By weaving together multiple threads encapsulating evolutionary biology, functional genomics and geochemistry, an international team headed by Yong-Guan Zhu from the Institute of Urban Environment of the Chinese Academy of Sciences and Barry P. Rosen of the Herbert Wertheim College of Medicine at Florida International University, and including scientists from Helmholtz Centre for Environmental Research – UFZ and Georgia Institute of Technology, has documented the evolutionary history of arsenic resistance systems facilitating radiation of life into a primordial toxic world. The study was recently published in the Proceedings of the National Academy of Sciences, USA.

Poisoning event in the early Earth

Life evolved in an environment rich in toxic heavy metal(loid)s, and the first organisms had to cope with changing landscapes of toxicity over the course of Earth’s history. One of the most notable events in the early Earth occurred between 2.45 and 2.35 billion years ago, during which the atmospheric oxygen rose to appreciation levels (~ 1% of oxygen present in the atmosphere today). This episode, known as the Great Oxidation Event (GOE), reorganized redox cycling of toxic metal(loid)s, including arsenic. Arsenic existed predominantly in its reduced form (i.e., arsenite) in oxygen-poor environments preceding the GOE. When oxygen built up in the atmosphere, the oxidized arsenic species (i.e., arsenate) took over. “The introduction of new toxicant – arsenate – into the anaerobic biosphere must have represented a catalysm in the history of life” says Professor Yong-Guan Zhu, co-corresponding author of the research article “How our ancestors overcame it remains largely unexplored”.

Modern-day genomes bear imprints of early evolutionary events

Part of the challenge in reconstructing the evolutionary history of arsenic detoxification systems lies with the paucity of fossil records, precluding studies on Precambrian life. “Can modern-day genomes serve as Precambrian fossils? Will ancient biogeochemistry events leave imprints on the composition of extant genomes?” asked the postdoc researcher Dr. Song-Can Chen in UFZ, lead author of the study. Following this direction, the research team compiled genetic data representing a full range of hitherto characterized arsenic resistance pathways from 786 living organisms and mapped their evolutionary origin onto a geological timeline using relaxed molecular clocks approaches. The results imply a genetic expansion of microbial arsenic resistance systems in response to the GOE. Prior to the GOE, microbial communities utilized anoxic pathways; following the GOE, microbes invented new resistance genes for detoxification of oxidized arsenic species. “Genetic innovations enabled ancient microbes to explore more complex ecosystems with stratified arsenic chemistry ensuing the GOE” explains Barry P. Rosen, who initiated this study.

Open questions remain

“Our results provide new insights into major questions of arsenic biology” says Professor Zhu “Further studies that benchmark of geochemical records against the evolutionary timeline present here are required to refine the interactions of metalloid redox chemistry, evolution and planetary history.”

Publication:

The Great Oxidation Event expanded the genetic repertoire of arsenic metabolism and cycling. Song-Can Chen, Guo-Xin Sun, Yu Yan, Konstantinos T. Konstantinidis, Si-Yu Zhang, Ye Deng, Xiao-Min Li, Hui-Ling Cui, Florin Musat, Denny Popp, Barry P. Rosen, Yong-Guan Zhu. Proceedings of the National Academy of Sciences 2016, DOI: 10.1073/pnas.2001063117