Stepwise pathway for early evolutionary assembly of dissimilatory sulfite and sulfate reduction

Microbial dissimilatory sulfur metabolism utilizing dissimilatory sulfite reductases (Dsr) influenced the biochemical sulfur cycle during Earth’s history and the Dsr pathway is thought to be an ancient metabolic process. Here we performed comparative genomics, phylogenetic, and synteny analyses of s...

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Bibliographic Details
Published in:The ISME Journal 2023-10, Vol.17 (10), p.1680-1692
Main Authors: Neukirchen, Sinje, Pereira, Inês A. C., Sousa, Filipa L.
Format: Article
Language:English
Subjects:
45
45/47
631/181/735
631/181/757
631/326/26/2526
631/326/41/2529
631/326/41/2530
Biomedical and Life Sciences
Complexity
Ecology
Evolutionary Biology
Inventions
Life Sciences
Microbial Ecology
Microbial Genetics and Genomics
Microbiology
Microorganisms
Oxidation
Phylogeny
Proteins
Reductases
Sulfate reduction
Sulfates
Sulfite
Sulfur
Sulfur cycle
Sulfur oxidation
Synteny
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Summary:Microbial dissimilatory sulfur metabolism utilizing dissimilatory sulfite reductases (Dsr) influenced the biochemical sulfur cycle during Earth’s history and the Dsr pathway is thought to be an ancient metabolic process. Here we performed comparative genomics, phylogenetic, and synteny analyses of several Dsr proteins involved in or associated with the Dsr pathway across over 195,000 prokaryotic metagenomes. The results point to an archaeal origin of the minimal DsrABCMK(N) protein set, having as primordial function sulfite reduction. The acquisition of additional Dsr proteins (DsrJOPT) increased the Dsr pathway complexity. Archaeoglobus would originally possess the archaeal-type Dsr pathway and the archaeal DsrAB proteins were replaced with the bacterial reductive-type version, possibly at the same time as the acquisition of the QmoABC and DsrD proteins. Further inventions of two Qmo complex types, which are more spread than previously thought, allowed microorganisms to use sulfate as electron acceptor. The ability to use the Dsr pathway for sulfur oxidation evolved at least twice, with Chlorobi and Proteobacteria being extant descendants of these two independent adaptations.
ISSN:1751-7362
1751-7370
DOI:10.1038/s41396-023-01477-y