Abstract—
Microorganisms disproportionating inorganic sulfur compounds are involved in biogeochemical cycles of elements in the modern biosphere. Sulfur-disproportionating prokaryotes are represented by 30 species of the Bacteria domain and belong to the phyla Proteobacteria, Thermodesulfobacteria, and Firmicutes. Most of the sulfur-disproportionating bacteria belong to four orders of the class Deltaproteobacteria. The microorganisms responsible for dismutation of sulfur compounds inhabit freshwater and shallow marine sediments, hypersaline and soda lakes, anthropogenic environments, and various natural thermal ecosystems. Most sulfur-disproportionating organisms are able to use other processes for growth, primarily dissimilatory sulfate reduction. Ability to grow autotrophically was shown for 17 sulfur-disproportionating strains from different phylogenetic groups. The biochemical mechanisms involved in disproportionation of sulfur compounds remain uncertain, which hinders the application of the current omics techniques. Comparative analysis of available complete genomes of the microorganisms capable of elemental sulfur disproportionation is provided. The presence of the complete set of the dissimilatory sulfate reduction genes was found not to be necessary for S0 disproportionation. This process does not require dissimilatory sulfite reductase (Dsr) and adenylyl-sulfate reductase (Apr). Sulfur relay proteins and the elemental sulfur- and/or polysulfides-reducing enzymes are important in sulfur disproportionation, but different microorganisms probably employ different sulfur transferases and polysulfide reductases in these processes.
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MICROBIAL DISPROPORTIONATION OF SULFUR COMPOUNDS
The biogeochemical cycle of sulfur, one of the most important biogenic elements, is presently caused mainly by prokaryotic activity. Sulfur has eight oxidation states, and can participate in a number of redox reactions. Sulfur-oxidizing and sulfate-reducing microorganisms are the best-studied microbial groups involved in the sulfur cycle (see reviews by Rabus et al., 2015; Wasmund et al., 2017). Another group of microorganisms, bacteria disproportionating inorganic sulfur compounds, such as thiosulfate, sulfite, and elemental sulfur, was discovered much later (Bak and Cypionka 1987). In this review, the terms sulfur-disproportionating microorganisms and sulfur disproportionators will be used for these microorganisms, independent on what specific sulfur compound is disproportionated.
Disproportionation or dismutation is a redox reaction in which a compound with an intermediate oxidation state is simultaneously reduced and oxidized, resulting in formation of two different products. Fermentation is the case of disproportionation of organic compounds. Thus, disproportionation of sulfur compounds may be considered inorganic fermentation:
Under standard conditions, the disproportionation of elemental sulfur is an endergonic reaction, but thermodynamic calculations show that it can be energetically favorable if, at a sulfate concentration of 28 mM (seawater salinity), the H2S concentration decreases to a level of 1.0–10.0 mM (Finster, 2008). Such sulfide concentration may result from hydrogen sulfide escape to the gas phase or by binding to the chemicals forming poorly soluble sulfides. Manganese (IV) and iron (III) minerals, e.g., ferrihydrite, are the most efficient sulfide scavengers. In the presence of ferrihydrite disproportionation of elemental sulfur is exergonic even under the standard conditions:
Elemental sulfur (S0) may exist in several allotropic modifications, of which cyclic molecules with eight atoms are the most stable (S8). S0 is very poorly soluble in water (~1 µg/L at 25°C) (Kamyshny 2009). In a number of studies soluble polysulfides formed from S0 in the presence of sulfide were shown to act as electron acceptors for microbial cells, rather than elemental sulfur (Blumentals et al., 1990; Schauder and Muller,1993; Poser et al 2013). Disproportionation of some polysulfides provides more energy gain than S0 disproportionation. (Calculated using the data of Thauer et al., 1977; Kamyshny et al., 2004):
Depending on physicochemical conditions, primarily pH and temperature, sulfur disproportionators may probably use either polysulfides or elemental sulfur. Microbial disproportionation of elemental sulfur was reported to occur at low pH, i.e., under conditions when polysulfide production from S0 must be insignificant (Hardisty et al., 2013). Nanocrystals of elemental sulfur are probably acting as intermediates in this process under acidic conditions (Boyd and Druschel,2013). At higher temperatures the solubility of elemental sulfur increases (15 µg/L at 80°C, Kamyshny 2009), and the energy gain from sulfur disproportionation increases. The change in ΔG°' of S0disproportionation (at \({\text{SO}}_{4}^{{2 - }}\) and H2S concentrations of 28 and 1.0 mM, respectively) at temperature increase from 25 to 70°C is ~10 kJ.
Biogeochemical data indicate that thiosulfate- and sulfur-disproportionating bacteria play an active part in the sulfur cycle in marine ecosystems (Jorgensen, 1990, Canfield and Thumdrup, 1996). Microbial disproportionation of elemental sulfur results in characteristic isotope fractionation, so that the forming sulfide is poor in 34S (Canfield and Thumdrup, 1994). Measurement of the isotopic composition of ancient sedimentary rocks and microscopic analysis of minerals and microfossils supported the hypothesis that the microorganisms involved in S0 disproportionation existed and were biogeochemically active in Archean time (Philippot et al., 2007; Wacey et al., 2011).
Disproportionation of sulfur compounds makes it possible for the cells to gain energy for growth using one organic compound as both an electron donor and electron acceptor and thus minimizing their requirements to the chemical composition of the biotope. Desulfovibrio sulfodismutans, the first described microorganism able to carry out thiosulfate and sulfite disproportionation, was incapable of autotrophic growth and grew only in the presence of acetate as a carbon source (Bak and Phennig, 1987). Ability to disproportionate thiosulfate and sulfite was subsequently shown for a number of autotrophic microorganisms. Ability of prokaryotes to disproportionate elemental sulfur was discovered later (Thamdrup et al., 1993;Lovley and Phillips, 1994). Until recently, little was known concerning microbial disproportionation of sulfur compounds at elevated temperatures, in spite of the important role the sulfur cycle processes could played in the ancient, probably thermal ecosystems (Jackson and McInerney 2000). Thermophilic chemolithoautotrophic sulfur-disproportionating bacteria were recently isolated from various hydrothermal habitats (Slobodkin et al., 2012, 2013, 2016; Kojima et al., 2016; Frolova et al., 2018).
SULFUR-DISPROPORTIONATING MICROORGANISMS
Presently, 36 cultured microbial strains are known to disproportionate sulfur compounds. Fourteen of them were isolated under sulfur disproportionation conditions; for the others strains, this ability was shown later (Table 1).
Phylogeny
Sulfur-disproportionating microorganisms are represented by 30 species of the Bacteria domain and belong to the phyla Proteobacteria, Thermodesulfobacteria, and Firmicutes (Table 2). The highest number of sulfur-disproportionating bacteria belongs to four orders of the class Deltaproteobacteria: Desulfobacterales (4 genera), Desulfovibrionales (4 genera), Desulfurellales (1 genus), and Syntrophobacterales (1 genus). Dissulfuribacter thermophilus, Dissulfurimicrobium hydrothermale, and Dissulfurirhabdus thermomarina are also Deltaproteobacteria with uncertain order and family ranks. Only one sulfur-disproportionating Pantoea strain is known among members of the class Gammaproteobacteria. Members of the genera Caldimicrobium, Thermosulfurimonas, and Thermosulfuriphilus belong to the phylum Thermodesulfobacteria. Members of the genera Desulfotomaculum and Dethiobacter belong to the class Clostridia within the phylum Firmicutes.
Habitats
Sulfur-disproportionating microorganisms occur in various natural and anthropogenic ecosystems (Table 2). Desulfovibrio sulfodismutans, the first described sulfur disproportionator, was isolated from anoxic sludge collected from a freshwater ditch near Konstanz, Germany (Bak and Cypionka, 1987; Bak and Phennig, 1987). Desulfobulbus propionicus, Desulfocapsa thiozymogenes, and Desulfocapsa sp. Cad626 were isolated from the sediments of freshwater lakes and small basins in Europe (Widdel and Pfennig, 1982; Janssen et al, 1996; Peduzzi et al, 2003). Desulfurella amilsii was isolated from acidic sediments of the Tinto River, Spain (Florentino et al 2016). Halophilic Desulfovibrio were found in hypersaline coastal lakes (Krekeler et al., 1997; Warthmann et al., 2005). However, the highest number of sulfur-disproportionating microbial species was isolated from the sediments of continental soda lakes in Eurasia, Africa, and North America. These alkaliphilic bacteria belong to the genera Desulfonatronospira, Desulfonatronovibrio, Desulfonatronum, Desulfurivibrio, Dethiobacter (Pikuta et al., 1998, 2003; Sorokin et al., 2008a, 2008b, 2011; Poser et al., 2013; Perez Bernal et al., 2017).
Desulfocapsa sulfoexigens, Desulfofustis glycolicus and Pantoea agglomerans were isolated from coastal marine sediments (Friedrich et al., 1996; Finster et al., 1998; Francis et al., 2000). The presence of sulfur disproportionators in enrichments carrying out anaerobic methane oxidation (AOM) obtained from marine ecosystems is well-documented. Members of the Desulfosarcina/Desulfococcus cluster are the main bacterial component of the AOM enrichment from the Isis mud volcano, Mediterranean. While these deltaproteobacteria actively disproportionate disulfide and are capable of autotrophic growth, their role in AOM is not completely clear (Milucka et al., 2012). Mesophilic elemental sulfur-disproportionating bacteria were also found in AOM enrichments from methane seeps of the Elba Island (Mediterranean), hydrotherms of the Guaymas Basin (Gulf of California), and a North Sea oil deposit. However, these microorganisms, related to Desulfurivibrio, Desulfocapsa, and uncultured groups of the Deltaproteobacteria, are a minor component of the enrichments, and the probability of their involvement in AOM is low (Wegener et al., 2016).
Sulfur disproportionators occur in diverse anthropogenic environments: Desulfomonile tiedje was isolated from wastewater sediment, Desulfotomaculum thermobenzoicum was retrieved from the sludge of a thermophilic anaerobic digester, while two Desulfotomaculum salinum strains were isolated from the mixture of formation and condensation water of a gas condensate deposit (DeWeerd et al., 1990; Tasaki et al., 1991; Nazina et al., 2005).
Sulfur disproportionators were relatively recently found in natural thermal ecosystems. Thermosulfurimonas dismutans, Dissulfuribacter thermophilus, and Thermosulfuriphilus ammonigenes thrive in deep-sea hydrothermal vents of the Lau spreading center in the Pacific (Slobodkin et al., 2012, 2013; Slobodkina et al., 2017b). Dissulfurirhabdus thermomarina and Thermosulfurimonas marina occur in shallow marine hydrotherms (Kuril Islands) (Slobodkina et al., 2016; Frolova et al., 2017). Dissulfurimicrobium hydrothermale, Caldimicrobium thiodismutans, and two Caldimicrobium rimae strains were isolated from terrestrial hot springs in Kamchatka and Japan (Slobodkin et al., 2016; Kojima et al., 2016; Merkel et al., 2017).
Application of molecular techniques to study the distribution of sulfur-disproportionating prokaryotes is limited due to the absence of unequivocal phylogenetic and functional markers. The 16S rRNA genes of Desulfocapsa species are constantly detected in the ecosystems with low redox potential, especially in methane seeps (Lloyd et al., 2006; Pjevac et al., 2014; Ruff et al., 2015). The 16S rRNA gene sequences of Thermosulfurimonas were detected in deep-sea hydrothermal vents of the Mid-Atlantic Ridge, Guaymas Basin, and Eastern Lau spreading center in the Pacific (Flores et al., 2011; Slobodkin et al., 2012). Caldimicrobium species are widespread in Kamchatka hot neutral springs, where their share in the prokaryotic diversity may be from 1 to 52% (Chernyh et al., 2015; Merkel et al., 2017).
Physiology
Most sulfur-disproportionating microorganisms may also grow by other energy processes (Table 3). However, no growth-supporting metabolic processes, apart from disproportionation, were found for Caldimicrobium thiodismutans, Desulfocapsa sulfoexigens, and Dissulfurimicrobium hydrothermale (Finster et al., 1998; Kojima et al., 2016; Slobodkin et al., 2016). A significant number of sulfur disproportionators are capable of dissimilatory sulfate reduction and were originally described as sulfate reducers. Certainly not all sulfate-reducing prokaryotes are capable of disproportionation, and some Desulfobacter, Desulfobacterium, Desulfotomaculum, and Desulfovibrio do not grow by dismutation (Kramer and Cypionka, 1989). All known sulfur disproportionators are strict anaerobes, except for the facultatively aerobic Pantoea agglomerans (Francis et al., 2000). Many sulfur disproportionators, both capable and incapable of sulfate reduction, reduce various electron acceptors, such as sulfite, thiosulfate, elemental sulfur, nitrate, Fe(III), fumarate, etc. (Table 3). Organic compounds or molecular hydrogen are used as electron donors. Many sulfur disproportionators are able to ferment organic compounds, especially pyruvate. A new microbial process of transformation of inorganic compounds, dissimilatory reduction of nitrate to ammonium with elemental sulfur as an electron donor, was recently reported for deep-sea thermophilic sulfur disproportionators Thermosulfurimonas dismutans, Dissulfuribacter thermophilus, and Thermosulfuriphilus ammonigenes (Slobodkina et al., 2017a; Slobodkina et al., 2017b).
Sulfur disproportionators vary in their capacity for dismutation of various sulfur compounds (Table 3). While thiosulfate is used by most sulfur disproportionators, several microorganisms are unable to disproportionate it. Ability to disproportionate sulfite was tested less often and is known for almost half of the strains. Elemental sulfur is used by all known non-sulfate-reducing sulfur disproportionators, but only two sulfate reducers can use it. The microorganisms for which the ability to disproportionate all three compounds (sulfide, thiosulfate, and elemental sulfur) was shown, include three mesophilic Desulfocapsa strains, as well as six thermophilic bacteria: Caldimicrobium thiodismutans, Dissulfuribacter thermophilus, Dissulfurimicrobium hydrothermale, Thermosulfurimonas dismutans, Thermosulfurimonas marina, and Thermosulfuriphilus ammonigenes (Janssen et al., 1996; Finster et al., 1998; Peduzzi et al., 2003; Kojima et al., 2016; Slobodkin et al., 2012, 2013, 2016; Slobodkina et al., 2017b; Frolova et al., 2018).
Sulfides in the form of H2S, HS–, or S2–, which are formed in the course of sulfur compounds disproportionation, may have a toxic effect on microbial growth. In laboratory cultures, addition of ferrihydrite (poorly crystalline Fe(III) oxide) significantly decrease sulfide concentration in the medium. Depending on strain sensitivity to sulfide, some microorganisms probably grow only in the presence of ferrihydrite, while others can grow without it (Slobodkin et al., 2012, 2013; Poser et al., 2013). The pH of the medium is probably less important, since disproportionation of S0 in the absence of ferrihydrite was demonstrated not only in alkaline, but also in neutral conditions, when the concentration of H2S, the most toxic sulfide form, should be higher (Poser et al., 2013; Florentino et al., 2019).
Many organisms can grow autotrophically while disproportionating sulfur compounds, with CO2 or its anions being the sole carbon source. Capacity for autotrophic growth was shown for 17 sulfur-disproportionating strains from several phylogenetic groups (Table 3). Other microorganisms require a carbon source, i.e., acetate.
Sulfur-disproportionating microorganisms are represented by both mesophilic and thermophilic species (Table 1). Among 13 thermophilic (with optimal growth temperature above 50°C) sulfur disproportionators, Thermosulfurimonas dismutans, growing at 92°C, is the most extreme (Slobodkin et al., 2012). Sulfur-disproportionating prokaryotes isolated from soda lakes are obligate halophiles with pH optimum for growth at 9.5‒10.0 (Table 1). Acid-tolerant Desulfurella amilsii, which reduces sulfur at pH 3.0, was shown to disproportionate elemental sulfur at pH 6.5 (Florentino et al., 2019). S0 disproportionation is probably involved in anaerobic metabolism of Acidithiobacillus ferrooxidans growing at pH 1.8 in the presence of Fe(III) (Osorio et al., 2013).
BIOCHEMICAL MECHANISMS OF DISPROPORTIONATION OF SULFUR COMPOUNDS
Little is known concerning the biochemical mechanisms of disproportionation of sulfur compounds and the enzymes involved in this process. Early research, which included measurement of the enzymatic activity, inhibitor analysis, and radoitracer experiments, did not result in unequivocal description of the disproportionation pathways. These data indicate that sulfate and sulfite disproportionation by Desulfovibriostrains probably involves action of adenosine phosphosulfate (APS) reductase and includes reverse electron flow, with sulfite and elemental sulfur as the possible intermediates of thiosulfate disproportionation (Kramer and Cypionka, 1989; Cypionka et al., 1998). Thiosulfate disproportionation by Desulfocapsa sulfoexigens involves participation of sulfite oxidoreductase, thiosulfate reductase, dissimilatory sulfite reductase, ATP sulfurilase, and APS reductase; however, the enzymes responsible for S0 oxidation by this organism have not been identified (Frederikson and Finster, 2003; Finster, 2008).
The oxidative branch of sulfur disproportionation is presently the least understood. None of the studied genomes contains the genes encoding the enzymes of known pathways for thiosulfate and elemental sulfur oxidation, such as the Sox enzyme system sulfur oxygenase-reductase (Sor), or sulfide: quinone oxidoreductase (Sqr). The presence of dissimilatory sulfite reductase (Dsr) genes in the genomes of most sulfur disproportionators supports the suggestion that, similar to sulfur-oxidizing bacteria, sulfane oxidation to sulfite is catalyzed by this enzyme operating in reverse direction. At the same time, in sulfur disproportionators possessing the Dsr system, the DsrAB subunits belong to the reductive type (Thorup et al., 2017). Moreover, no genes encoding dissimilatory sulfite reductase were found in the genome of Dethiobacter alkaliphilus (Melton et al., 2017). Completeness of sequencing of this genome (95.8%) is, however, insufficient for unequivocal conclusion of the absence of the DsrAB genes. Another hypothesis suggests that elemental sulfur oxidation is carried out by the QmoABC electron transport complex and heterodisulfide reductase (Quatrini et al., 2009; Finster et al., 2013; Mardanov et al., 2016). Further sulfite oxidation to sulfate probably also occurs via the reversible sulfate reduction pathway involving APS reductase. The genes encoding this enzyme were found in all known genomes of sulfur disproportionators, except for Desulfurella amilsii, which probably uses another, presently unknown pathway of sulfite oxidation (Florentino et al., 2017). In addition to the genes of dissimilatory sulfate reduction, the genomes of most microorganisms also contain the genes of membrane-bound molybdopterin oxidoreductases, which may be involved in sulfur metabolism as subunits of thiosulfate, polysulfide, or tetrathionate reductases.
Differential proteomic research on sulfur disproportionation was carried out on Desulfurella amilsii (Florentino et al., 2019). Sixteen proteins were identified only in the cultures grown under conditions of sulfur disproportionation, while 112 proteins exhibited significant differences in activity for the cultures grown under conditions of sulfur reduction and sulfur disproportionation. The elemental sulfur-disproportionating cultures exhibited the highest relative content of rhodanese-like sulfur transferase (DESAMIL20_2007), while most proteins of the Dsr complex were not detected.
COMPARATIVE ANALYSIS OF THE GENOMES OF ELEMENTAL SULFUR-DISPROPORTIONATING MICROORGANISMS
Uncertainty concerning the molecular mechanisms underlying sulfur disproportionation hinders the application of genomic data for investigation of this process. Although analysis of complete genomes in order to determine the biochemical pathways of sulfur metabolism has been carried out at different level of detail for six organisms, genomic determinants of sulfur disproportionation were not revealed (Finster et al., 2013; Mardanov et al., 2016; Slobodkina et al., 2017a; Thorup et al., 2017).
As of March 2019, 18 complete genomes of the microorganisms capable of thiosulfate, sulfite, and elemental sulfur disproportionation have been in public domain. In the present work, comparative analysis of all available complete genomes of the microorganisms capable of S0 disproportionation (10 genomes) was carried out. The analyzed genes and gene clusters included the genes for dissimilatory sulfate reduction, the genes associated with sulfur activation and transfer into the cell, and the genes of membrane-bound molybdopterin oxidoreductases involved in sulfur metabolism (Table 4). The work was carried out using the bioinformatic approaches provided by the RAST (http://rast.nmpdr.org) and IMG/M (https://img.jgi. doe.gov) servers.
None of the studied genomes contained all the genes chosen for analysis. Most genomes contained the key genes for dissimilatory sulfate reduction (Pereira et al., 2011), including sat (sulfate-adenylyl transferase), aprAB (A and B subunits of adenylyl-sulfate reductase), the dsrABD cluster (dissimilatory sulfite reductase), dsrС (protein component of the dissimilatory sulfite reductase), dsrMK (electron-transporting complex associated with adenosyl phosphosulfate reductase). As was stated above, Dethiobacter alkaliphilus, with the genome lacking both dsrABD and dsrС, dsrMK, and qmoABC, as well as Desulfurella amilsii, possessing the Dsr system genes, but not aprAB, qmoABC, and sat, were exceptions.
None of the genomes contained the sox, sor, or sqr genes encoding the proteins responsible for sulfur and thiosulfate oxidation and homologous to those occurring in sulfur-oxidizing microorganisms. The dsrL homologue encoding the Fe-S- and flavin-containing NAD(P)-dependent oxidoreductase involved in sulfur oxidation in Allochromatium vinosum (Lübbe et al., 2006) was found only in the genome of Desulfurella amilsii. Most microorganisms share the genes associated with activation of insoluble sulfur compounds and their transfer into the cells. These include tusA, encoding a small sulfur-transporting protein of the sulfotransferase family, dsrE2,encoding a small transmemebrane protein, and dsrE, encoding the protein acting as a sulfur donor for DsrC in sulfur-oxidizing bacteria (Stockdreher et al., 2012; Venceslau et al., 2014). However, none of these three genes occurs in the genome of Desulfurella amilsii, while Dethiobacter alkaliphilus has no dsrE. Homologues of the DESAMIL20_2007 gene encoding the rhodanese-like sulfur transferase in Desulfurella amilsii, a specific protein predominant under sulfur disproportionation conditions (Florentino et al., 2019), is present in the genomes of Dissulfuribacter thermophilus and Thermosulfurimonas dismutans. The genes of other sulfur transferases with two rhodanese domains (SseA) were detected in the genomes of six analyzed sulfur disproportionators. The genes of molybdopterin-containing thiosulfate and polysulfide reductases (phsA/psrA) were found in all analyzed microorganisms, except for Dethiobacter alkaliphilus. Homologues of the genes encoding the cytoplasmic NAD(P)-dependent hydrogenase, which also catalyzed polysulfide reduction to sulfide (Ma et al., 2000) (sulfide dehydrogenase, SUDH), were found in the genomes of Desulfurella amilsii, Desulfofustis glycolicus, and Dethiobacter alkaliphilus.
Thus, a complete set of dissimilatory sulfate reduction genes is not required for ability to disproportionate elemental sulfur. The presence of the Dsr (dissimilatory sulfite reductase) and Apr (adenylyl-sulfate reductase) enzyme complexes is probably also not required for this process. While the proteins transferring the sulfur-containing groups and the enzymes reducing elemental sulfur and/or polysulfides are the components important for sulfur disproportionation, sulfur transferases and polysulfide reductase of different structure may be responsible for these processes in different microorganisms.
CONCLUSION
Disproportionation of sulfur compounds makes it possible to microorganisms to obtain energy using a single inorganic compound as both an electron donor and electron acceptor. About 50% of the cultured sulfur disproportionators are capable of autotrophic growth. Chemolithoautotrophic microorganisms are an important component of the biogeochemical cycles of carbon and other biogenic elements. Ability of chemolithoautotrophs to carry out primary production of organic matter enables existence of autonomous microbial communities, which probably played an important part in formation of the early Earth biosphere. While the role of microbial disproportionation of sulfur compounds in the present-day biogeochemical cycle of sulfur has been insufficiently studied, wide occurrence of thiosulfate, sulfite, and S0 disproportionation among prokaryotes inhabiting diverse marine and terrestrial biotopes indicate an important biological role of these microorganisms. The presently known sulfur-disproportionating prokaryotes belong to 30 bacterial species, most of which are members of the class Deltaproteobacteria. While ability to disproportionate sulfur compounds is common among sulfate-reducing bacteria, it is not a universal feature of this physiological group. Interestingly, the genomes of some sulfur-disproportionating bacteria unable to reduce sulfate contain a complete set of the genes required for dissimilatory sulfate reduction, so that the reason why these microorganisms are incapable of \({\text{SO}}_{4}^{{2 - }}\) reduction in laboratory cultures remains unclear. Although a number of microorganisms were described, for which dismutation of sulfur compounds is the only type of energy metabolism, it is premature to state the existence of obligate sulfur disproportionators. Thus, Thermosulfurimonas dismutans was recently shown to oxidize elemental sulfur with nitrate as an electron acceptor. New physiological properties may possibly be discovered in other “obligate” sulfur disproportionators. Only hypothetical descriptions of the biochemical mechanisms of sulfur compounds disproportionation exist presently, and the key enzymes of this process have not been determined, which hinders the application of modern omics methods for investigation of this process. Comparative analysis of complete genomes of the elemental sulfur-disproportionating bacteria did not reveal the set of proteins required for S0 dismutation, which was common to all microorganisms. Existence of several different pathways for disproportionation of sulfur compounds is therefore quite probable.
REFERENCES
Bak, F. and Cypionka, H., A novel type of energy metabolism involving fermentation of inorganic sulphur compounds, Nature, 1987, vol. 326, pp. 891‒892.
Bak, F. and Phennig, N., Chemolithotrophic growth of Desulfovibrio sulfodismutans sp. nov. by disproportionation of inorganic sulfur compounds, Arch. Microbiol., 1987, vol. 147, pp. 184‒189.
Blumentals, I.I., Itoh, M., Olson, G.J. and Kelly, R.M., Role of polysulphides in reduction of elemental sulfur by the hyperthermophilic archaebacterium Pyrococcus furiosus, Appl. Environ. Microbiol., 1990, vol. 56, pp. 1255‒1262.
Boyd, E.S. and Druschel, G.K., Involvement of intermediate sulfur species in biological reduction of elemental sulfur under acidic, hydrothermal conditions, Appl. Environ. Microbiol., 2013, vol. 79, pp. 2061‒2068.
Canfield, D.E. and Thamdrup, B., The production of 34S depleted sulfide during bacterial disproportionation of elemental sulfur, Science, 1994, vol. 266, pp. 1973–1975.
Canfield, D.E. and Thamdrup, B., Fate of elemental sulfur in an intertidal sediment, FEMS Microbiol. Ecol., 1996, vol. 19, pp. 95–103.
Chernyh, N.A., Mardanov, A.V., Gumerov, V.M., Miroshnichenko, M.L., Lebedinsky, A.V., Merkel, A.Y., Crowe, D., Pimenov, N.V., Rusanov, I.I., Ravin, N.V., Moran, and M.A., Bonch-Osmolovskaya, E.A., Microbial life in Bourlyashchy, the hottest thermal pool of Uzon Caldera, Kamchatka, Extremophiles, 2015, vol. 19, pp. 1157–1171.
Cypionka, H., Smock, A.M, and Böttcher, M.E., A combined pathway of sulfur compound disproportionation in Desulfovivrio desulfuricans, FEMS Microbiol. Lett., 1998, vol. 166, pp. 181–186.
DeWeerd, K.A., Mandelco, L., Tanner, R.S., Woese, C.R., and Suflita, J.M., Desulfomonile tiedjei gen. nov. and sp. nov., a novel anaerobic, dehalogenating, sulfate-reducing bacterium, Arch. Microbiol., 1990, vol. 154, pp. 23‒30.
Finster, K.A.I., Liesack, W., and Thamdrup, B.O., Elemental sulfur and thiosulfate disproportionation by Desulfocapsa sulfoexigens sp. nov., a new anaerobic bacterium isolated from marine surface sediment, Appl. Environ. Microbiol., 1998, vol. 64, pp. 119‒125.
Finster, K., Microbiological disproportionation of inorganic sulfur compounds, J. Sulfur Chem., 2008, vol. 29, pp. 281–292. https://doi.org/10.1080/17415990802105770
Finster K.W., Kjeldsen K.U., Kube M., Reinhardt R., Mussmann M., Amann R., Schreiber L. Complete genome sequence of Desulfocapsa sulfexigens, a marine deltaproteobacterium specialized in disproportionating inorganic sulfur compounds, Stand. Genomic. Sci. 2013, vol. 8, pp. 58‒68.
Florentino, A.P., Brienza, C., Stams, A.J.M., and Sánchez-Andrea, I., Desulfurella amilsii sp. nov., a novel acidotolerant sulfur-respiring bacterium isolated from acidic river sediments, Int. J. Syst. Evol. Microbiol., 2016, vol. 66, pp. 1249‒1253. https://doi.org/10.1099/ijsem.0.000866
Florentino, A.P., Stams, A.J.M., and Sánchez-Andrea, I., Genome sequence of Desulfurella amilsii strain TR1 and comparative genomics of Desulfurellaceae family, Front. Microbiol., 2017, vol. 8, p. 222.https://doi.org/10.3389/fmicb.2017.00222
Florentino, A.P., Pereira, I.A.C., Boeren, S., van den Born, M., Stams, A.J.M., and Sánchez-Andrea, I., Insight into the sulfur metabolism of Desulfurella amilsii by differential proteomics, Environ. Microbiol., 2019, vol. 21, pp. 209-225. https://doi.org/10.1111/1462-2920.14442
Flores, G.E., Campbell, J.H., Kirshtein, J.D., Meneghin, J., Podar, M., Steinberg, J.I., Seewald, J.S., Tivey, M.K., Voytek, M.A., Yang, Z.K., and Reysenbach, A.L., Microbial community structure of hydrothermal deposits from geochemically different vent fields along the Mid-Atlantic Ridge, Environ. Microbiol., 2011, vol. 13, pp. 2158–2171.
Francis, C.A., Obraztsova, A.Y., and Tebo, B.M., Dissimilatory metal reduction by the facultative anaerobe Pantoea agglomerans SP1, Appl. Environ. Microbiol., 2000, vol. 66, pp. 543‒548.
Frederiksen, T.M. and Finster, K., Sulfite-oxido-reductase is involved in the oxidation of sulfite in Desulfocapsa sulfoexigens during disproportionation of thiosulfate and elemental sulfur, Biodegradation, 2003, vol. 14, pp. 189–198.
Friedrich, M., Springer, N., Ludwig, W., and Schink, B., Phylogenetic positions of Desulfofustis glycolicus gen. nov., sp. nov., and Syntrophobotulus glycolicus gen. nov., sp. nov., two new strict anaerobes growing with glycolic acid, Int. J. Syst. Bacteriol., 1996, vol. 46, pp. 1065‒1069.
Frolova, A.A., Slobodkina, G.B. Baslerov, R.V., Novikov, A.A., Bonch-Osmolovskaya, E.A., and Slobodkin, A.I. Thermosulfurimonas marina sp. nov., an autotrophic sulfur-disproportionating and nitrate-reducing bacterium isolated from a shallow-sea hydrothermal vent, Microbiology (Moscow), 2018, vol. 87, no. 4, pp. 502–507. https://doi.org/10.1134/S0026261718040082
Hardisty, D.S., Olyphant, G.A., Bell, J.B., Johnson, A.P., and Pratt, L.M., Acidophilic sulfur disproportionation, Geochim. Cosmochim. Acta, 2013, vol. 113, pp. 136–151.
Janssen, P.H., Schuhmann, A., Bak, F., and Liesack, W., Disproportionation of inorganic sulfur compounds by the sulfate-reducing bacterium Desulfocapsa thiozymogenes gen. nov., sp. nov., Arch. Microbiol., 1996, vol. 166, pp. 184–192.
Jackson, B.E. and McInerney, M., Thiosulfate disproportionation by Desulfotomaculum thermobenzoicum, Appl. Environ. Microbiol., 2000, vol. 66, pp. 3650‒3653.
Jorgensen, B.B., A thiosulfate shunt in the sulfur cycle ofmarine sediments, Science, 1990, vol. 249, pp. 152‒154.
Kamyshny, A., Jr., Goifman, A., Gun, J., Rizkov, D., and Lev, O., Equilibrium distribution of polysulfide ions in aqueous solutions at 25°C: a new approach for the study of polysulfides' equilibria, Environ. Sci. Technol., 2004, vol. 38, pp. 6633–6644.
Kamyshny, A., Solubility of cyclooctasulfur in pure water and sea water at different temperatures, Geochim. Cosmochim. Acta, 2009, vol. 73, pp. 6022–6028.
Kojima, H., Umezawa, K., and Fukui, M. Caldimicrobium thiodismutans sp. nov., a sulfur-disproportionating bacterium isolated from a hot spring, and emended description of the genus Caldimicrobium, Int. J. Syst. Evol. Microbiol., 2016, vol. 66, pp. 1828‒1831. https://doi.org/10.1099/ijsem.0.000947
Kramer, M. and Cypionka, H., Sulfate formation via ATP sulfurylase in thiosulfate- and sulfite-disproportionating bacteria, Arch. Microbiol., 1989, vol. 151, pp. 232‒237.
Krekeler, D., Sigalevich, P., Teske, A., Cypionka, H., and Cohen, Y., A sulfate-reducing bacterium from the oxic layer of a microbial mat from Solar Lake (Sinai), Desulfovibrio oxyclinae sp. nov., Arch. Microbiol., 1997, vol. 167, pp. 369‒375.
Lloyd, K.G., Lapham, L., and Teske, A., An anaerobic methane- oxidizing community of ANME-1b archaea in hypersaline Gulf of Mexico sediments, Appl. Environ. Microbiol., 2006, vol. 72, pp. 7218–7230. doi:. 00886-06https://doi.org/10.1128/AEM
Lovley, D.R. and Phillips, E.J.P., Novel processes for anaerobic sulfate production from elemental sulfur by sulfate-reducing bacteria, Appl. Environ. Microbiol., 1994, vol. 60, pp. 2394–2399.
Lübbe, Y.J., Youn, H.-S., Timkovich, R., and Dahl, C., Siro(haem)amide in Allochromatium vinosum and relevance of DsrL and DsrN, a homolog of cobyrinic acid a,c-diamide synthase, for sulphur oxidation, FEMS Microbiol. Lett., 2006, vol. 261, pp. 194–202.
Ma, K., Weiss, R., and Adams, M.W.W., Characterization of hydrogenase II from the hyperthermophilic archaeon Pyrococcus furiosus and assessment of its role in sulfur reduction, J. Bacteriol., 2000, vol. 182, pp. 1864–1871.
Mardanov, A.V., Beletsky, A.V., Kadnikov, V.V., Slobodkin, A.I., and Ravin, N.V., Genome analysis of Thermosulfurimonas dismutans, the first thermophilic sulfur-disproportionating bacterium of the phylum Thermodesulfobacteria, Front. Microbiol., 2016, vol. 7, p. 950. https://doi.org/10.3389/fmicb.2016.00950
Melton, E.D., Sorokin, D.Y., Overmars, L., Lapidus, A.L., Pillay, M., Ivanova, N., del Rio, T.G., Kyrpides, N.C., Woyke, T., and Muyzer, G., Draft genome sequence of Dethiobacter alkaliphilus strain AHT1T, a gram-positive sulfidogenic polyextremophile, Stand. Genomic Sci., 2017, vol. 12, p. 57.
Merkel, A.Yu., Pimenov, N.V., Rusanov, I.I., Slobodkin, A.I., Slobodkina, G.B., Tarnovetckii, I.Yu., Frolov, E.N., Dubin, A.V., Perevalova, A.A., and Bonch‑Osmolovskaya, E.A., Microbial diversity and autotrophic activity in Kamchatka hot springs, Extremophiles, 2017, vol. 21, pp. 307–317. https://doi.org/10.1007/s00792-016-0903-1
Milucka, J., Ferdelman, T.G., Polerecky, L., Franzke, D., Wegener, G., Schmid, M., Lieberwirth, I., Wagner, M., Widdel, F., and Kuypers, M.M.,Zero-valent sulphur is a key intermediate in marine methane oxidation, Nature,2012, vol. 491, pp. 541–546. https://doi.org/10.1038/nature11656
Mohn, W.W. and Tiedje, J.M., Catabolic thiosulfate disproportionation and carbon dioxide reduction in strain DCB-1, a reductively dechlorinating anaerobe, J. Bacteriol., 1990, vol. 172, pp. 2065–2070.
Nazina, T.N., Rozanova, E.P., Belyakova, E.V., Lysenko, A.M., Poltaraus, A.B., Tourova, T.P., Osipov, G.A., and Beliaev, S.S., Description of “Desulfotomaculum nigrificans subsp. salinus” as a new species, Desulfotomaculum salinum sp. nov., Microbiology (Moscow), 2005, vol. 74, no. 5, pp. 567–574. https://doi.org/10.1007/s11021-005-0104-x
Obraztsova, A.Y., Francis, C.A., and Bradley, M.T., Sulfur disproportionation by the facultative anaerobe Pantoea agglomerans SP1 as a mechanism for chromium(VI) reduction, Geomicrobiol. J., 2002, vol. 19, pp. 121–132.
Osorio, H., Mangold, S., Denis, Y., Ñancucheo, I., Esparza, M., Johnson, D.B., Bonnefoy, V., Dopson, M., and Holmes, D.S., Anaerobic sulfur metabolism coupled to dissimilatory iron reduction in the extremophile Acidithiobacillus ferrooxidans, Appl. Environ. Microbiol., 2013, vol. 79, pp. 2172‒2181.
Pagani, I., Lapidus, A., Nolan, M., Lucas, S., Hammon, N., Deshpande, S., Cheng, J.F., Chertkov, O., Davenport, K., Tapia, R., Han, C., Goodwin, L., Pitluck, S., Liolios, K., Mavromatis, K., et al., Complete genome sequence of Desulfobulbus propionicus type strain (1pr3), Stand. Genomic Sci., 2011, vol. 4, p. 100. https://doi.org/10.4056/sigs.1613929
Peduzzi, S., Tonalla, M., and Hahn, D., Isolation and characterization of aggregate-forming sulfate-reducing and purple sulfur bacteria from the chemocline of meromictic Lake Cadagno, Switzerland, FEMS Microbiol. Ecol., 2003, vol. 45, pp. 29–37.
Pereira, I.A.C., Ramos, A.R., Grein, F., Marques, M.C., da Silva, S.M., and Venceslau, S.S., A comparative genomic analysis of energy metabolism in sulfate- reducing bacteria and archaea, Front. Microbiol., 2011, vol. 2, p. 69. https://doi.org/10.3389/fmicb.2011.00069
Perez Bernal, M.F., Souza Brito, M.A., Bartoli, M., Aube, J., Fardeau, M.-L., Cuevas Rodriguez, G., Ollivier, B., Guyoneaud, R., and Hirschler-Rea, A., Desulfonatronum parangueonense sp. nov., a sulfate-reducing bacterium isolated from sediment of an alkaline crater lake, Int. J. Syst. Evol. Microbiol., 2017, vol. 67, pp. 4999–5005. https://doi.org/10.1099/ijsem.0.002399
Philippot, P., Van Zuilen, M., Lepot, K., Thomazo, C., Farquhar, J., and Van Kranendonk, M.J., Early Archaean microorganisms preferred elemental sulfur, not sulfate, Science, 2007, vol. 317, pp. 1534–1537.
Pikuta, E.V., Zhilina, T.N., Zavarzin, G.A., Kostrikina, N.A., Osipov, G.A., and Rainey, F.A., Desulfonatronum lacustre gen. nov., sp. nov.: a new alkaliphilic sulfate-reducing bacterium utilizing ethanol, Microbiology (Moscow), 1998, vol. 67, no. 1, pp. 105‒113.
Pikuta, E.V., Hoover, R.B., Bej, A.K, Marsic, D., Whitman, W.B., Cleland, D., and Krader, P., Desulfonatronum thiodismutans sp. nov., a novel alkaliphilic, sulfate-reducing bacterium capable of lithoautotrophic growth, Int. J. Syst. Evol. Microbiol., 2003, vol. 53, pp. 1327–1332.
Poser, A., Lohmayer, R., Vogt, C., Knoeller, K., Planer-Friedrich, B., Sorokin, D., Richnow, H-H., and Finster, K., Disproportionation of elemental sulfur by haloalkaliphilic bacteria from soda lakes, Extremophiles, 2013, vol. 17, pp. 1003‒1012. https://doi.org/10.1007/s00792-013-0582-1
Pjevac, P. Kamyshny, A., Jr., Dyksma, S., and Mußmann, M., Microbial consumption of zero-valence sulfur in marine benthic habitats, Environ. Microbiol., 2014, vol. 16, pp. 3416–3430. https://doi.org/10.1111/1462-2920.12410
Quatrini, R., Appia-Ayme, C., Denis, Y., Jedlicki, E., Holmes, D., and Bonnefoy, V., Extending the models for iron and sulfur oxidation in the extreme acidophile Acidithiobacillus ferrooxidans, BMC Genomics,2009, vol. 10, p. 394. https://doi.org/10.1186/1471-2164-10-394
Rabus, R., Venceslau, S.S., Wohlbrand, L., Voordouw, G., Wall, J.D., and Pereira, I.A.C., A post-genomic view of the ecophysiology, catabolism and biotechnological relevance of sulphate-reducing prokaryotes, Adv. Microb. Physiol., 2015, vol. 66, pp. 55‒321. https://doi.org/10.1016/bs.ampbs.2015.05.002
Ruff, S.E., Biddle, J.F., Teske, A.P., Knittel, K., Boetius, A., and Ramette, A.,Global dispersion and local diversification of the methane seep microbiome, Proc. Natl. Acad. Sci. U. S. A.,2015, vol. 112, pp. 4015–4020. https://doi.org/10.1073/pnas.1421865112
Schauder, R. and Muëller, E., Polysulphide as a possible substrate for sulphur-reducing bacteria, Arch. Microbiol., 1993, vol. 160, pp. 377‒382.
Slobodkin, A.I., Reysenbach, A.-L., Slobodkina, G.B., Baslerov, R.V., Kostrikina, N.A., Wagner, I.D., and Bonch-Osmolovskaya, E.A. Thermosulfurimonas dismutans gen. nov., sp. nov. a novel extremely thermophilic sulfur-disproportionating bacterium from a deep-sea hydrothermal vent, Int. J. Syst. Evol. Microbiol., 2012, vol. 62, pp. 2565‒2571. https://doi.org/10.1099/ijs.0.034397-0
Slobodkin, A.I., Reysenbach, A.-L., Slobodkina, G.B., Kolganova, T.V., Kostrikina, N.A., and Bonch-Osmolovskaya, E.A., Dissulfuribacter thermophilus gen. nov., sp. nov. a novel thermophilic autotrophic sulfur-disproportionating deeply-branching delta-proteobacterium from a deep-sea hydrothermal vent of the Eastern Lau Spreading Center, Int. J. Syst. Evol. Microbiol., 2013, vol. 63, pp. 1967‒1971. https://doi.org/10.1099/ijs.0.046938-0
Slobodkin, A.I., Slobodkina, G.B., Panteleeva, A.N., Chernyh, N.A., Novikov, A.A., and Bonch-Osmolovskaya, E.A., Dissulfurimicrobium hydrothermale gen. nov., sp. nov., a thermophilic, autotrophic, sulfur-disproportionating deltaproteobacterium isolated from a hydrothermal pond of Uzon Caldera, Kamchatka, Int. J. Syst. Evol. Microbiol., 2016, vol. 66, pp. 1022-1026. https://doi.org/10.1099/ijsem.0.000828
Slobodkina, G.B., Kolganova, T.V., Kopitsyn, D.S., Viryasov, M.B., Bonch-Osmolovskaya, E.A., and Slobodkin, A.I., Dissulfurirhabdus thermomarina gen. nov., sp. nov. a thermophilic, autotrophic, sulfite-reducing and disproportionating deltaproteobacterium isolated from a shallow-sea hydrothermal vent, Int. J. Syst. Evol. Microbiol., 2016, vol. 66, pp. 2515‒2519. https://doi.org/10.1099/ijsem.0.001083
Slobodkina, G.B., Mardanov, A.V., Ravin, N.V., Frolova, A.A., Chernyh, N.A., Bonch-Osmolovskaya, E.A., and Slobodkin, A.I., Respiratory ammonification of nitrate coupled to anaerobic oxidation of elemental sulfur in deep-sea autotrophic thermophilic bacteria, Front. Microbiol., 2017a, vol. 8, p. 87. https://doi.org/10.3389/fmicb.2017.00087
Slobodkina, G.B., Reysenbach, A.-L., Kolganova, T.V., Novikov, A.A, Bonch-Osmolovskaya, E.A., and Slobodkin, A.I., Thermosulfuriphilus ammonigenes gen. nov., sp. nov., a thermophilic, chemolithoautotrophic bacterium capable of respiratory ammonification of nitrate with elemental sulfur, Int. J. Syst. Evol. Microbiol., 2017b, vol. 67, pp. 3474‒3479. https://doi.org/10.1099/ijsem.0.002142
Sorokin, D.Y., Tourova, T.P., Henstra, A.M., Stams, A.J.M., Galinski, E.A., and Muyzer, G., Sulfidogenesis under extremely haloalkaline conditions by Desulfonatronospira thiodismutans gen. nov., sp. nov., and Desulfonatronospira delicata sp. nov. – a novel lineage of Deltaproteobacteria from hypersaline soda lakes, Microbiology (UK), 2008a, vol. 154, pp. 1444–1453.
Sorokin, D.Y., Tourova, T.P., Mußmann, M., and Muyzer, G., Dethiobacter alkaliphilus gen. nov. sp. nov., and Desulfurivibrio alkaliphilus gen. nov. sp. nov.: two novel representatives of reductive sulfur cycle from soda lakes, Extremophiles, 2008b, vol. 12, pp. 431‒439.
Sorokin, D.Y., Tourova, T.P., Kolganova, T.V., Detkova, E.N., Galinski, E.A. and Muyzer, G., Culturable diversity of lithotrophic haloalkaliphilic sulfate-reducing bacteria in soda lakes and the description of Desulfonatronum thioautotrophicum sp. nov., Desulfonatronum thiosulfatophilum sp. nov., Desulfonatronovibrio thiodismutans sp. nov., and Desulfonatronovibrio magnus sp. nov., Extremophiles, 2011, vol. 15, pp. 391–401.
Stockdreher, Y., Venceslau, S.S., Josten, M., Sahl, H.G., Pereira, I.A.C., and Dahl, C., Cytoplasmic sulfurtransferases in the purple sulfur bacterium Allochromatium vinosum: evidence for sulfur transfer from DsrEFH to DsrC, PLoS One, 2012, vol. 7, no. 7, e40785.
Tasaki, M., Kamagata, Y., Nakamura, K., and Mikami, E., Isolation and characterization of a thermophilic benzoate-degrading, sulfate-reducing bacterium Desulfotomaculum thermobenzoicum sp. nov., Arch. Microbiol., 1991, vol. 155, pp. 348‒352.
Thamdrup, B., Finster, K., Hansen, J.W., and Bak, F., Bacterial disproportionation of elemental sulfur coupled to chemical reduction of iron or manganese, Appl. Environ. Microbiol., 1993, vol. 59, pp. 101–108.
Thauer, R.K., Jungermann, K., and Decker, K., Energy conservation in chemotrophic anaerobic bacteria, Bacteriol. Rev., 1977, vol. 41, pp. 100–180.
Thorup, C., Schramm, A., Findlay, A.J., Finster, K.W., and Schreiber, L., Disguised as a sulfate reducer: growth of the deltaproteobacterium Desulfurivibrio alkaliphilus by sulfide oxidation with nitrate, mBio, 2017, vol. 8, e00671-17. https://doi.org/10.1128/mBio.00671-17
Trubitsyn, D., Geurink, C., Pikuta, E., Lefèvre, C.T., McShan, W.M., Gillaspy, A.F., and Bazylinski, D., Draft genome sequence of the obligately alkaliphilic sulfate-reducing bacterium Desulfonatronum thiodismutans strain MLF1, Genome Announc., 2014, vol. 2, no. 4, e00741-14. https://doi.org/10.1128/genomeA.00741-14
Venceslau, S.S., Stockdreher, Y., Dahl, C., and Pereira, I.A.C., The “bacterial heterodisulfide” DsrC is a key protein in dissimilatory sulfur metabolism, Biochim. Biophys. Acta, 2014, vol. 1837, pp. 1148–1164.
Warthmann, R., Vasconcelos, C., Sass, H., and McKenzie, J.A., Desulfovibrio brasiliensis sp. nov., a moderate halophilic sulfate-reducing bacterium from Lagoa Vermelha (Brazil) mediating dolomite formation, Extremophiles, 2005, vol. 9, pp. 255–261.
Wacey, D., Kilburn, M.R., Saunders, M., Cliff, J. and Brasier, M.D., Microfossils of sulphur-metabolizing cells in 3.4-billion-yearold rocks of Western Australia, Nat. Geosci., 2011, vol. 4, pp. 698–702.
Wasmund, K., Mußmann, M., and Loy, A., The life sulfuric: microbial ecology of sulfur cycling in marine sediments, Environ. Microbiol. Rep., 2017, vol. 9, pp. 323–344.
Wegener, G., Krukenberg, V., Ruff, S.E., Kellermann, M.Y., and Knittel, K., Metabolic capabilities of microorganisms involved in and associated with the anaerobic oxidation of methane, Front. Microbiol., 2016, vol. 7:46. https://doi.org/10.3389/fmicb.2016.00046
Widdel, F. and Pfennig, N., Studies on dissimilatory sulfate-reducing bacteria that decompose fatty acids. 11. Incomplete oxidation of propionate by Desulfobulbus propionicus gen. nov., sp. nov., Arch. Microbiol., 1982, vol. l31, pp. 360‒365.
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Slobodkin, A.I., Slobodkina, G.B. Diversity of Sulfur-Disproportionating Microorganisms. Microbiology 88, 509–522 (2019). https://doi.org/10.1134/S0026261719050138
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DOI: https://doi.org/10.1134/S0026261719050138