. Sahinkaya performed a new SADN using a membrane bioreactor (MBR) to remove nitrate from drinking water [141]. Complete denitrification was achieved when the influent nitrate concentration was 25–50 mg NO3-N/L and the HRT was as low as 5 h. Zhang et al. achieved a removal efficiency of 4.0 g NO3-N/L·d using a novel sulfur-oxidizing autotrophic denitrifying anaerobic fluidized bed membrane bioreactor (AnFB-MBR). They found Thiobacillus, Sulfurimonas, and Ignavibacteriales to be the dominant sulfur-oxidizing bacterial genera [66]. Denitrification is alkalinity-depleting, so cheap and easily available materials, such as CaCO3 or crushed oyster shells, are good choices to neutralize alkalinity. SADN has been applied in wastewater treatment plants and for the production of drinking water [142].
S0-based oxidation bioreactors have also been applied for chromium removal from drinking water. Chromium contamination is not uncommon in industrial wastewater and groundwater [143]. In nature, hexavalent (VI) and trivalent (III) chromium are the main forms, the former is water soluble and strongly carcinogenic, and the latter is insoluble in neutral conditions. The main method of chromium removal from water bodies is to reduce Cr(VI) to Cr(III) [144]. After 60 days of operation, 92.9% removal of chromate was achieved with the reactor using elemental sulfur as the only electron donor.

3.2.4. Sulfur-Oxidation Bacteria (S0OB) and Molecular Mechanisms

Sulfur-oxidizing bacteria (S0OB) are microorganisms capable of directly using elemental sulfur as an electron donor. Due to the relevance of the metabolism of reduced sulfur species (sulfide, sulfite, thiosulfate), S0OB can oxidize the above-mentioned reducing sulfur species. Here, we review two known metabolic pathways for microbial elemental sulfur oxidation: the rDSR (reverse dissimilatory sulfite reductase) pathway and the Hdr (heterodisulfide reductase) pathway (Figure 7). The rDSR pathway involves several enzymes in dissimilatory sulfate reduction as mentioned in previous sections [145]. The sulfur atoms in elemental sulfur being sequentially transferred to the active site of rDSR through proteins Rhd, TusA, DsrEFH, and DsrC. The two active Cys of protein DsrC and the received sulfur atoms form a trisulfide peroxide catalyzed by the membrane-bound protein complex DsrMKJOP, and SO32− is produced by the DsrAB protein. In this process, low-molecular-weight organic persulfides (e.g., glutamine persulfide) are carriers for the transfer of sulfur from the periplasmic space to the cytoplasm. The Hdr pathway is a sulfur-atom-transfer pathway, similar to the rDSR pathway, which produces sulfite [146]. The difference is that the Hdr complex is a membrane-bound protein containing at least five subunits.

4. Prospects and Conclusions

This study highlights the scientific and environmental aspects of relying on the sulfur cycle for pollutant treatment by reviewing current advanced biotechnologies and the available molecular biological knowledge. Yet, there remains a gulf between currently known molecular mechanisms and practical biotechnological guidance. A better interplay between the two should be addressed in the future for both basic theoretical research and practical engineering applications. The relevant biological principles and mechanisms in biological treatment need to be optimized by calibrating operating parameters and elucidating more efficient microbial pathways.
RSS are involved in several biotechnological processes as an important intermediate in the microbially driven sulfur cycle. One of the challenges of RSS is the interconversion of different sulfur species through redox reactions, leading to the inability to accurately quantify them, especially polysulfides. The role played by RSS in environmental technology research is also complicated by the oxidative-stress products of functional microorganisms in bioreactors and their interactions with contaminants.
Some substantial advances have been made in sulfur-cycle-based biotechnology for wastewater treatment. A variety of sulfur-packed bioreactors are emerging and the development of single-stage bioreactors for the simultaneous removal of multiple pollutants is a future research direction. Sulfur-packed reactors show their superiority, but safety during transportation and storage should not be ignored.

Author Contributions

Writing—original draft, K.F.; revision of the manuscript, W.W.; finalization of the manuscript, X.X.; writing—review and editing, Y.Y., N.R., D.-J.L. and C.C.; funding acquisition, C.C. All authors have read and agreed to the published version of the manuscript.


The research was supported by the National Natural Science Foundation of China (Grant No. 52076063 and 52100035), the National Key Research and Development Program (No. 2019YFC0408503), the Fundamental Research Funds for the Central Universities (Grant No.HIT.OCEF.2021031), and the State Key Laboratory of Urban Water Resource and Environment (Harbin Institute of Technology) (No. 2022TS41).

Institutional Review Board Statement

Not applicable.

Informed Consent Statement

Not applicable.

Data Availability Statement

No data was used for the research described in the article.

Conflicts of Interest

The authors declare no conflict of interest.


  1. Raiswell, R.; Canfield, D.E. The iron biogeochemical cycle past and present. Geochem. Perspect. 2012, 1, 1–220. [Google Scholar] [CrossRef][Green Version]
  2. Olson, K.R.; Straub, K.D. The role of hydrogen sulfide in evolution and the evolution of hydrogen sulfide in metabolism and signaling. Physiology 2016, 31, 60–72. [Google Scholar] [CrossRef] [PubMed][Green Version]
  3. Schopf, J.W. Geological evidence of oxygenic photosynthesis and the biotic response to the 2400-2200 Ma “Great Oxidation Event”. Biochem.-Mosc. 2014, 79, 165–177. [Google Scholar] [CrossRef] [PubMed]
  4. Jones, D.P.; Sies, H. The Redox Code. Antioxid. Redox Signal. 2015, 23, 734–746. [Google Scholar] [CrossRef][Green Version]
  5. Grman, M.; Nasim, M.J.; Leontiev, R.; Misak, A.; Jakusova, V.; Ondrias, K.; Jacob, C. Inorganic reactive sulfur-nitrogen species: Intricate release mechanisms or cacophony in yellow, blue and red? Antioxidants 2017, 6, 14. [Google Scholar] [CrossRef][Green Version]
  6. Giles, G.I.; Jacob, C. Reactive sulfur species: An emerging concept in oxidative stress. Biol. Chem. 2002, 383, 375–388. [Google Scholar] [CrossRef]
  7. Olson, K.R. Reactive oxygen species or reactive sulfur species: Why we should consider the latter. J. Exp. Biol. 2020, 223, 196352. [Google Scholar] [CrossRef]
  8. Czerewko, M.A.; Cripps, J.C.; Reid, J.M.; Duffell, C.G. Sulfur species in geological materials—sources and quantification. Cem. Concr. Compos. 2003, 25, 657–671. [Google Scholar] [CrossRef]
  9. Fike, D.A.; Bradley, A.S.; Rose, C.V. Rethinking the Ancient Sulfur Cycle. In Annual Review of Earth and Planetary Sciences; Jeanloz, R., Freeman, K.H., Eds.; Annual Reviews: Palo Alto, CA, USA, 2015; Volume 43, pp. 593–622. [Google Scholar]
  10. Giles, G.I.; Tasker, K.M.; Jacob, C. Hypothesis: The role of reactive sulfur species in oxidative stress. Free Radic. Biol. Med. 2001, 31, 1279–1283. [Google Scholar] [CrossRef]
  11. Brannan, R.G. Reactive sulfur species act as prooxidants in liposomal and skeletal muscle model systems. J. Agric. Food Chem. 2010, 58, 3767–3771. [Google Scholar] [CrossRef]
  12. Gruhlke, M.C.H.; Slusarenko, A.J. The biology of reactive sulfur species (RSS). Plant Physiol. Biochem. 2012, 59, 98–107. [Google Scholar] [CrossRef] [PubMed]
  13. Ingenbleek, Y. The nutritional relationship linking sulfur to nitrogen in living organisms. J. Nutr. 2006, 136S, 1641S–1651S. [Google Scholar] [CrossRef] [PubMed][Green Version]
  14. Stein, A.; Bailey, S.M. Redox biology of hydrogen sulfide: Implications for physiology, pathophysiology, and pharmacology. Redox Biol. 2013, 1, 32–39. [Google Scholar] [CrossRef][Green Version]
  15. Czyzewski, B.K.; Wang, D. Identification and characterization of a bacterial hydrosulphide ion channel. Nature 2012, 483, 155–494. [Google Scholar] [CrossRef] [PubMed][Green Version]
  16. Maki, J.S. Bacterial intracellular sulfur globules: Structure and function. J. Plant Biochem. Biotechnol. 2013, 23, 270–280. [Google Scholar] [CrossRef]
  17. Chen, Z.; Xia, Y.; Liu, H.; Liu, H.; Xun, L. The mechanisms of thiosulfate toxicity against Saccharomyces cerevisiae. Antioxidants 2021, 10, 646. [Google Scholar] [CrossRef] [PubMed]
  18. Xu, H.; Xuan, G.; Liu, H.; Xia, Y.; Xun, L. Sulfane sulfur is a strong inducer of the multiple antibiotic resistance regulator MarR in Escherichia coli. Antioxidants 2021, 10, 1778. [Google Scholar] [CrossRef]
  19. Toohey, J.I.; Cooper, A.J.L. Thiosulfoxide (sulfane) sulfur: New chemistry and new regulatory roles in biology. Molecules 2014, 19, 12789–12813. [Google Scholar] [CrossRef][Green Version]
  20. Lau, N.; Pluth, M.D. Reactive sulfur species (RSS): Persulfides, polysulfides, potential, and problems. Curr. Opin. Chem. Biol. 2019, 49, 1–8. [Google Scholar] [CrossRef]
  21. Zhang, X.; Xin, Y.; Chen, Z.; Xia, Y.; Xun, L.; Liu, H. Sulfide-quinone oxidoreductase is required for cysteine synthesis and indispensable to mitochondrial health. Redox Biol. 2021, 47, 102169. [Google Scholar] [CrossRef]
  22. Wang, Q.; Chen, Z.; Zhang, X.; Xin, Y.; Xia, Y.; Xun, L.; Liu, H. Rhodanese Rdl2 produces reactive sulfur species to protect mitochondria from reactive oxygen species. Free Radic. Biol. Med. 2021, 177, 287–298. [Google Scholar] [CrossRef]
  23. Su, C.; Ran, X.; Hu, J.; Shao, C. Photocatalytic process of simultaneous desulfurization and denitrification of flue gas by tio2-polyacrylonitrile nanofibers. Environ. Sci. Technol. 2013, 47, 11562–11568. [Google Scholar] [CrossRef] [PubMed]
  24. Guimera, X.; Mora, M.; Dorado, A.D.; Bonsfills, A.; Gabriel, D.; Gamisans, X. Optimization of SO2 and NOx sequential wet absorption in a two-stage bioscrubber for elemental sulphur valorisation. Environ. Sci. Pollut. Res. 2021, 28, 24605–24617. [Google Scholar] [CrossRef] [PubMed]
  25. Crowe, S.A.; Paris, G.; Katsev, S.; Jones, C.; Kim, S.; Zerkle, A.L.; Nomosatryo, S.; Fowle, D.A.; Adkins, J.F.; Sessions, A.L.; et al. Sulfate was a trace constituent of Archean seawater. Science 2014, 346, 735–739. [Google Scholar] [CrossRef] [PubMed][Green Version]
  26. Hao, T.; Xiang, P.; Mackey, H.R.; Chi, K.; Lu, H.; Chui, H.; van Loosdrecht, M.C.M.; Chen, G. A review of biological sulfate conversions in wastewater treatment. Water Res. 2014, 65, 1–21. [Google Scholar] [CrossRef]
  27. Zhang, L.; Qiu, Y.; Zhou, Y.; Chen, G.; Loosdrecht, M.C.M.V.; Jiang, F. Elemental sulfur as electron donor and/or acceptor: Mechanisms, applications and perspectives for biological water and wastewater treatment. Water Res. 2021, 202, 117373. [Google Scholar] [CrossRef] [PubMed]
  28. Kuypers, M.M.M.; Marchant, H.K.; Kartal, B. The microbial nitrogen-cycling network. Nat. Rev. Microbiol. 2018, 16, 263–276. [Google Scholar] [CrossRef] [PubMed]
  29. Pang, Y.; Wang, J. Various electron donors for biological nitrate removal: A review. Sci. Total Environ. 2021, 794, 148699. [Google Scholar] [CrossRef]
  30. Wang, J.; Lu, H.; Chen, G.; Lau, G.N.; Tsang, W.L.; van Loosdrecht, M.C.M. A novel sulfate reduction, autotrophic denitrification, nitrification integrated (SANI) process for saline wastewater treatment. Water Res. 2009, 43, 2363–2372. [Google Scholar] [CrossRef]
  31. Jin, Q.; Bethke, C.M. Cellular energy conservation and the rate of microbial sulfate reduction. Geology 2009, 37, 1027–1030. [Google Scholar] [CrossRef]
  32. Sorensen, J.; Christensen, D.; Jorgensen, B.B. Volatile fatty acids and hydrogen as substrates for sulfate-reducing bacteria in anaerobic marine sediment. Appl. Environ. Microbiol. 1981, 42, 5–11. [Google Scholar] [CrossRef] [PubMed][Green Version]
  33. Kumar, M.; Nandi, M.; Pakshirajan, K. Recent advances in heavy metal recovery from wastewater by biogenic sulfide precipitation. J. Environ. Manage. 2021, 278, 111555. [Google Scholar] [CrossRef]
  34. Mendez-Garcia, C.; Pelaez, A.I.; Mesa, V.; Sanchez, J.; Golyshina, O.V.; Ferrer, M. Microbial diversity and metabolic networks in acid mine drainage habitats. Front. Microbiol. 2015, 6, 475. [Google Scholar] [CrossRef][Green Version]
  35. Li, Y.; Xu, Z.; Wu, J.; Mo, P. Efficiency and mechanisms of antimony removal from wastewater using mixed cultures of iron-oxidizing bacteria and sulfate-reducing bacteria based on scrap iron. Sep. Purif. Technol. 2020, 246, 116756. [Google Scholar] [CrossRef]
  36. Xi, Y.; Lan, S.; Li, X.; Wu, Y.; Yuan, X.; Zhang, C.; Liu, Y.; Huang, Y.; Quan, B.; Wu, S. Bioremediation of antimony from wastewater by sulfate-reducing bacteria: Effect of the coexisting ferrous ion. Int. Biodeterior. Biodegrad. 2020, 148, 104912. [Google Scholar] [CrossRef]
  37. Xie, P.; Chen, C.; Zhang, C.; Su, G.; Ren, N.; Ho, S. Revealing the role of adsorption in ciprofloxacin and sulfadiazine elimination routes in microalgae. Water Res. 2020, 172, 115475. [Google Scholar] [CrossRef] [PubMed]
  38. Jia, Y.; Khanal, S.K.; Shu, H.; Zhang, H.; Chen, G.; Lu, H. Ciprofloxacin degradation in anaerobic sulfate-reducing bacteria (SRB) sludge system: Mechanism and pathways. Water Res. 2018, 136, 64–74. [Google Scholar] [CrossRef]
  39. Zhang, H.; Song, S.; Jia, Y.; Wu, D.; Lu, H. Stress-responses of activated sludge and anaerobic sulfate-reducing bacteria sludge under long-term ciprofloxacin exposure. Water Res. 2019, 164, 114964. [Google Scholar] [CrossRef]
  40. Boopathy, R. Anaerobic phenol degradation by microorganisms of swine manure. Curr. Microbiol. 1997, 35, 64–67. [Google Scholar] [CrossRef]
  41. Abu Laban, N.; Selesi, D.; Jobelius, C.; Meckenstock, R.U. Anaerobic benzene degradation by Gram-positive sulfate-reducing bacteria. Fems Microbiol. Ecol. 2009, 68, 300–311. [Google Scholar] [CrossRef][Green Version]
  42. Guo, X.J.; Lu, Z.Y.; Wang, P.; Li, H.; Huang, Z.Z.; Lin, K.F.; Liu, Y.D. Diversity and degradation mechanism of an anaerobic bacterial community treating phenolic wastewater with sulfate as an electron acceptor. Environ. Sci. Pollut. Res. 2015, 22, 16121–16132. [Google Scholar] [CrossRef]
  43. Xie, X.; Mueller, N. Enzymes involved in the anaerobic degradation of phenol by the sulfate-reducing bacterium Desulfatiglans anilini. BMC Microbiol. 2018, 18, 1–10. [Google Scholar] [CrossRef] [PubMed][Green Version]
  44. Finke, N.; Vandieken, V.; Jorgensen, B.B. Acetate, lactate, propionate, and isobutyrate as electron donors for iron and sulfate reduction in Arctic marine sediments, Svalbard. Fems Microbiol. Ecol. 2007, 59, 10–22. [Google Scholar] [CrossRef] [PubMed][Green Version]
  45. Muyzer, G.; Stams, A.J.M. The ecology and biotechnology of sulphate-reducing bacteria. Nat. Rev. Microbiol. 2008, 6, 441–454. [Google Scholar] [CrossRef] [PubMed]
  46. Gittel, A.; Mussmann, M.; Sass, H.; Cypionka, H.; Koenneke, M. Identity and abundance of active sulfate-reducing bacteria in deep tidal flat sediments determined by directed cultivation and CARD-FISH analysis. Environ. Microbiol. 2008, 10, 2645–2658. [Google Scholar] [CrossRef]
  47. Jochum, L.M.; Chen, X.; Lever, M.A.; Loy, A.; Jorgensen, B.B.; Schramm, A.; Kjeldsen, K.U. Depth distribution and assembly of sulfate-reducing microbial communities in marine sediments of Aarhus bay. Appl. Environ. Microbiol. 2017, 83, e01547-17. [Google Scholar] [CrossRef][Green Version]
  48. Chen, C.; Ren, N.; Wang, A.; Yu, Z.; Lee, D. Microbial community of granules in expanded granular sludge bed reactor for simultaneous biological removal of sulfate, nitrate and lactate. Appl. Microbiol. Biotechnol. 2008, 79, 1071–1077. [Google Scholar] [CrossRef]
  49. Yuan, Y.; Chen, C.; Liang, B.; Huang, C.; Zhao, Y.; Xu, X.; Tan, W.; Zhou, X.; Gao, S.; Sun, D.; et al. Fine-tuning key parameters of an integrated reactor system for the simultaneous removal of COD, sulfate and ammonium and elemental sulfur reclamation. J. Hazard. Mater. 2014, 269, 56–67. [Google Scholar] [CrossRef]
  50. Madani, R.M.; Liang, J.; Cui, L.; Zhang, D.; Otitoju, T.A.; Elsalahi, R.H.; Song, X. Novel simultaneous anaerobic ammonium and sulfate removal process: A review. Environ. Technol. Innov. 2021, 23, 101661. [Google Scholar] [CrossRef]
  51. Peck, H.D.J. Enzymatic basis for assimilatory and dissimilatory sulfate reduction. J. Bacteriol. 1961, 82, 933–939. [Google Scholar] [CrossRef][Green Version]
  52. Prior, A.; Uhrig, J.F.; Heins, L.; Wiesmann, A.; Lillig, C.H.; Stoltze, C.; Soll, J.; Schwenn, J.D. Structural and kinetic properties of adenylyl sulfate reductase from Catharanthus roseus cell cultures. Biochim. Biophys. Acta Protein Struct. Molecul. Enzymol. 1999, 1430, 25–38. [Google Scholar] [CrossRef] [PubMed]
  53. Fritz, G.; Buchert, T.; Huber, H.; Stetter, K.O.; Kroneck, P. Adenylylsulfate reductases from archaea and bacteria are 1:1 alpha beta-heterodimeric iron-sulfur flavoenzymes—high similarity of molecular properties emphasizes their central role in sulfur metabolism. Febs Lett. 2000, 473, 63–66. [Google Scholar] [CrossRef] [PubMed][Green Version]
  54. Santos, A.A.; Venceslau, S.S.; Grein, F.; Leavitt, W.D.; Dahl, C.; Johnston, D.T.; Pereira, I.A.C. A protein trisulfide couples dissimilatory sulfate reduction to energy conservation. Science 2015, 350, 1541–1545. [Google Scholar] [CrossRef]
  55. Mueller, A.L.; Kjeldsen, K.U.; Rattei, T.; Pester, M.; Loy, A. Phylogenetic and environmental diversity of DsrAB-type dissimilatory (bi) sulfite reductases. Isme J. 2015, 9, 1152–1165. [Google Scholar] [CrossRef] [PubMed][Green Version]
  56. Davidson, M.M.; Bisher, M.E.; Pratt, L.M.; Fong, J.; Southam, G.; Pfiffner, S.M.; Reches, Z.; Onstott, T.C. Sulfur isotope enrichment during maintenance metabolism in the thermophilic sulfate-reducing bacterium Desulfotomaculum putei. Appl. Environ. Microbiol. 2009, 75, 5621–5630. [Google Scholar] [CrossRef][Green Version]
  57. Wing, B.A.; Halevy, I. Intracellular metabolite levels shape sulfur isotope fractionation during microbial sulfate respiration. Proc. Natl. Acad. Sci. USA. 2014, 111, 18116–18125. [Google Scholar] [CrossRef][Green Version]
  58. Xu, X.; Chen, C.; Wang, A.; Fang, N.; Yuan, Y.; Ren, N.; Lee, D. Enhanced elementary sulfur recovery in integrated sulfate-reducing, sulfur-producing rector under micro-aerobic condition. Bioresour. Technol. 2012, 116, 517–521. [Google Scholar] [CrossRef]
  59. Beulig, F.; Roy, H.; Glombitza, C.; Jorgensen, B.B. Control on rate and pathway of anaerobic organic carbon degradation in the seabed. Proc. Natl. Acad. Sci. USA. 2018, 115, 367–372. [Google Scholar] [CrossRef][Green Version]
  60. Das, B.K.; Gauri, S.S.; Bhattacharya, J. Sweetmeat waste fractions as suitable organic carbon source for biological sulfate reduction. Int. Biodeterior. Biodegrad. 2013, 82, 215–223. [Google Scholar] [CrossRef]
  61. Hussain, A.; Iqbal, M.A.; Javid, A.; Razaq, A.; Aslam, S.; Hasan, A.; Akmal, M.; Qazi, J.I. Application of fruit wastes as cost-effective carbon sources for biological sulphate reduction. Iran. J. Sci. Technol. Trans. A-Sci. 2019, 43, 33–41. [Google Scholar] [CrossRef]
  62. Jorgensen, B.B.; Findlay, A.J.; Pellerin, A. The biogeochemical sulfur cycle of marine sediments. Front. Microbiol. 2019, 10, 849. [Google Scholar] [CrossRef] [PubMed]
  63. Mardanov, A.V.; Kadnikov, V.V.; Beletsky, A.V.; Ravin, N.V. Sulfur and methane-oxidizing microbial community in a terrestrial mud volcano revealed by metagenomics. Microorganisms 2020, 8, 1333. [Google Scholar] [CrossRef] [PubMed]
  64. Shahsavari, S.; Seth, R.; Chaganti, S.R.; Biswas, N. Inhibition of anaerobic biological sulfate reduction process by copper precipitates. Chemosphere 2019, 236, 124246. [Google Scholar] [CrossRef] [PubMed]
  65. Zhang, L.; Lin, X.; Zhang, Z.; Chen, G.; Jiang, F. Elemental sulfur as an electron acceptor for organic matter removal in a new high-rate anaerobic biological wastewater treatment process. Chem. Eng. J. 2018, 331, 16–22. [Google Scholar] [CrossRef]
  66. Zhang, L.; Zhang, C.; Hu, C.; Liu, H.; Qu, J. Denitrification of groundwater using a sulfur-oxidizing autotrophic denitrifying anaerobic fluidized-bed MBR: Performance and bacterial community structure. Appl. Microbiol. Biotechnol. 2015, 99, 2815–2827. [Google Scholar] [CrossRef]
  67. Sun, R.; Li, Y.; Lin, N.; Ou, C.; Wang, X.; Zhang, L.; Jiang, F. Removal of heavy metals using a novel sulfidogenic AMD treatment system with sulfur reduction: Configuration, performance, critical parameters and economic analysis. Environ. Int. 2020, 136, 105457. [Google Scholar] [CrossRef] [PubMed]
  68. Qiu, Y.; Zhang, L.; Mu, X.; Li, G.; Guan, X.; Hong, J.; Jiang, F. Overlooked pathways of denitrification in a sulfur-based denitrification system with organic supplementation. Water Res. 2020, 169, 115084. [Google Scholar] [CrossRef]
  69. Zhang, Q.; Xu, X.; Zhang, R.; Shao, B.; Fan, K.; Zhao, L.; Ji, X.; Ren, N.; Lee, D.; Chen, C. The mixed/mixotrophic nitrogen removal for the effective and sustainable treatment of wastewater: From treatment process to microbial mechanism. Water Res. 2022, 226, 119269. [Google Scholar] [CrossRef]
  70. Zhang, L.; Zhang, Z.; Sun, R.; Liang, S.; Chen, G.; Jiang, F. Self-accelerating sulfur reduction via polysulfide to realize a high-rate sulfidogenic reactor for wastewater treatment. Water Res. 2018, 130, 161–167. [Google Scholar] [CrossRef]
  71. Zhang, Y.; Zhang, L.; Li, L.; Chen, G.; Jiang, F. A novel elemental sulfur reduction and sulfide oxidation integrated process for wastewater treatment and sulfur recycling. Chem. Eng. J. 2018, 342, 438–445. [Google Scholar] [CrossRef]
  72. Li, G.; Liang, Z.; Sun, J.; Qiu, Y.; Qiu, C.; Liang, X.; Zhu, Y.; Wang, P.; Li, Y.; Jiang, F. A pilot-scale sulfur-based sulfidogenic system for the treatment of Cu-laden electroplating wastewater using real domestic sewage as electron donor. Water Res. 2021, 195, 116999. [Google Scholar] [CrossRef] [PubMed]
  73. Gorny, J.; Billon, G.; Lesven, L.; Dumoulin, D.; Made, B.; Noiriel, C. Arsenic behavior in river sediments under redox gradient: A review. Sci. Total Environ. 2015, 505, 423–434. [Google Scholar] [CrossRef] [PubMed]
  74. de Matos, L.P.; Costa, P.F.; Moreira, M.; Silva Gomes, P.C.; Silva, S.D.Q.; Alves Gurgel, L.V.; Teixeira, M.C. Simultaneous removal of sulfate and arsenic using immobilized non-traditional SRB mixed culture and alternative low-cost carbon sources. Chem. Eng. J. 2018, 334, 1630–1641. [Google Scholar] [CrossRef]
  75. Sun, J.; Hong, Y.; Guo, J.; Yang, J.; Huang, D.; Lin, Z.; Jiang, F. Arsenite removal without thioarsenite formation in a sulfidogenic system driven by sulfur reducing bacteria under acidic conditions. Water Res. 2019, 151, 362–370. [Google Scholar] [CrossRef]
  76. King, J.K.; Harmon, S.M.; Fu, T.T.; Gladden, J.B. Mercury removal, methylmercury formation, and sulfate-reducing bacteria profiles in wetland mesocosms. Chemosphere 2002, 46, 859–870. [Google Scholar] [CrossRef]
  77. Wang, J.; Zhang, L.; Kang, Y.; Chen, G.; Jiang, F. Long-term feeding of elemental sulfur alters microbial community structure and eliminates mercury methylation potential in sulfate-reducing bacteria abundant activated sludge. Environ. Sci. Technol. 2018, 52, 4746–4753. [Google Scholar] [CrossRef]
  78. Sun, J.; Li, L.; Zhou, G.; Wang, X.; Zhang, L.; Liu, Y.; Yang, J.; Lu, X.; Jiang, F. Biological sulfur reduction to generate H2S as a reducing agent to achieve simultaneous catalytic removal of so2 and no and sulfur recovery from flue gas. Environ. Sci. Technol. 2018, 52, 4754–4762. [Google Scholar] [CrossRef]
  79. Qiu, Y.; Gong, X.; Zhang, L.; Zhou, S.; Li, G.; Jiang, F. Achieving a novel polysulfide-involved sulfur-based autotrophic denitrification process for high-rate nitrogen removal in elemental sulfur-packed bed reactors. ACS EsT Eng. 2022, 2, 1504–1513. [Google Scholar] [CrossRef]
  80. Hedderich, R.; Klimmek, O.; Kroger, A.; Dirmeier, R.; Keller, M.; Stetter, K.O. Anaerobic respiration with elemental sulfur and with disulfides. Fems Microbiol. Rev. 1998, 22, 353–381. [Google Scholar] [CrossRef]
  81. Schauder, R.; Kroger, A. Bacterial sulfur respiration. Arch. Microbiol. 1993, 159, 491–497. [Google Scholar] [CrossRef]
  82. Segerer, A.; Neuner, A.; Kristjansson, J.K.; Stetter, K.O. Acidianus infernus gen-nov, sp-nov, and Acidianus brierleyi comb-nov—facultatively aerobic, extremely acidophilic thermophilic sulfur-metabolizing archaebacteria. Int. J. Syst. Bacteriol. 1986, 36, 559–564. [Google Scholar] [CrossRef][Green Version]
  83. Fischer, F.; Zillig, W.; Stetter, K.O.; Schreiber, G. Chemolithoautotrophic metabolism of anaerobic extremely thermophilic archaebacteria. Nature 1983, 301, 511–513. [Google Scholar] [CrossRef] [PubMed]
  84. Gonzalez, J.M.; Masuchi, Y.; Robb, F.T.; Ammerman, J.W.; Maeder, D.L.; Yanagibayashi, M.; Tamaoka, J.; Kato, C. Pyrococcus horikoshii sp. nov., a hyperthermophilic archaeon isolated from a hydrothermal vent at the Okinawa Trough. Extremophiles 1998, 2, 123–130. [Google Scholar] [CrossRef] [PubMed]
  85. Deppenmeier, U.; Lienard, T.; Gottschalk, G. Novel reactions involved in energy conservation by methanogenic archaea. Febs Lett. 1999, 457, 291–297. [Google Scholar] [CrossRef] [PubMed][Green Version]
  86. Huber, R.; Wilharm, T.; Huber, D.; Trincone, A.; Burggraf, S.; Konig, H.; Rachel, R.; Rockinger, I.; Fricke, H.; Stetter, K.O. Aquifex pyrophilus gen-nov sp-nov represents a novel group of marine hyperthermophilic hydrogen-oxidizing bacteria. Syst. Appl. Microbiol. 1992, 15, 340–351. [Google Scholar] [CrossRef]
  87. L’Haridon, S.; Cilia, V.; Messner, P.; Raguénès, G.; Gambacorta, A.; Sleytr, U.B.; Prieur, D.; Jeanthon, C. Desulfurobacterium thermolithotrophum gen. nov., sp. nov., a novel autotrophic, sulphur-reducing bacterium isolated from a deep-sea hydrothermal vent. Int. J. Syst. Evol. Microbiol. 1998, 48, 701–711. [Google Scholar] [CrossRef][Green Version]
  88. Pfennig, N.; Biebl, H. Desulfuromonas acetoxidans gen. nov. and sp. nov., a new anaerobic, sulfur-reducing, acetate-oxidizing bacterium. Arch. Microbiol. 1976, 110, 3–12. [Google Scholar] [CrossRef]
  89. Liesack, W.; Finster, K. Phylogenetic analysis of five strains of gram-negative, obligately anaerobic, sulfur-reducing bacteria and description of Desulfuromusa gen. nov., including Desulfuromusa kysingii sp. nov., Desulfuromusa bakii sp. nov., and Desulfuromusa succinoxidans sp. Int. J. Syst. Evol. Microbiol. 1994, 44, 753–758. [Google Scholar] [CrossRef]
  90. Huber, R.; Woese, C.R.; Langworthy, T.A.; Kristjansson, J.K.; Stetter, K.O. Fervidobacterium-islandicum sp-nov, a new extremely thermophilic eubacterium belonging to the thermotogales. Arch. Microbiol. 1990, 154, 105–111. [Google Scholar] [CrossRef]
  91. Caccavo, F.; Lonergan, D.J.; Lovley, D.R.; Davis, M.; Stolz, J.F.; Mcinerney, M.J. Geobacter sulfurreducens sp-nov, a hydrogen-oxidizing and acetate-oxidizing dissimilatory metal-reducing microorganism. Appl. Environ. Microbiol. 1994, 60, 3752–3759. [Google Scholar] [CrossRef][Green Version]
  92. Wolfe, R.S.; Penning, N. Reduction of sulfur by spirillum 5175 and syntrophism with Chlorobium. Appl. Environ. Microbiol. 1977, 33, 427–433. [Google Scholar] [CrossRef][Green Version]
  93. Windberger, E.; Huber, R.; Trincone, A.; Fricke, H.; Stetter, K.O. Thermotoga thermarum sp-nov and Thermotoga neapolitana occurring in African continental solfataric springs. Arch. Microbiol. 1989, 151, 506–512. [Google Scholar] [CrossRef]
  94. Huber, R.; Woese, C.R.; Langworthy, T.A.; Fricke, H.; Stetter, K.O. Thermosipho africanus gen-nov, represents a new genus of thermophilic eubacteria within the thermotogales. Syst. Appl. Microbiol. 1989, 12, 32–37. [Google Scholar] [CrossRef]
  95. Macy, J.M.; Schroder, I.; Thauer, R.K.; Kroger, A. Growth the Wolinella succinogenes on H2S plus fumarate and on formate plus sulfur as energy sources. Arch. Microbiol. 1986, 144, 147–150. [Google Scholar] [CrossRef]
  96. Jelen, B.; Giovannelli, D.; Falkowski, P.G.; Vetriani, C. Elemental sulfur reduction in the deep-sea vent thermophile, Thermovibrio ammonificans. Environ. Microbiol. 2018, 20, 2301–2316. [Google Scholar] [CrossRef] [PubMed]
  97. Koschorreck, M. Microbial sulphate reduction at a low pH microbial sulphate reduction at a low pH. Fems Microbiol. Ecol. 2008, 64, 329–342. [Google Scholar] [CrossRef]
  98. Grubba, D.; Yin, Z.; Majtacz, J.; Al-Hazmi, H.E.; Makinia, J. Incorporation of the sulfur cycle in sustainable nitrogen removal systems-A review. J. Clean Prod. 2022, 372, 133495. [Google Scholar] [CrossRef]
  99. Huang, C.; Liu, Q.; Li, Z.; Ma, X.; Hou, Y.; Ren, N.; Wang, A. Relationship between functional bacteria in a denitrification desulfurization system under autotrophic, heterotrophic, and mixotrophic conditions. Water Res. 2021, 188, 116526. [Google Scholar] [CrossRef]
  100. Bi, Z.; Zhang, Q.; Xu, X.; Yuan, Y.; Ren, N.; Lee, D.; Chen, C. Perspective on inorganic electron donor-mediated biological denitrification process for low C/N wastewaters. Bioresour. Technol. 2022, 363, 127890. [Google Scholar] [CrossRef]
  101. Fernandez, M.; Ramirez, M.; Maria Perez, R.; Manuel Gomez, J.; Canter, D. Hydrogen sulphide removal from biogas by an anoxic biotrickling filter packed with Pall rings. Chem. Eng. J. 2013, 225, 456–463. [Google Scholar] [CrossRef]
  102. Ramos, I.; Perez, R.; Fdz-Polanco, M. Microaerobic desulphurisation unit: A new biological system for the removal of H2S from biogas. Bioresour. Technol. 2013, 142, 633–640. [Google Scholar] [CrossRef]
  103. Jung, H.; Kim, D.; Choi, H.; Lee, C. A review of technologies for in-situ sulfide control in anaerobic digestion. Renew. Sust. Energ. Rev. 2022, 157, 112068. [Google Scholar] [CrossRef]
  104. Wang, W.; Zhang, R.; Huang, Z.; Chen, C.; Xu, X.; Zhou, X.; Yin, T.; Wang, A.; Lee, D.; Ren, N. Performance of a novel IAHD-DSR process with methane and sulfide as co-electron donors. J. Hazard. Mater. 2020, 386, 121657. [Google Scholar] [CrossRef] [PubMed]
  105. Reyes-Avila, J.S.; Razo-Flores, E.; Gomez, J. Simultaneous biological removal of nitrogen, carbon and sulfur by denitrification. Water Res. 2004, 38, 3313–3321. [Google Scholar] [CrossRef] [PubMed]
  106. Chen, C.; Ren, N.; Wang, A.; Yu, Z.; Lee, D. Simultaneous biological removal of sulfur, nitrogen and carbon using EGSB reactor. Appl. Microbiol. Biotechnol. 2008, 78, 1057–1063. [Google Scholar] [CrossRef]
  107. Zhang, R.; Xu, X.; Chen, C.; Xing, D.; Shao, B.; Liu, W.; Wang, A.; Lee, D.; Ren, N. Interactions of functional bacteria and their contributions to the performance in integrated autotrophic and heterotrophic denitrification. Water Res. 2018, 143, 355–366. [Google Scholar] [CrossRef]
  108. Huang, C.; Li, Z.; Chen, F.; Liu, Q.; Zhao, Y.; Gao, L.; Chen, C.; Zhou, J.; Wang, A. Efficient regulation of elemental sulfur recovery through optimizing working height of upflow anaerobic sludge blanket reactor during denitrifying sulfide removal process. Bioresour. Technol. 2016, 200, 1019–1023. [Google Scholar] [CrossRef]
  109. Huang, C.; Liu, W.; Li, Z.; Zhang, S.; Chen, F.; Yu, H.; Shao, S.; Nan, J.; Wang, A. High recycling efficiency and elemental sulfur purity achieved in a biofilm formed membrane filtration reactor. Water Res. 2018, 130, 1–12. [Google Scholar] [CrossRef]
  110. Marques, E.L.S.; Dias, J.C.T.; Gross, E.; de Cerqueira E Silva, A.B.; de Moura, S.R.; Rezende, R.P. Purple sulfur bacteria dominate microbial community in Brazilian limestone cave. Microorganisms 2019, 7, 29. [Google Scholar] [CrossRef][Green Version]
  111. Gregersen, L.H.; Bryant, D.A.; Frigaard, N. Mechanisms and evolution of oxidative sulfur metabolism in green sulfur bacteria. Front. Microbiol. 2011, 2, 116. [Google Scholar] [CrossRef][Green Version]
  112. Karr, E.A.; Sattley, W.M.; Jung, D.O.; Madigan, M.T.; Achenbach, L.A. Remarkable diversity of phototrophic purple bacteria in a permanently frozen Antarctic lake. Appl. Environ. Microbiol. 2003, 69, 4910–4914. [Google Scholar] [CrossRef][Green Version]
  113. Madigan, M.T. Anoxygenic phototrophic bacteria from extreme environments. Photosynth. Res. 2003, 76, 157–171. [Google Scholar] [CrossRef] [PubMed]
  114. Eckert, C.A.; Freed, E.; Wawrousek, K.; Smolinski, S.; Yu, J.; Maness, P. Inactivation of the uptake hydrogenase in the purple non-sulfur photosynthetic bacterium Rubrivivax gelatinosus CBS enables a biological water-gas shift platform for H-2 production. J. Ind. Microbiol. Biotechnol. 2019, 46, 993–1002. [Google Scholar] [CrossRef]
  115. Chan, L.; Morgan-Kiss, R.; Hanson, T.E. Sulfur oxidation in Chlorobium tepidum (syn. Chlorobaculum tepidum) Genetic and proteomic analyses. In Microbial Sulfur Metabolism; Springer: Munster, Germany, 2008; p. 117. [Google Scholar]
  116. Stout, J.; De Smet, L.; Vergauwen, B.; Savvides, S.; Van Beeumen, J. Structural insights into component SoxY of the thiosulfate-oxidizing multienzyme system of Chlorobaculum thiosulfatiphilum. In Microbial Sulfur Metabolism; Springer: Munster, Germany, 2008; p. 127. [Google Scholar]
  117. Serrano, W.; Schruebbers, J.; Amann, R.; Fischer, U. Allochromatium humboldtianum sp. nov., isolated from soft coastal sediments. Int. J. Syst. Evol. Microbiol. 2015, 65, 2980. [Google Scholar] [CrossRef] [PubMed]
  118. Caumette, P.; Baulaigue, R.; Matheron, R. Characterization of Chromatium salexigens sp. nov., a Halophilic Chromatiaceae Isolated from Mediterranean Salinas—ScienceDirect. Syst. Appl. Microbiol. 1988, 10, 284–292. [Google Scholar] [CrossRef]
  119. Bertini, I.; Gaudemer, A.; Luchinat, C.; Piccioli, M. Electron self-exchange in high-potential iron-sulfur proteins. Characterization of protein I from Ectothiorhodospira vacuolata. Biochemistry 1993, 32, 12887–12893. [Google Scholar] [CrossRef] [PubMed]
  120. Hensen, D.; Sperling, D.; Trüper, H.G.; Brune, D.C.; Dahl, C. Thiosulphate oxidation in the phototrophic sulphur bacterium Allochromatium vinosum. Mol. Microbiol. 2010, 62, 794–810. [Google Scholar] [CrossRef]
  121. Harwood, C.S.; Gibson, J. Anaerobic and aerobic metabolism of diverse aromatic compounds by the photosynthetic bacterium Rhodopseudomonas palustris. Appl. Environ. Microbiol. 1988, 54, 712–717. [Google Scholar] [CrossRef][Green Version]
  122. Pfennig, N. Rhodocyclus purpureus gen. nov. and sp. nov., a Ring-Shaped, Vitamin B12-Requiring Member of the Family Rhodospirillaceae. Int. J. Syst. Bacteriol. 1978, 30, 283–288. [Google Scholar]
  123. Dziewit, L.; Baj, J.; Szuplewska, M.; Maj, A.; Tabin, M.; Czyzkowska, A.; Skrzypczyk, G.; Adamczuk, M.; Sitarek, T.; Stawinski, P. Insights into the transposable mobilome of Paracoccus spp. (Alphaproteobacteria). PLoS ONE 2012, 7, e32277. [Google Scholar] [CrossRef][Green Version]
  124. Valdés, J.; Pedroso, I.; Quatrini, R.; Dodson, R.J.; Tettelin, H.; Blake, R.; Eisen, J.A.; Holmes, D.S. Acidithiobacillus ferrooxidans metabolism: From genome sequence to industrial applications. BMC Genomics 2008, 9, 597. [Google Scholar] [CrossRef][Green Version]
  125. Takai, K. Thiomicrospira thermophila sp. nov., a novel microaerobic, thermotolerant, sulfur-oxidizing chemolithomixotroph isolated from a deep-sea hydrothermal fumarole in the TOTO caldera, Mariana Arc, Western Pacific. Int. J. Syst. Evol. Microbiol. 2004, 54, 2325. [Google Scholar]
  126. Nelson, D.C.; Jrgensen, B.B.; Revsbech, N.P. Growth pattern and yield of a chemoautotrophic Beggiatoa sp. in oxygen-sulfide microgradients. Appl. Environ. Microbiol. 1986, 52, 225–233. [Google Scholar] [CrossRef] [PubMed][Green Version]
  127. Shao, M.; Zhang, T.; Fang, H.H. Sulfur-driven autotrophic denitrification: Diversity, biochemistry, and engineering applications. Appl. Microbiol. Biotechnol. 2010, 88, 1027–1042. [Google Scholar] [CrossRef] [PubMed]
  128. Xia, Y.; Lu, C.; Hou, N.; Xin, Y.; Liu, J.; Liu, H.; Xun, L. Sulfide production and oxidation by heterotrophic bacteria under aerobic conditions. ISME J. 2017, 11, 2754–2766. [Google Scholar] [CrossRef] [PubMed][Green Version]
  129. Xin, Y.; Liu, H.; Cui, F.; Liu, H.; Xun, L. Recombinant Escherichia coli with sulfide: Quinone oxidoreductase and persulfide dioxygenase rapidly oxidises sulfide to sulfite and thiosulfate via a new pathway. Environ. Microbiol. 2016, 18, 5123–5136. [Google Scholar] [CrossRef]
  130. Lu, C.; Xia, Y.; Liu, D.; Zhao, R.; Gao, R.; Liu, H.; Xun, L. Cupriavidus necator H16 uses flavocytochrome c sulfide dehydrogenase to oxidize self-produced and added sulfide. Appl. Environ. Microbiol. 2017, 83, e01610-17. [Google Scholar] [CrossRef][Green Version]
  131. Xin, Y.; Gao, R.; Cui, F.; Lu, C.; Liu, H.; Liu, H.; Xia, Y.; Xun, L. The heterotrophic bacterium Cupriavidus pinatubonensis JMP134 oxidizes sulfide to sulfate with thiosulfate as a key intermediate. Appl. Environ. Microbiol. 2020, 86, e01835-20. [Google Scholar] [CrossRef]
  132. Fan, K.; Xu, X.; Xu, F.; Shi, J.; Sun, K.; Fedorova, I.; Ren, N.; Lee, D.; Chen, C. A novel intra- and extracellular distribution pattern of elemental sulfur in Pseudomonas sp. C27-driven denitrifying sulfide removal process. Environ. Res. 2022, 213, 113674. [Google Scholar] [CrossRef]
  133. Jorgensen, B.B. Ecology of the bacteria of the sulphur cycle with special reference to anoxic-oxic interface environments. Philos. Trans. R. Soc. Lond. B Biol. Sci. 1982, 298, 543–561. [Google Scholar] [CrossRef]
  134. Luther, G.W.I.; Findlay, A.J.; Macdonald, D.J.; Owings, S.M.; Hanson, T.E.; Beinart, R.A.; Girguis, P.R. Thermodynamics and kinetics of sulfide oxidation by oxygen: A look at inorganically controlled reactions and biologically mediated processes in the environment. Front. Microbiol. 2011, 2, 62. [Google Scholar] [CrossRef][Green Version]
  135. Marazioti, C.; Kornaros, M.; Lyberatos, G. Kinetic modeling of a mixed culture of Pseudomonas denitrificans and Bacillus subtilis under aerobic and anoxic operating conditions. Water Res. 2003, 37, 1239–1251. [Google Scholar] [CrossRef] [PubMed]
  136. Chen, C.; Zhang, R.; Xu, X.; Fang, N.; Wang, A.; Ren, N.; Lee, D. Enhanced performance of denitrifying sulfide removal process at high carbon to nitrogen ratios under micro-aerobic condition. Bioresour. Technol. 2017, 232, 417–422. [Google Scholar] [CrossRef] [PubMed]
  137. Lohwacharin, J.; Annachhatre, A.P. Biological sulfide oxidation in an airlift bioreactor. Bioresour. Technol. 2010, 101, 2114–2120. [Google Scholar] [CrossRef] [PubMed]
  138. Zhang, R.; Chen, C.; Shao, B.; Wang, W.; Xu, X.; Zhou, X.; Xiang, Y.; Zhao, L.; Lee, D.; Ren, N. Heterotrophic sulfide-oxidizing nitrate-reducing bacteria enables the high performance of integrated autotrophic-heterotrophic denitrification (IAHD) process under high sulfide loading. Water Res. 2020, 178, 115848. [Google Scholar] [CrossRef] [PubMed]
  139. Liang, S.; Zhang, L.; Jiang, F. Indirect sulfur reduction via polysulfide contributes to serious odor problem in a sewer receiving nitrate dosage. Water Res. 2016, 100, 421–428. [Google Scholar] [CrossRef] [PubMed]
  140. Cui, Y.; Biswal, B.K.; Guo, G.; Deng, Y.; Huang, H.; Chen, G.; Wu, D. Biological nitrogen removal from wastewater using sulphur-driven autotrophic denitrification. Appl. Microbiol. Biotechnol. 2019, 103, 6023–6039. [Google Scholar] [CrossRef]
  141. Sahinkaya, E.; Yurtsever, A.; Aktas, O.; Ucar, D.; Wang, Z. Sulfur-based autotrophic denitrification of drinking water using a membrane bioreactor. Chem. Eng. J. 2015, 268, 180–186. [Google Scholar] [CrossRef]
  142. Sahinkaya, E.; Kilic, A.; Duygulu, B. Pilot and full scale applications of sulfur-based autotrophic denitrification process for nitrate removal from activated sludge process effluent. Water Res. 2014, 60, 210–217. [Google Scholar] [CrossRef]
  143. Jamieson-Hanes, J.H.; Gibson, B.D.; Lindsay, M.B.J.; Kim, Y.; Ptacek, C.J.; Blowes, D.W. Chromium isotope fractionation during reduction of CR(VI) under saturated flow conditions. Environ. Sci. Technol. 2012, 46, 6783–6789. [Google Scholar] [CrossRef]
  144. Shi, J.; Zhang, B.; Qiu, R.; Lai, C.; Jiang, Y.; He, C.; Guo, J. Microbial chromate reduction coupled to anaerobic oxidation of elemental sulfur or zerovalent iron. Environ. Sci. Technol. 2019, 53, 3198–3207. [Google Scholar] [CrossRef]
  145. Loy, A.; Duller, S.; Wagner, M. Evolution and ecology of microbes dissimilating sulfur compounds Insights from siroheme sulfite reductases. In Microbial Sulfur Metabolism; Springer: Berlin/Heidelberg, Germany, 2008; pp. 46–59. [Google Scholar] [CrossRef]
  146. Dahl, C. Cytoplasmic sulfur trafficking in sulfur-oxidizing prokaryotes. IUBMB Life 2015, 67, 268–274. [Google Scholar] [CrossRef] [PubMed]
Figure 1. Global sulfur cycle.
Figure 1. Global sulfur cycle.
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Figure 2. Hypothetical pathway of polysulfide generation.
Figure 2. Hypothetical pathway of polysulfide generation.
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Figure 3. Diagram of SANI process.
Figure 3. Diagram of SANI process.
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Figure 4. Two sulfate-reduction pathways. The left is the dissimilatory sulfate-reduction pathway, where the product is hydrogen sulfide, and the right is the assimilatory sulfate reduction, where sulfide is utilized for cysteine synthesis.
Figure 4. Two sulfate-reduction pathways. The left is the dissimilatory sulfate-reduction pathway, where the product is hydrogen sulfide, and the right is the assimilatory sulfate reduction, where sulfide is utilized for cysteine synthesis.
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Figure 5. Two known mechanisms of sulfur respiration. (A) The Psr pathway where electrons for sulfur reduction are derived from hydrogenase. (B) The Nsr pathway where electrons for sulfur reduction come directly from NAD(P)H and require the participation of coenzyme A.
Figure 5. Two known mechanisms of sulfur respiration. (A) The Psr pathway where electrons for sulfur reduction are derived from hydrogenase. (B) The Nsr pathway where electrons for sulfur reduction come directly from NAD(P)H and require the participation of coenzyme A.
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Figure 6. Biological oxidation pathway of sulfides. FCSD and SOX are located in periplasmic space and the SQR/PDO/ST pathway is located in the cytoplasm.
Figure 6. Biological oxidation pathway of sulfides. FCSD and SOX are located in periplasmic space and the SQR/PDO/ST pathway is located in the cytoplasm.
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Figure 7. Biological oxidation pathway of elemental sulfur. (A) The rDSR pathway and (B) the Hdr pathway.
Figure 7. Biological oxidation pathway of elemental sulfur. (A) The rDSR pathway and (B) the Hdr pathway.
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Table 1. Representative sulfur-containing substances in different valence states.
Table 1. Representative sulfur-containing substances in different valence states.
ComponentChemical FormulaValence of Sulfur
Inorganic sulfur species:
Pyretic sulfurFeS/FeS2−2 and −1
Inorganic polysulfidesH-Sn-H/Sn2− (n ≥ 2)−1 and 0
Elemental sulfurS/S8/S00
Sulfur dioxideSO2+4
Organic sulfur species:
Reduced organic sulfur compoundsCysteine, methionine−2
Organic polysulfidesR-Sn-R/R-SnH (n ≥ 2)0
Table 2. Representative archaea and bacterial members of sulfur respiration.
Table 2. Representative archaea and bacterial members of sulfur respiration.
Taxonomic CategoryElectron DonorReference
ThermoproteusH2, peptides, maltose, formate, fumarate, ethanol, malate, methanol, glycogen, starch, amylopectin, formamide[83]
PyrococcusComplex substrates, amino acids, starch, maltose, pyruvate[84]
MethanococcusH2, formate[85]
AquifexH2, sulfur, thiosulfate[86]
DesulfuromonasAcetate, pyruvate, ethanol[88]
DesulfuromusaAcetate, propionate[89]
FervidobacteriumSugars, pyruvate, yeast extract[90]
SulfospirillumH2, formate[92]
ThermotogaSugars, peptone, yeast extract, bacterial and archaeal cell homogenates[93]
ThermosiphoYeast extract, brain heart infusion, peptone, tryptone[94]
WolinellaH2, formate[95]
Table 3. Representative strains of sulfide-oxidizing bacteria and their metabolic features.
Table 3. Representative strains of sulfide-oxidizing bacteria and their metabolic features.
Taxonomic CategoryRepresentative SpeciesMetabolic FeaturesSulfur Oxidation GenesDistributed EnvironmentReference
Chlorobaculum tepidum,
Chlorobaculum thiosulfatiphilum
Obligate phototrophy; S2–, S0, or S2O32− as e donors for reduction of CO2; extracellular S0 globules; potential mixotrophySoxXAYZB, APS reductase, Qmo complex, and FccAnaerobic waters, oceans, soils, the Yellowstone hot springs and sediments [115,116]
Allochromatium warmingi
Isochromatium buderi
Photoautotrophy except for Rheinheimera spp.; S2− and S0 as e donors of photosynthesis; intracellular S0 globules-Oceans, stagnant aquifers, eutrophic lakes with water bodies, and extreme environments rich in sulfides[117,118]
EctothiorhodospiraceaeAllochromatium vinosum
Ectothiorhodospira vacuolata
Oxidation of S2− for all the members; extracellular S0 globules; polysulfides under alkaline conditions; some can oxidize S2O32− to SO42−SoxXAYZB, Sqr, DsrABEFHCMKLJOPNRS, APS reductase, and Fcc[119,120]
Rhodopseudomonas palustrisThe preferred photoheterotrophy under anaerobic conditions; photolithoautotrophy with S2−/S2O32−SoxXAYZBCD, SoxEF, and SqrWaste ponds, coastal lagoons and other aquatic-habitat stagnant areas, sediments, wet soils, and rice paddies[121]
BetaproteobacteriaRhodocyclus purpureusChemoorganotrophy/chemolithoautotrophy under aerobic or microaerobic conditions-[122]
Paracoccus spp. Facultative chemolithoautotrophy; oxidation of S2−, S0, S2O32−, or SO32− to SO42−SoxXAYZBCD and SoxEFActivated sludge, wastewater treatment systems, farmland, and natural ecological environment such as orchards[123]
AcidithiobacilliaAcidithiobacillus ferrooxidansObligate chemolithoautotrophy; oxidation of S0, S2O32−, or S4O62− by the incomplete Sox system; S0 globules as intermediatesSoxXAYZB and Sqr[124]
GammaproteobacteriaThiomicrospira crunogenaObligate chemolithoautotrophy; extracellular S0 globules under low oxygen/pH; transient accumulation of SO32− or polythionate during S0 globules or S2O32− oxidationSoxXAYZBCD and Sqr[125]
GammaproteobacteriaBeggiatoa spp.Chemolithoheterotrophy/mixotrophy; intracellular S0 globulesDsr, Sqr, and APS reductase[126]
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Fan, K.; Wang, W.; Xu, X.; Yuan, Y.; Ren, N.; Lee, D.-J.; Chen, C. Recent Advances in Biotechnologies for the Treatment of Environmental Pollutants Based on Reactive Sulfur Species. Antioxidants 2023, 12, 767.

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Fan K, Wang W, Xu X, Yuan Y, Ren N, Lee D-J, Chen C. Recent Advances in Biotechnologies for the Treatment of Environmental Pollutants Based on Reactive Sulfur Species. Antioxidants. 2023; 12(3):767.

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Fan, Kaili, Wei Wang, Xijun Xu, Yuan Yuan, Nanqi Ren, Duu-Jong Lee, and Chuan Chen. 2023. "Recent Advances in Biotechnologies for the Treatment of Environmental Pollutants Based on Reactive Sulfur Species" Antioxidants 12, no. 3: 767.

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