Iron or sulfur respiration - an adaptive choice determining the fitness of a natronophilic bacterium Dethiobacter alkaliphilus in geochemicaly contrasting environments.
Haloalkaliphilic microorganisms are double extremophiles functioning optimally at high salinity and pH. Their typical habitats are soda lakes, representing geologically ancient ecosystems which are still widespread on Earth and supposedly harbor relict microbial communities. We compared metabolic features and their genomic determinants in two strains of a single natronophilic species Dethiobacter alkaliphilus, the only cultured representative of 'Dethiobacteria' class within Bacillota phylum. The strains of D. alkaliphilus were previously isolated from geographically remote Mongolian and Kenyan soda lakes. The type strain AHT1T was described as a facultatively chemolithoautotrophic sulfidogen reducing or disproportionating sulfur or thiosulfate, while strain Z-1002 was isolated as a chemolithoautotrophic iron reducer. Here, we uncovered iron reducing ability of strain AHT1T, as well as the capability of strain Z-1002 for thiosulfate reduction and anaerobic Fe(II) oxidation. Key catabolic processes sustaining the growth of both strains appeared to fit the geochemical settings of two contrasting alkaline environments where the majority of Dethiobacterial phylotypes were detected. Those are sulfur-enriched soda lakes and iron-enriched serpentinites. Genome analysis revealed that the most probable determinants of iron and sulfur redox transformations in D. alkaliphilus are multiheme c-type cytochromes. Their phylogeny reconstruction showed that sulfur and thiosulfate respiration is most probably provided by evolutionary early forms of unconventional octaheme tetrathionate and sulfite reductases sharing a root with structurally similar group of OmhA/OcwA Fe(III)-reductases. Large sets of other multihemes are likely to provide Fe(III) reduction in both strains. Also, several different, yet phylogenetically related, determinants of anaerobic Fe(II) oxidation were identified in Z-1002 genome, and the oxidation process was further experimentally proven. Considering these results and phylogenetic relatedness of D. alkaliphilus's sulfur reductases with Fe(III) reducing cytochromes, but not with archetypal bacterial sulfur/thiosulfate reductases, we suggest that sustaining high variation of multiheme cytochromes is an effective adaptive strategy to occupy geochemically contrasting alkaline anaerobic environments. We further propose that sulfur-enriched soda lakes are secondary habitats for D. alkaliphilus comparing to Fe-rich serpentinites, and discuss the evolutionary traits which might occur in prokaryotes on a crucial junction of the biosphere's history, when intensification of the sulfur cycle outweighed the global significance of the iron cycle.