Atmospheric chemosynthesis is phylogenetically and geographically widespread and contributes significantly to carbon fixation throughout cold deserts
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 withi...
Published in: | The ISME Journal |
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Oxford University Press (OUP)
2022
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Online Access: | http://hdl.handle.net/1959.4/unsworks_81297 https://unsworks.unsw.edu.au/bitstreams/34b89145-671e-428d-8776-5a6a2880a939/download https://doi.org/10.1038/s41396-022-01298-5 |
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ftunswworks:oai:unsworks.library.unsw.edu.au:1959.4/unsworks_81297 2024-05-19T07:32:27+00:00 Atmospheric chemosynthesis is phylogenetically and geographically widespread and contributes significantly to carbon fixation throughout cold deserts Ray, AE Zaugg, J Benaud, N Chelliah, DS Bay, S Wong, HL Leung, PM Ji, M Terauds, A Montgomery, K Greening, C Cowan, DA Kong, W Williams, TJ Hugenholtz, P Ferrari, BC 2022-11-01 application/pdf http://hdl.handle.net/1959.4/unsworks_81297 https://unsworks.unsw.edu.au/bitstreams/34b89145-671e-428d-8776-5a6a2880a939/download https://doi.org/10.1038/s41396-022-01298-5 unknown Oxford University Press (OUP) http://hdl.handle.net/1959.4/unsworks_81297 https://unsworks.unsw.edu.au/bitstreams/34b89145-671e-428d-8776-5a6a2880a939/download https://doi.org/10.1038/s41396-022-01298-5 open access https://purl.org/coar/access_right/c_abf2 CC BY https://creativecommons.org/licenses/by/4.0/ free_to_read urn:ISSN:1751-7362 urn:ISSN:1751-7370 ISME Journal, 16, 11, 2547-2560 Carbon Cycle Hydrogenase Ribulose-Bisphosphate Carboxylase Soil Soil Microbiology Verrucomicrobia anzsrc-for: 05 Environmental Sciences anzsrc-for: 06 Biological Sciences anzsrc-for: 10 Technology journal article http://purl.org/coar/resource_type/c_6501 2022 ftunswworks https://doi.org/10.1038/s41396-022-01298-5 2024-05-01T00:11:20Z 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. Article in Journal/Newspaper Antarc* Antarctic Antarctica Arctic UNSW Sydney (The University of New South Wales): UNSWorks The ISME Journal 16 11 2547 2560 |
institution |
Open Polar |
collection |
UNSW Sydney (The University of New South Wales): UNSWorks |
op_collection_id |
ftunswworks |
language |
unknown |
topic |
Carbon Cycle Hydrogenase Ribulose-Bisphosphate Carboxylase Soil Soil Microbiology Verrucomicrobia anzsrc-for: 05 Environmental Sciences anzsrc-for: 06 Biological Sciences anzsrc-for: 10 Technology |
spellingShingle |
Carbon Cycle Hydrogenase Ribulose-Bisphosphate Carboxylase Soil Soil Microbiology Verrucomicrobia anzsrc-for: 05 Environmental Sciences anzsrc-for: 06 Biological Sciences anzsrc-for: 10 Technology Ray, AE Zaugg, J Benaud, N Chelliah, DS Bay, S Wong, HL Leung, PM Ji, M Terauds, A Montgomery, K Greening, C Cowan, DA Kong, W Williams, TJ Hugenholtz, P Ferrari, BC Atmospheric chemosynthesis is phylogenetically and geographically widespread and contributes significantly to carbon fixation throughout cold deserts |
topic_facet |
Carbon Cycle Hydrogenase Ribulose-Bisphosphate Carboxylase Soil Soil Microbiology Verrucomicrobia anzsrc-for: 05 Environmental Sciences anzsrc-for: 06 Biological Sciences anzsrc-for: 10 Technology |
description |
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. |
format |
Article in Journal/Newspaper |
author |
Ray, AE Zaugg, J Benaud, N Chelliah, DS Bay, S Wong, HL Leung, PM Ji, M Terauds, A Montgomery, K Greening, C Cowan, DA Kong, W Williams, TJ Hugenholtz, P Ferrari, BC |
author_facet |
Ray, AE Zaugg, J Benaud, N Chelliah, DS Bay, S Wong, HL Leung, PM Ji, M Terauds, A Montgomery, K Greening, C Cowan, DA Kong, W Williams, TJ Hugenholtz, P Ferrari, BC |
author_sort |
Ray, AE |
title |
Atmospheric chemosynthesis is phylogenetically and geographically widespread and contributes significantly to carbon fixation throughout cold deserts |
title_short |
Atmospheric chemosynthesis is phylogenetically and geographically widespread and contributes significantly to carbon fixation throughout cold deserts |
title_full |
Atmospheric chemosynthesis is phylogenetically and geographically widespread and contributes significantly to carbon fixation throughout cold deserts |
title_fullStr |
Atmospheric chemosynthesis is phylogenetically and geographically widespread and contributes significantly to carbon fixation throughout cold deserts |
title_full_unstemmed |
Atmospheric chemosynthesis is phylogenetically and geographically widespread and contributes significantly to carbon fixation throughout cold deserts |
title_sort |
atmospheric chemosynthesis is phylogenetically and geographically widespread and contributes significantly to carbon fixation throughout cold deserts |
publisher |
Oxford University Press (OUP) |
publishDate |
2022 |
url |
http://hdl.handle.net/1959.4/unsworks_81297 https://unsworks.unsw.edu.au/bitstreams/34b89145-671e-428d-8776-5a6a2880a939/download https://doi.org/10.1038/s41396-022-01298-5 |
genre |
Antarc* Antarctic Antarctica Arctic |
genre_facet |
Antarc* Antarctic Antarctica Arctic |
op_source |
urn:ISSN:1751-7362 urn:ISSN:1751-7370 ISME Journal, 16, 11, 2547-2560 |
op_relation |
http://hdl.handle.net/1959.4/unsworks_81297 https://unsworks.unsw.edu.au/bitstreams/34b89145-671e-428d-8776-5a6a2880a939/download https://doi.org/10.1038/s41396-022-01298-5 |
op_rights |
open access https://purl.org/coar/access_right/c_abf2 CC BY https://creativecommons.org/licenses/by/4.0/ free_to_read |
op_doi |
https://doi.org/10.1038/s41396-022-01298-5 |
container_title |
The ISME Journal |
container_volume |
16 |
container_issue |
11 |
container_start_page |
2547 |
op_container_end_page |
2560 |
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1799470496245350400 |