Atmospheric chemosynthesis is phylogenetically and geographically widespread and contributes significantly to carbon fixation throughout cold deserts

• Published in: The ISME Journal
• Main Authors: Ray, Angelique E., Zaugg, Julian, Benaud, Nicole, Chelliah, Devan S., Bay, Sean, Wong, Hon Lun, Leung, Pok Man, Ji, Mukan, Terauds, Aleks, Montgomery, Kate, Greening, Chris, Cowan, Don A., Kong, Weidong, Williams, Timothy J., Hugenholtz, Philip, Ferrari, Belinda C.
• Format: Article in Journal/Newspaper
• Language: English
• Published: Springer Nature 2022
• Subjects: Cold desert soil microbiomes; Moisture; Nutrient limitations; Eastern Antarctic soils; SDG-15: Life on land; Antarctic; Arctic; Antarc*; Antarctica
• Online Access: http://hdl.handle.net/2263/93459; https://doi.org/10.1038/s41396-022-01298-5

DATA AVAILABILITY : Next generation sequencing data that supports the findings of this study have been deposited in GenBank with the accession code PRJNA664610. All other data supporting the findings of this study are available in the article/Supplementary Information. Cold desert soil microbiomes thrive despite severe moisture and nutrient limitations. In Eastern Antarctic soils, bacterial primary production is supported by trace gas oxidation and the light-independent RuBisCO form IE. This study aims to determine if atmospheric chemosynthesis is widespread within Antarctic, Arctic and Tibetan cold deserts, to identify the breadth of trace gas chemosynthetic taxa and to further characterize the genetic determinants of this process. H2 oxidation was ubiquitous, far exceeding rates reported to fulfill the maintenance needs of similarly structured edaphic microbiomes. Atmospheric chemosynthesis occurred globally, contributing significantly (p < 0.05) to carbon fixation in Antarctica and the high Arctic. Taxonomic and functional analyses were performed upon 18 cold desert metagenomes, 230 dereplicated medium-to-high-quality derived metagenome-assembled genomes (MAGs) and an additional 24,080 publicly available genomes. Hydrogenotrophic and carboxydotrophic growth markers were widespread. RuBisCO IE was discovered to co-occur alongside trace gas oxidation enzymes in representative Chloroflexota, Firmicutes, Deinococcota and Verrucomicrobiota genomes. We identify a novel group of high-affinity [NiFe]-hydrogenases, group 1m, through phylogenetics, gene structure analysis and homology modeling, and reveal substantial genetic diversity within RuBisCO form IE (rbcL1E), and high-affinity 1h and 1l [NiFe]-hydrogenase groups. We conclude that atmospheric chemosynthesis is a globally-distributed phenomenon, extending throughout cold deserts, with significant implications for the global carbon cycle and bacterial survival within environmental reservoirs. The Australian Government Research Training Program (RTP) ...