Methane, arsenic, selenium and the origins of the DMSO reductase family

Michael Wells,Ronald S Oremland,Narthana Jeganathar Kanmanii,Al Muatasim Al Zadjali,Jan E Janecka,John F Stolz,Partha Basu

doi:10.1038/s41598-020-67892-9

Abstract

Mononuclear molybdoenzymes of the dimethyl sulfoxide reductase (DMSOR) family catalyze a number of reactions essential to the carbon, nitrogen, sulfur, arsenic, and selenium biogeochemical cycles. These enzymes are also ancient, with many lineages likely predating the divergence of the last universal common ancestor into the Bacteria and Archaea domains. We have constructed rooted phylogenies for over 1,550 representatives of the DMSOR family using maximum likelihood methods to investigate the evolution of the arsenic biogeochemical cycle. The phylogenetic analysis provides compelling evidence that formylmethanofuran dehydrogenase B subunits, which catalyze the reduction of CO2 to formate during hydrogenotrophic methanogenesis, constitutes the most ancient lineage. Our analysis also provides robust support for selenocysteine as the ancestral ligand for the Mo/W atom. Finally, we demonstrate that anaerobic arsenite oxidase and respiratory arsenate reductase catalytic subunits represent a more ancient lineage of DMSORs compared to aerobic arsenite oxidase catalytic subunits, which evolved from the assimilatory nitrate reductase lineage. This provides substantial support for an active arsenic biogeochemical cycle on the anoxic Archean Earth. Our work emphasizes that the use of chalcophilic elements as substrates as well as the Mo/W ligand in DMSORs has indelibly shaped the diversification of these enzymes through deep time.

Highlights

Ubiquitous in Archaea and Bacteria, mononuclear molybdoenzymes of the dimethyl sulfoxide reductase (DMSOR) family are believed to have been core components of the first anaerobic respiratory chains, and present at life’s origins[1,2,3,4]
We demonstrate that the ArxA/ArrA lineage is more deeply rooted in the tree topology than AioA, consistent with an Archean origin for chemo- and photolithoautotrophic arsenite oxidation in anoxic environments
The untrimmed phylogeny positions the formate dehydrogenase N catalytic subunits (FdhG) lineage within a clade of DMSOR members that include the respiratory dimethyl sulfoxide reductase (DmsA), respiratory nitrate reductase (NarG), polysulfide reductase of Wolinella succinogenes (PsrA)/PhsA/SrrA, ArxA/ArrA, and TtrA/Selenate reductase (SrdA)/archaeal arsenate reductase lineages that interact with the membrane quinone pool during anaerobic respiration using the canonical subunits identified by Rothery et al.[13]

Summary

Introduction

Ubiquitous in Archaea and Bacteria, mononuclear molybdoenzymes of the dimethyl sulfoxide reductase (DMSOR) family are believed to have been core components of the first anaerobic respiratory chains, and present at life’s origins[1,2,3,4]. Phylogenies constructed using the neighbor-joining method have been used previously to support the idea that AioA was the primordial arsenite oxidase catalytic subunit and present in the last universal common ancestor (LUCA) of the two prokaryotic d omains[1,24,25,26], given that bacterial and archaeal homologs have formed separate monophyletic clades in these tree topologies.

Results

Conclusion