Biochemistry and molecular biology of lithotrophic sulfur oxidation by taxonomically and ecologically diverse bacteria and archaea

Abstract

Lithotrophic sulfur oxidation is an ancient metabolic process. Ecologically and taxonomically diverged prokaryotes have differential abilities to utilize different reduced sulfur compounds as lithotrophic substrates. Different phototrophic or chemotrophic species use different enzymes, pathways and mechanisms of electron transport and energy conservation for the oxidation of any given substrate. While the mechanisms of sulfur oxidation in obligately chemolithotrophic bacteria, predominantly belonging to Beta- (e.g. Thiobacillus) and Gammaproteobacteria (e.g. Thiomicrospira), are not well established, the Sox system is the central pathway in the facultative bacteria from Alphaproteobacteria (e.g. Paracoccus). Interestingly, photolithotrophs such as Rhodovulum belonging to Alphaproteobacteria also use the Sox system, whereas those from Chromatiaceae and Chlorobi use a truncated Sox complex alongside reverse-acting sulfate-reducing systems. Certain chemotrophic magnetotactic Alphaproteobacteria allegedly utilize such a combined mechanism. Sulfur-chemolithotrophic metabolism in Archaea, largely restricted to Sulfolobales, is distinct from those in Bacteria. Phylogenetic and biomolecular fossil data suggest that the ubiquity of sox genes could be due to horizontal transfer, and coupled sulfate reduction/sulfide oxidation pathways, originating in planktonic ancestors of Chromatiaceae or Chlorobi, could be ancestral to all sulfur-lithotrophic processes. However, the possibility that chemolithotrophy, originating in deep sea, is the actual ancestral form of sulfur oxidation cannot be ruled out.

Generation of Acid Mine Lakes Associated with Abandoned Coal Mines in Northwest Turkey

“…The presence of bacterial species with closest affiliation to Fe-oxidizer bacteria (Acidithiobacillus spp.) indicates that the microbial oxidation of Fe(II) is a significant biogeochemical process in the sediments of AML 2 as noted in previous studies (e.g., Friedrich et al 2005;Rohwerder and Sand 2007;Ghosh and Dam 2009;Schippers et al 2010;Dopson and Johnson 2012;Chen et al 2013). Insignificant variations in pH, along with observed changes in DO and Fe concentration throughout the water column until a depth of 6 m, also suggest co-occurrences of Fe(II) oxidation and precipitation of Fe(III) minerals buffering pH as reported in various AMLs with pH ranging from 2.59 to 3.79 (Kusel 2003;Peiffer et al 2013;Vithana et al 2015).…”

Sulfur oxidizers dominate carbon fixation at a biogeochemical hot spot in the dark ocean

“…Lastly, other bacteria oxidize reduced sulfur compounds via formation of a tetrathionate intermediate. These organisms have no sox genes or an incomplete set of sox genes (Ghosh and Dam, 2009). Environmental genomic data suggest that marine GSOs harbor incomplete sets of sox and dsr genes, oxidizing sulfur via the formation of a tetrathionate intermediate or via the branched thiosulfate oxidation pathway.…”

“…A second group uses the branched thiosulfate oxidation pathway via an incomplete sox system (soxABXYZ, but not soxC or soxD) and the dsr system (Friedrich et al, 2001(Friedrich et al, , 2005Ghosh and Dam, 2009). Once the more reduced sulfur compounds have been exhausted, this group stores elemental sulfur in globules for later oxidation to sulfite by dsr proteins (e.g., sulfite reductase) and to sulfate by Vent plume GSOs TE Mattes et al APS reductase (i.e., AprAB) and ATP sulfurylase (i.e., SAT) (Hensen et al, 2006;Ghosh and Dam, 2009). Lastly, other bacteria oxidize reduced sulfur compounds via formation of a tetrathionate intermediate.…”

The sole cysteine residue (Cys301) of tetrathionate hydrolase from Acidithiobacillus ferrooxidans does not play a role in enzyme activity

“…1) Elemental sulfur from anoxygenic photosynthesis is further oxidized to sulfate by these bacterial species or aerobic sulfur oxidizers such as members of the Paracoccus and Starkeya genera. 2,3) RISCs are abundant in acidic environments such as volcanic and geothermal areas and also in acid mine drainage due to human activities. Chemolithoautotrophic RISCs' oxidizers play a pivotal role as primary producers in such acidic environments.…”

“…[4][5][6] At least two major dissimilatory RISCs oxidation pathways have been proposed, and various enzymes involved in RISCs oxidation metabolism have been identified and characterized. 2,3,[7][8][9][10] One of the most common pathways for RISCs' oxidation is the sulfur-oxidizing (Sox) system which is found in both phototrophic and chemolithotrophic sulfur-oxidizing bacteria. 2,11,12) This pathway has been extensively investigated in the neutrophilic thiosulfate-oxidizing bacterium Paracoccus pantotrophus.…”