Expanded Genomic Sampling Refines Current Understanding of the Distribution and Evolution of Sulfur Metabolisms in the Desulfobulbales

Abstract

The reconstruction of modern and paleo-sulfur cycling relies on understanding the long-term relative contribution of its main actors; these include microbial sulfate reduction (MSR) and microbial sulfur disproportionation (MSD). However, a unifying theory is lacking for how MSR and MSD, with the same enzyme machinery and intimately linked evolutionary histories, perform two drastically different metabolisms. Here, we aim at shedding some light on the distribution, diversity, and evolutionary histories of MSR and MSD, with a focus on the Desulfobulbales as a test case. The Desulfobulbales is a diverse and widespread order of bacteria in the Desulfobacterota (formerly Deltaproteobacteria) phylum primarily composed of sulfate reducing bacteria. Recent culture- and sequence-based approaches have revealed an expanded diversity of organisms and metabolisms within this clade, including the presence of obligate and facultative sulfur disproportionators. Here, we present draft genomes of previously unsequenced species of Desulfobulbales, substantially expanding the available genomic diversity of this clade. We leverage this expanded genomic sampling to perform phylogenetic analyses, revealing an evolutionary history defined by vertical inheritance of sulfur metabolism genes with numerous convergent instances of transition from sulfate reduction to sulfur disproportionation.

Pyropia yezoensis porphyran alleviates metabolic disorders via modulating gut microbiota in high‐sucrose‐fed Drosophila melanogaster

“…It has been reported that Desulfobacterota and Campilobacterota are composed of sulfate-reducing bacteria and sulfide-oxidizing bacteria respectively. 51,52 Their variations might be related to sulfate groups contained in PYP. Previous studies have also shown that sulfate groups have a positive effect on the ability of natural plant polysaccharides to ameliorate metabolic disorders.…”

“…Desulfobacterota and Campilobacterota showed changes in gut microbiota in the PYP group compared with those in the HS group. It has been reported that Desulfobacterota and Campilobacterota are composed of sulfate‐reducing bacteria and sulfide‐oxidizing bacteria respectively 51,52 . Their variations might be related to sulfate groups contained in PYP.…”

Thiovibrio frasassiensisgen. nov., sp. nov., an autotrophic, elemental sulfur disproportionating bacterium isolated from sulfidic karst sediment, and proposal of Thiovibrionaceae fam. nov.

“…The genes and pathways present in the genome are consistent with the ability of strain RS19-109 T to reduce sulfate with hydrogen, disproportionate thiosulfate, reduce iron, reduce nitrate, and utilize bicarbonate/CO 2 as a carbon source. To date, genomic markers for S 0 disproportionation have not been identified (Slobodkin & Slobodkina, 2019; Ward et al ., 2021), and we were thus unable to ascribe any genes or pathways to the ability of RS19-109 T to disproportionate S 0 .…”

The evolution and spread of sulfur-cycling enzymes reflect the redox state of the early Earth

“…Given the significant limitations and uncertainties presented by the geochemical record, pairing geochemical analysis with top-down phylogenetics approaches can provide a novel perspective into the emergence and spread of distinct sulfur-cycling microbial metabolisms on the early Earth. Though no dedicated molecular clock work to date has been conducted on sulfur metabolisms, genomics-based studies suggest that dissimilatory sulfite and sulfate reduction and sulfide oxidation emerged as early forms of energy metabolism (25)(26)(27)(28). Phylogenetics analysis suggests that the dsr genes, which catalyze the reduction of sulfite to sulfide or in the reverse for sulfide oxidation, were among the first sulfur-based genes to arise (25,27), with the reductive form arising first (29).…”

“…Anaerobic anoxygenic photosynthesizers would likely have emerged soon thereafter, possibly using these genes to oxidize sulfur and sulfide ( 30, 31 ). Genomics analyses also indicate that sulfur disproportionation likely arose subsequently ( 27, 28 ). As the oceans became increasingly oxygenated, thiosulfate would have become more available, paving the way for the evolution of thiosulfate oxidation/reduction via the sox pathway ( 26 ).…”