Recurrent horizontal transfer of arsenite methyltransferase genes facilitated adaptation of life to arsenic

Song-Can Chen,Barry P Rosen,Ye Deng,Bo-Kai Zhu,Yong-Guan Zhu,Si-Yu Zhang,Christopher Rensing,Guo-Xin Sun

doi:10.1038/s41598-017-08313-2

Abstract

The toxic metalloid arsenic has been environmentally ubiquitous since life first arose nearly four billion years ago and presents a challenge for the survival of all living organisms. Its bioavailability has varied dramatically over the history of life on Earth. As life spread, biogeochemical and climate changes cyclically increased and decreased bioavailable arsenic. To elucidate the history of arsenic adaptation across the tree of life, we reconstructed the phylogeny of the arsM gene that encodes the As(III) S-adenosylmethionine (SAM) methyltransferase. Our results suggest that life successfully moved into arsenic-rich environments in the late Archean Eon and Proterozoic Eon, respectively, by the spread of arsM genes. The arsM genes of bacterial origin have been transferred to other kingdoms of life on at least six occasions, and the resulting domesticated arsM genes promoted adaptation to environmental arsenic. These results allow us to peer into the history of arsenic adaptation of life on our planet and imply that dissemination of genes encoding diverse adaptive functions to toxic chemicals permit adaptation to changes in concentrations of environmental toxins over evolutionary history.

Highlights

Arsenic is a pervasive environmental toxin, and exposure to arsenic was no doubt one of the challenges to the origin of life[1]
We propose that the acquisition of an arsM gene by eukaryotes from bacteria conferred diatoms with the ability to cope with stressful marine arsenic concentrations
Natural selection has favored human AS3MT haplotypes that associate with more efficient arsenic metabolism in populations with generations of severe arsenic exposure as a result of increased expression of the gene[64], and we suggest that Horizontal gene transfer (HGT) followed by selection for higher arsM expression in marine cyanobacteria that resulted in an increase in arsenic methylation rates may contribute to the ability of cyanobacteria to thrive in arsenic-rich marine environments

Summary

Introduction

Arsenic is a pervasive environmental toxin, and exposure to arsenic was no doubt one of the challenges to the origin of life[1]. The composition of genomes and proteomes of extant organisms may bear imprints of ancient biogeochemical events[6,7,8,9] that can help to reconstruct the evolutionary history of how life adapted to ancient changes in arsenic geochemistry. Multiple pathways for detoxification of both inorganic and organic arsenicals have been evolved in microorganisms The genes for these defenses are usually encoded in arsenic resistance (ars) operons[10]. The phylogenetic distribution, geological timing and evolutionary history for arsM were determined using phylogenomic methods By examining these data, we infer the timing and complex genetic events that have marked the history of arsM, representing the genomic fossils that illustrate how life adapts to toxic arsenic throughout evolutionary history

Methods

Results

Conclusion