Microbial oxidation of sulfur
Most of the sulfur oxidizers are autotrophs that can use reduced sulfur species as electron donors for CO2 fixation. The microbial oxidation of sulfur is an important link in the biogeochemical cycling of sulfur in environments hosting both abundant reduced sulfur species and low concentrations of oxygen, such as marine sediments, oxygen minimum zones (OMZs) and hydrothermal systems.[3]
Ecology
The oxidation of hydrogen sulfide has been considered one of the most important processes in the environment, given that the oceans have had very low oxygen and high sulfidic conditions over most of the Earth's history. The modern analog ecosystems are deep marine basins, for instance in the Black Sea, near the Cariaco trench and the Santa Barbara basin. Other zones of the ocean that experience periodic anoxic and sulfidic conditions are the upwelling zones off the coasts of Chile and Namibia, and hydrothermal vents, which are a key source of H2S to the ocean.[4] Sulfur oxidizing microorganisms (SOM) are thus restricted to upper sediment layers in these environments, where oxygen and nitrate are available. The SOM may play an important yet unconsidered role in carbon sequestration,[5] since some models[6] and experiments with Gammaproteobacteria[7][8] have suggested that sulfur-dependent carbon fixation in marine sediments could be responsible for almost half of total dark carbon fixation in the oceans. Besides, they may have been critical for the evolution of eukaryotic organisms, given that sulfur metabolism could have driven the formation of the symbiotic associations that sustained them[9] (see below).
Although the biological oxidation of reduced sulfur compounds competes with abiotic chemical reactions (e.g. the iron-mediated oxidation of sulfide to iron sulfide (FeS) or pyrite (FeS2)),[10] thermodynamic and kinetic considerations suggest that biological oxidation far exceeds the chemical oxidation of sulfide in most environments.[4] Experimental data from the anaerobic phototroph Chlorobaculum tepidum indicate that microorganisms enhance sulfide oxidation by three or more orders of magnitude.[4] However, the general contribution of microorganisms to total sulfur oxidation in marine sediments is still unknown. The SOM of Alphaproteobacteria, Gammaproteobacteria and Campylobacterota account for average cell abundances of 108 cells/m3 in organic-rich marine sediments.[11] Considering that these organisms have a very narrow range of habitats, as explained below, a major fraction of sulfur oxidation in many marine sediments may be accounted for by these groups.[12]
Given that the maximal concentrations of oxygen, nitrate and sulfide are usually separated in depth profiles, many SOM cannot directly access their hydrogen or electron sources (reduced sulfur species) and energy sources (O2 or nitrate) at the same time. This limitation has led SOM to develop different morphological adaptations.
Another evolutionary strategy of SOM is to partner up with motile eukaryotic organisms. The symbiotic SOM provides carbon and, in some cases, bioavailable nitrogen to the host, and gets enhanced access to resources and shelter in return. This lifestyle has evolved independently in sediment-dwelling ciliates, oligochaetes, nematodes, flatworms and bivalves.[14] Recently, a new mechanism for sulfur oxidation was discovered in filamentous bacteria. It is called electrogenic sulfur oxidation (e-SOx), and involves the formation of multicellular bridges that connect the oxidation of sulfide in anoxic sediment layers with the reduction of oxygen or nitrate in oxic surface sediments, generating electric currents over centimeter distances. The so-called cable bacteria are widespread in shallow marine sediments,[15] and are believed to conduct electrons through structures inside a common periplasm of the multicellular filament,[16] a process that may influence the cycling of elements at aquatic sediment surfaces, for instance, by altering iron speciation.[17] The LSB and cable bacteria seem to be restricted to undisturbed sediment with stable hydrodynamic conditions,[18] while symbiotic SOM and their hosts have been mainly found in permeable coastal sediments.[12]
Microbial diversity
The oxidation of reduced
Anaerobic SOB (AnSOB) are mainly neutrophilic/mesophilic
Biochemistry
There are two described pathways for the microbial oxidation of sulfide:
- The sulfide:quinone oxidorreductase pathway (SQR), widespread in green sulfur bacteria, that involves the formation of intermediate compounds such as
- The Sox pathway,[36] or Kelly-Friedrich pathway as established in the Alphaproteobacteria Paracoccus spp., mediated by the thiosulfate-oxidizing multi-enzyme (TOMES) complex, in which sulfide or elemental sulfur form a complex with the enzyme SoxY and remains bound to it until its final conversion to sulfate.[37][38][39]
Similarly, two pathways for the oxidation of sulfite (SO32-) have been identified:
- The rDsr pathway, used by some microorganisms in the
- The direct oxidation of sulfite to sulfate by a type of mononuclear molybdenum enzyme known as sulfite oxidoreductase. Three different groups of these enzymes are recognized (the xanthine oxidase, sulfite oxidase (SO) and dimethyl sulfoxide reductase families), and they are present in the three domains of life.[41]
On the other hand, at least three pathways exist for the oxidation of thiosulfate (S2O32-) :
- The aforementioned Sox pathway, through which both sulfur atoms in thiosulfate are oxidized to sulfate without the formation of any free intermediate.[37][38][39]
- The oxidation of thiosulfate (S2O32-) via the formation of tetrathionate (S4O62-) intermediate, that is present in several obligate chemolithotrophic Gamma and Betaproteobacteria as well as in facultative chemolithotrophic Alphaproteobacteria.[42]
- The branched thiosulfate oxidation pathway, a mechanism in which water-insoluble globules of intermediate sulfur are formed during the oxidation of thiosulfate and sulfide. It is present in all the anoxygenic photolithotrophic green and purple sulfur bacteria, and the free-living as well as symbiotic strains of certain sulfur-chemolithotrophic bacteria.[43]
In any of these pathways, oxygen is the preferred electron acceptor, but in oxygen-limited environments nitrate, oxidized forms of iron and even organic matter are used instead.[44]
Cyanobacteria normally perform oxygenic photosynthesis using water as electron donor. However, in the presence of sulfide, oxygenic photosynthesis is inhibited, and some cyanobacteria can perform anoxygenic photosynthesis by oxidation of sulfide to thiosulfate − using Photosystem I with sulfite− as a possible intermediate sulfur compound.[45][46]
Oxidation of sulfide
Sulfide oxidation can proceed under aerobic or anaerobic conditions. Aerobic sulfide-oxidizing bacteria usually oxidize sulfide to sulfate and are obligate or facultative chemolithoautotrophs. The latter can grow as heterotrophs, obtaining carbon from organic sources, or as autotrophs, using sulfide as the electron donor (energy source) for CO2 fixation.[3] The oxidation of sulfide can proceed aerobically by two different mechanisms: substrate-level phosphorylation, which is dependent on adenosine monophosphate (AMP), and oxidative phosphorylation independent of AMP,[47] which has been detected in several Thiobacilli (T. denitrificans, T. thioparus, T. novellus and T. neapolitanus), as well as in Acidithiobacillus ferrooxidans.[48] The archaeon Acidianus ambivalens appears to possess both an ADP-dependent and an ADP independent pathway for the oxidation of sulfide.[49] Similarly, both mechanisms operate in the chemoautotroph Thiobacillus denitrificans,[50] which can oxidize sulfide to sulfate anaerobically using nitrate as terminal electron acceptor [51] which is reduced to dinitrogen (N2).[52] Two other anaerobic strains that can perform a similar process were identified as similar to Thiomicrospira denitrificans and Arcobacter.[53]
Among the heterotrophic SOB are included species of Beggiatoa that can grow mixotrophically, using sulfide to obtain energy (autotrophic metabolism) or to eliminate metabolically formed hydrogen peroxide in the absence of catalase (heterotrophic metabolism).[54] Other organisms, such as the Bacteria Sphaerotilus natans [55] and the yeast Alternaria [56] are able to oxidize sulfide to elemental sulfur by means of the rDsr pathway.[57]
Oxidation of elemental sulfur
Some Bacteria and Archaea can aerobically oxidize elemental sulfur to sulfuric acid.[3] Acidithiobacillus ferrooxidans and Thiobacillus thioparus can oxidize sulfur to sulfite by means of an oxygenase enzyme, although it is thought that an oxidase could be used as well as an energy saving mechanism.[58] For the anaerobic oxidation of elemental sulfur, it is thought that the Sox pathway plays an important role, although this is not yet completely understood.[39] Thiobacillus denitrificans uses oxidized forms on nitrogen as energy source and terminal electron acceptor instead of oxygen.[59]
Oxidation of thiosulfate and tetrathionate
Most of the chemosynthetic autotrophic bacteria that can oxidize elemental sulfur to sulfate are also able to oxidize thiosulfate to sulfate as a source of reducing power for carbon dioxide assimilation. However, the mechanisms that they utilize may vary, since some of them, such as the photosynthetic purple bacteria, transiently accumulate extracellular elemental sulfur during the oxidation of tetrathionate before oxidizing it to sulfate, while the green sulfur bacteria do not.[3] A direct oxidation reaction (T. versutus [60]), as well as others that involve sulfite (T. denitrificans) and tetrathionate (A. ferrooxidans, A. thiooxidans and Acidiphilum acidophilum [61]) as intermediate compounds, have been proposed. Some mixotrophic bacteria only oxidize thiosulfate to tetrathionate.[3]
The mechanism of bacterial oxidation of tetrathionate is still unclear and may involve sulfur disproportionation, during which both sulfide and sulfate are produced from reduced sulfur species, and hydrolysis reactions.[3]
Isotope fractionations
The fractionation of sulfur and oxygen isotopes during microbial sulfide oxidation (MSO) has been studied to assess its potential as a proxy to differentiate it from the abiotic oxidation of sulfur.[62] The light isotopes of the elements that are most commonly found in organic molecules, such as 12C, 16O, 1H, 14N and 32S, form bonds that are broken slightly more easily than bonds between the corresponding heavy isotopes, 13C, 18O, 2H, 15N and 34S . Because there is a lower energetic cost associated with the use of light isotopes, enzymatic processes usually discriminate against the heavy isotopes, and, as a consequence, biological fractionations of isotopes are expected between the reactants and the products. A normal kinetic isotope effect is that in which the products are depleted in the heavy isotope relative to the reactants (low heavy isotope to light isotope ratio), and although this is not always the case, the study of isotope fractionations between enzymatic processes may allow tracing the source of the product.
Fractionation of oxygen isotopes
The formation of
Starting compound (reactant) | Intermediate or end compounds (products) |
Organism | Average 18O fractionation (product/reactant) | Details | Reference |
Sulfide | Sulfate | A. ferrooxidans (chemolithotroph) | 4.1‰ (30 °C) | Aerobic | Taylor et al. (1984)[64] |
A. ferrooxidans (chemolithotroph) | 6.4‰ 3.8‰ (no temperature provided) |
Aerobic
Anaerobic |
Thurston et al. (2010)[65] | ||
Thiomicrospira sp. strain CVO (chemolithotroph) | 0‰
(no temperature provided) |
Anaerobic, coupled to DNR | Hubert et al. (2009)[66] | ||
T. denitrificans (chemolithotroph) Sulfurimonas denitrificans (chemolithotroph) |
−6 to −1.8‰ (30 °C)
|
Anaerobic, coupled to DNR, SQR pathway Anaerobic, coupled to DNR, Sox pathway |
Poser et al. (2014)[63] | ||
Elemental sulfur | Sulfate | Desulfocapsa thiozymogenes
(chemolithotroph; "cable bacteria") Enrichment culture |
11.0 to 18.4‰ (28 °C)
12.7 to 17.9‰ (28 °C) |
Disproportionation, in the presence of iron scavengers | Böttcher et al. (2001)[67] |
Desulfocapsa thiozymogenes
(chemolithotroph; "cable bacteria") Enrichment culture |
8 to 12 ‰ (28 °C) | Disproportionation, attenuated isotope effect due to reoxidation by manganese oxides | Böttcher & Thamdrup (2001)[68] |
Fractionation of sulfur isotopes
Aerobic MSO generates depletions in the 34S of sulfate that have been found to be as small as −1.5‰ and as large as -18‰. For most microorganisms and oxidation conditions, only small fractionations accompany either the aerobic or anaerobic oxidation of sulfide, elemental sulfur, thiosulfate and sulfite to elemental sulfur or sulfate. The phototrophic oxidation of sulfide to thiosulfate under anoxic conditions also generates negligible fractionations. Although the change in sulfur isotopes is usually small during MSO, MSO oxidizes reduced forms of sulfur which are usually depleted in 34S compared to seawater sulfate. Therefore large-scale MSO can also significantly change the sulfur isotopes of a reservoir. It has been proposed that the observed global average S-isotope fractionation is around −50‰ instead of the theoretically predicted value -70‰ because of MSO.[69]
In the chemolithotrophs Thiobacillus denitrificans and Sulfurimonas denitrificans, MSO coupled to DNR has the effect of inducing the SQR and Sox pathways, respectively. In both cases, a small fractionation in the 34S of the sulfate, lower than -4.3‰, has been measured. Sulfate depletion in 34S from MSO could be used to trace sulfide oxidation processes in the environment, although it does not allow a discrimination between the SQR and Sox pathways.[63] The depletion produced by MSO coupled to DNR is similar to up to -5‰ depletion estimated for the 34S in the sulfide produced from rDsr.[70][71] In contrast, disproportionation under anaerobic conditions generates sulfate enriched in 34S up to 9‰ and ~34‰ from sulfide and elemental sulfur, respectively. The isotope effect of disproportionation is however limited by the rates of sulfate reduction and MSO.[72] Just like the fractionation of oxygen isotopes, the larger fractionations in sulfate from the disproportionation of elemental sulfur point to a key step or pathway critical for inducing this large kinetic isotope effect. The table below summarizes the reported fractionations of sulfur isotopes from MSO in different organisms and conditions.
Starting compound (reactant) | Intermediate or end compounds (products) |
Organism | Average 34S fractionation
(product/reactant) |
Details | Oxidant | Reference |
Sulfide | Sulfate | T. neopolitanus, T. intermedius and T. ferrooxidans (chemolithotrophs) | -2 to -5.5‰
(no temperature provided) |
Aerobic pH 5 to 6 |
Carbon dioxide | Toran (1986)[73] |
---|---|---|---|---|---|---|
Polythionates (SnO62-) Elemental sulfur Sulfate |
T. concretivorus (chemolithotroph) | 0.6 to 19‰ (30 °C) -2.5 to 1.2‰ (30 °C) -18 to -10.5‰ (30 °C) |
Aerobic | Carbon dioxide | Kaplan & Rittenberg (1964)[74] | |
Sulfate | A. ferrooxidans (chemolithotroph) | −1.5‰ −4‰ (no temperature provided) |
Aerobic
Anaerobic |
Carbon dioxide | Thurston et al. (2010)[65] | |
Sulfate | T. denitrificans (chemolithotroph) Sulfurimonas denitrificans (chemolithotroph) |
−4.3 to −1.3‰ (30 °C)
−2.9 to −1.6‰ (28 °C) |
Anaerobic, coupled to DNR, SQR pathway Anaerobic, coupled to DNR, Sox pathway |
Carbon dioxide | Poser et al. (2014)[63] | |
Sulfate | Thiomicrospira sp. strain CVO
(chemolithotroph) |
1‰ (no temperature provided) | Anaerobic, coupled to DNR, no intermediates in complete oxidation of sulfide to sulfate (potentially only uses Sox pathway) | Carbon dioxide | Hubert et al. (2009)[66] | |
Elemental sulfur | Chlorobium thiosulphatophilum (green sulfur bacteria) |
5‰ (no temperature provided) | Anaerobic | Carbon dioxide | Kelly et al. (1979)[75] | |
Thiosulfate | Oscillatoria sp. (Cyanobacteria)
Calothrix sp. (Cyanobacteria) |
0‰ (30 °C) | Anaerobic, anoxygenic photosynthesis | Carbon dioxide | Habicht et al.(1988)[76] | |
Elemental sulfur
Sulfate |
Chromatium vinosum (purple sulfur bacteria) | 0‰ (30-35 °C)
2‰ (30-35 °C) |
Anaerobic, anoxygenic photosynthesis | Fry et al. (1985)[77] | ||
Elemental sulfur
Sulfate |
Ectothiorhodospira shaposhnikovii (purple sulfur bacteria) | ±5‰ (no temperature provided) | Anaerobic, anoxygenic photosynthesis | Ivanov et al. (1976)[78] | ||
Polythionates (SnO62-) Elemental sulfur Sulfate |
Chromatium sp. (purple sulfur bacteria) | 4.9 to 11.2‰ (30 °C) -10 to -3.6‰ (30 °C) -2.9 to -0.9‰ (30 °C) |
Anaerobic | Kaplan & Rittenberg (1964)[74] | ||
Thiosulfate | Sulfate | T. intermedius (chemolithotroph) | -4.7‰ (no temperature provided) | Aerobic | Kelly et al. (1979)[75] | |
Sulfate | T. versutus (chemolithotroph) | 0‰ (28 °C) | Aerobic | Fry et al. (1986)[79] | ||
Elemental sulfur + Sulfate | Chromatium vinosum (purple sulfur bacteria) | 0‰ (30-35 °C) | Anaerobic | Fry et al. (1985)[77] | ||
Sulfate | Desulfovibrio sulfodismutans
(chemolithotroph) D. thiozymogenes (chemolithotroph; "cable bacteria") |
For both bacteria:
0‰ (30 °C; compared to the sulfonate functional group); 2 to 4‰ (30 °C; compared to the sulfane functional group) |
Anaerobic, disproportionation | Habicht et al.(1988)[76] | ||
Elemental sulfur | Sulfate | Desulfocapsa thiozymogenes
(chemolithotroph; "cable bacteria") Enrichment culture |
17.4‰ (28 °C)
16.6‰ (28 °C) |
Anaerobic, disproportionation, in the presence of iron scavengers | Böttcher et al. (2001)[67] | |
Desulfocapsa sulfoexigens
Desulfocapsa thiozymogenes (chemolithotrophs; "cable bacteria") Desulfobulbus propionicus (chemoorganotroph) Marine enrichments and sediments |
16.4‰ (30 °C)
17.4‰ (30 °C) 33.9‰ (35 °C) 17.1 to 20.6‰ (28 °C) |
Anaerobic, disproportionation | Canfield et al. (1998)[80] | |||
Desulfocapsa thiozymogenes
(chemolithotroph; "cable bacteria") Enrichment culture |
−0.6 to 2.0‰ (28 °C)
−0.2 to 1.1‰ (28 °C) |
Anaerobic, disproportionation, attenuated isotope effect due to reoxidation by manganese oxides | Böttcher & Thamdrup (2001)[68] | |||
Sulfite | Sulfate | Desulfovibrio sulfodismutans
(chemolithotroph) D. thiozymogenes (chemolithotroph; "cable bacteria") |
9 to 12‰ (30 °C)
7 to 9‰ (30 °C) |
Anaerobic, disproportionation | Habicht et al.(1988)[76] |
See also
- Isotope fractionation
- Microbial metabolism
- Sulfur metabolism
- Sulfate-reducing microorganisms
- Dissimilatory sulfate reduction
- Dissimilatory nitrate reduction
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