Sulfur-reducing bacteria are microorganisms able to reduce elemental sulfur (S0) to hydrogen sulfide (H2S). These microbes use inorganic sulfur compounds as electron acceptors to sustain several activities such as respiration, conserving energy and growth, in absence of oxygen. The final product of these processes, sulfide, has a considerable influence on the chemistry of the environment and, in addition, is used as electron donor for a large variety of microbial metabolisms. Several types of bacteria and many non-methanogenic archaea can reduce sulfur. Microbial sulfur reduction was already shown in early studies, which highlighted the first proof of S0 reduction in a vibrioid bacterium from mud, with sulfur as electron acceptor and as electron donor. The first pure cultured species of sulfur-reducing bacteria, Desulfuromonas acetoxidans, was discovered in 1976 and described by Pfennig Norbert and Biebel Hanno as an anaerobic sulfur-reducing and acetate-oxidizing bacterium, not able to reduce sulfate. Only few taxa are true sulfur-reducing bacteria, using sulfur reduction as the only or main catabolic reaction. Normally, they couple this reaction with the oxidation of acetate, succinate or other organic compounds. In general, sulfate-reducing bacteria are able to use both sulfate and elemental sulfur as electron acceptors. Thanks to its abundancy and thermodynamic stability, sulfate is the most studied electron acceptor for anaerobic respiration that involves sulfur compounds. Elemental sulfur, however, is very abundant and important, especially in deep-sea hydrothermal vents, hot springs and other extreme environments, making its isolation more difficult. Some bacteriasuch as Proteus, Campylobacter, Pseudomonas and Salmonellahave the ability to reduce sulfur, but can also use oxygen and other terminal electron acceptors.
Taxonomy Sulfur reducers are known to cover about 74 genera within the Bacteria domain. Several types of sulfur-reducing bacteria have been discovered in different habitats like deep and shallow sea hydrothermal vents, freshwater, volcanic acidic hot springs and others. Many sulfur reducers belong to the phylum Thermodesulfobacteriota (Desulfuromonas, Pelobacter, Desulfurella, Geobacter), the class Gammaproteobacteria, and the phylum Campylobacterota according to GTDB classification. Other phyla that present sulfur-reducing bacteria are: Bacillota (Desulfitobacterium, Ammonifex, and Carboxydothermus), Aquificota (Desulfurobacterium and Aquifex), Synergistota (Dethiosulfovibrio), Deferribacterota (Geovibrio), Thermodesulfobacteriota, Spirochaetota, and Chrysiogenota. +
Table 1. Genera of sulfur-reducing bacteria (NCBI classification).PhylumClassGenus (74) (and species)Aquificota AquificiaAquifex (pyrophilus), Balnearium (lithotrophicum), Desulfurobacterium (crinifex, pacificum, thermolithotrophum), Persephonella (guaimasensis, marina), Thermocrinis (ruber), Thermosulfidibacter (takaii),
Thermovibrio (ammonificans, guaymasensis, ruber)BacteroidotaBacteroidiaPetrimonas (sulfuriphila)CaldisericotaCaldisericiaCaldisericum (exile)CalditrichotaCalditrichaeCaldithrix (abyssi)ChrysiogenotaChrysiogenetesDesulfurispirillum (alkaliphilum)CoprothermobacterotaCoprothermobacteriaCoprothermobacter (proteoliticus)DeferribacterotaDeferribacteresDeferribacter (desulfuricans), Geovibrio (thiophilus)DeinococcotaDeinococci Oceanithermus (desulfurans)BacillotaClostridia Ammonifex (degensii), Carboxydothermus (pertinax), Clostridium (thiosulfatireducens, tunisiense, sulfidigenes), Dethiobacter (alkaliphilus), Desulfitibacter (alkalitolerans), Desulfitispora (alkaliphila), Desulfitobacterium (hafniense, chlororespirans, dehalogenans, metallireducens),
Desulfosporosinus (acididurans, acidiphilus, orientis, meridiei, auripigmenti), Desulfotomaculum (thermosubterraneus, salinum,
geothermicum, reducens, intricatum), Ercella (succinogenes), Halanaerobium (congolense), Halarsenatibacter (silvermanii),
Sporanaerobacter (acetigenes), Thermoanaerobacter (sulfurophilus)PseudomonadotaGammaproteobacteria Acidithiobacillus (ferrooxidans), Pseudomonas (mendocina), Shewanella (putrefaciens)ThermodesulfobacteriotaDesulfobacter (postgatei), Desulfobacterium, Desulfobotulus (alkaliphilus), Desulfobulbus (propionicus), Desulfomicrobium (baculatum), Desulfomonile (tiedjei), Desulfonatronovibrio (thiodismutans), Desulfonatronum (thioautotrophicum), Desulfovermiculus (halophilus),
Desulfovibrio, Desulfurella, Desulfurivibrio (alkaliphilus), Desulfuromonas, Desulfuromusa, Geoalkalibacter (subterraneus), Geobacter,
Hippea (maritima), Pelobacter
Caldimicrobium (exile), Thermodesulfobacterium (geofontis)CampylobacterotaCaminibacter, Hydrogenimonas, Lebetimonas, Nautilia, Nitratiruptor, Sulfurimonas, Sulfurospirillum, Sulfurovum, Thioreductor (incertae sedis), Wolinella (succinogenes)SpirochaetotaSpirochaetiaSpirochaeta (perfilievii, smaragdinae)SynergistotaSynergistiaAnaerobaculum (mobile, thermoterrenum), Dethiosulfovibrio (acidaminovorans, marinus, peptidovorans, russensis), Thermanaerovibrio (acidaminovorans, velox), Thermovirga (lienii),ThermotogotaThermotogaeFervidobacterium (changbaicum, islandicum, nodosum, riparium, ), Geotoga (petraea, subterranea), Marinitoga (camini, hydrogenitolerans, okinawensis, piezophila), Mesotoga (infera, prima), Petrotoga (mexicana, miotherma, mobilis), Thermosipho (aficanus), Thermotoga (lettingae, maritima, naphthophila, neapolitana), +Table 2. Genera of sulfur-reducing bacteria (GTDB classification) PhylumClassGenus (74)Aquificota AquificiaAquifex, Persephonella, Thermocrinis ThermodesulfobacteriotaBalnearium, Desulfurobacterium, ThermovibrioDesulfobacteriaDesulfobacter, Desulfobacterium, DesulfobotulusDesulfobulbiaDesulfobulbus, Desulfurivibrio DesulfovibrioniaDesulfomicrobium, Desulfonatronovibrio, Desulfonatronum, Desulfovermiculus, Desulfovibrio, Desulfuromonadia;Desulfuromonas, Desulfuromusa, Geoalkalibacter, Geobacter, PelobacterDesulfomoniliaDesulfomonileThermodesulfobacteriaCaldimicrobium, Thermodesulfobacterium, ThermosulfidibacteriaThermosulfidibacter BacteroidotaBacteroidiaPetrimonasCaldisericotaCaldisericiaCaldisericumCalditrichota CalditrichiaCaldithrix CampylobacterotaCampylobacteriaCaminibacter, Hydrogenimonas, Lebetimonas, Nautilia, Nitratiruptor, Sulfurimonas, Sulfurospirillum,
Sulfurovum, Wolinella DesulfurelliaDesulfurella, HippeaChrysiogenotaChrysiogenetesDesulfurispirillumCoprothermobacterotaCoprothermobacteriaCoprothermobacterDeferribacterotaDeferribacteresDeferribacter, GeovibrioDeinococcotaDeinococciOceanithermusBacillota_AClostridiaClostridium, Sporanaerobacter ThermoanaerobacteriaThermoanaerobacter Bacillota_BDesulfitobacteriaDesulfitobacterium, DesulfosporosinusDesulfotomaculiaAmmonifex, Carboxydothermus, DesulfotomaculumMoorelliaDesulfitibacter Bacillota_DDethiobacteriaDethiobacterBacillota_FHalanaerobiaHalanaerobium, Halarsenatibacter PseudomonadotaGammaproteobacteriaAcidithiobacillus, Pseudomonas, ShewanellaSpirochaetotaSpirochaetiaSediminispirochaetaSynergistotaSynergistiaAnaerobaculum, Dethiosulfovibrio, Thermanaerovibrio, ThermotogotaThermotogaeFervidobacterium, Geotoga, Marinitoga, Mesotoga, Petrotoga, Thermosipho, ThermotogaUnclassified (from NCBI)Desulfitispora (alkaliphila), Ercella (succinogenes), Thermovirga, Thioreductor
Metabolism Sulfur reduction metabolism is an ancient process, found in the deep branches of the phylogenetic tree. Sulfur reduction uses elemental sulfur (S0) and generates hydrogen sulfide (H2S) as the main end product. This metabolism is widespread in extreme environments, where, especially in recent years, many microorganisms have been isolated, providing new and important data on the subject.
Many sulfur-reducing bacteria are able to produce ATP through lithotrophic sulfur respiration, using zero-valence sulfur as electron acceptor, for instance the genera Wolinella, Ammonifex, Desulfuromonas and Desulfurobacterium. On the other side, there are obligate fermenters able to reduce elemental sulfur, for example Thermotoga, Thermosipho and Fervidobacterium. Among these fermenters, there are species, such as Thermotoga maritina, that are not dependent on sulfur reduction and utilize it as a supplementary electron sink. Some researches propose the hypothesis that polysulfide could be an intermediate of sulfur respiration, due to the conversion of elemental sulfur into polysulfide that occurs in sulfide solutions, performing this reaction:
Pseudomonadota The Pseudomonadota are a major phylum of gram-negative bacteria. There is a wide range of metabolisms. Most members are facultative or obligately anaerobic, chemoautotrophs and heterotrophs. Many are able to move using flagella, and others are nonmotile. They are currently divided into several classes, referred to by Greek letters, based on rRNA sequences: Alphaproteobacteria, Betaproteobacteria, Gammaproteobacteria, Zetaproteobacteria, etc.
Class Gammaproteobacteria The Gammaproteobacteria class include several medically, ecologically and scientifically important groups of bacteria. They are major organisms in diverse marine ecosystems and even extreme environments. This class contains a huge variety of taxonomic and metabolic diversity, including aerobic and anaerobic species, chemolitoauthotrophic, chemoorganotrophic and phototrophic species and also free living, biofilms formers, commensal and symbionts.
Acidithiobacillus spp. Acidithiobacillus are chemolithoautotrophs, gram-negative rod-shaped bacteria, using energy from the oxidation of iron and sulfur-containing minerals for growth. They can live at extremely low pH (pH 1–2) and fix both carbon and nitrogen from the atmosphere. It solubilizes copper and other metals from rocks and plays an important role in nutrient and metal biogeochemical cycling in acid environments. Acidithiobacillus ferrooxidans is abundant in natural environments associated with pyritic ore bodies, coal deposits, and their acidified drainages. It obtains energy from the oxidation of reduced sulfur compounds and can also reduce ferric ions and elemental sulfur, thereby promoting the recycling of iron and sulfur compounds under anaerobic conditions. It can also fix and nitrogen and be a primary producer of carbon and nitrogen in acidic environments.
Shewanella spp. Shewanella are gram-negative, motile bacilli. The first description of the species was provided in 1931, Shewanella putrefaciens, a non-fermentative bacillus with a single polar flagellum that grows well on conventional solid media. This species is pathogenic for humans, even if infections are rare and reported especially in the geographic area characterized by warm climates.
Pseudomonas spp. Pseudomonas are gram-negative chemoorganotrophic Gammaproteobacteria, straight or slightly curved rod-shaped. They can move thanks to one or several polar flagella; rarely nonmotile. Aerobic, having a strictly respiratory type of metabolism with oxygen as the terminal electron acceptor; in some cases, allowing growth anaerobically, nitrate can be used as an alternate electron acceptor. Almost all the species fail to grow under acid conditions (pH 4.5 or lower). Pseudomonas are widely distributed in nature. Some species are pathogenic for humans, animals, or plants. Type species: Pseudomonas mendocina.
Phylum Thermodesulfobacteriota The Thermodesulfobacteriota phylum comprises several morphologically distinct gram-negative, non-spore-forming bacterial groups that exhibit either anaerobic or aerobic growth. They are ubiquitous in marine sediments and contain most of the known sulfur-reducing bacteria (e.g. Desulfuromonas spp.). Aerobic bacteria can digest other bacteria, and several of these members are important constituents of the microflora in soil and water.
Desulfuromusa spp.