Multiple energy sources and metabolic strategies sustain microbial diversity in Antarctic desert soils
Numerous diverse microorganisms reside in the cold desert soils of continental Antarctica, though we lack a holistic understanding of the metabolic processes that sustain them. Here, we profile the composition, capabilities, and activities of the microbial communities in 16 physicochemically diverse...
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ftunivpretoria:oai:repository.up.ac.za:2263/88530 2023-05-15T14:05:19+02:00 Multiple energy sources and metabolic strategies sustain microbial diversity in Antarctic desert soils Ortiz, Maximiliano Leung, Pok Man Shelley, Guy Jirapanjawat, Thanavit Nauer, Philipp A. Van Goethem, Marc W. Bay, Sean K. Islam, Zahra F. Jordaan, Karen Vikram, Surendra Chown, Steven L. Hogg, Ian Makhalanyane, Thulani P. Grinter, Rhys Cowan, Don A. Greening, Chris 2021-11 https://repository.up.ac.za/handle/2263/88530 https://doi.org/10.1073/pnas.2025322118 en eng National Academy of Sciences https://repository.up.ac.za/handle/2263/88530 Ortiz, M., Leung, P.M., Shelley, G. et al. 2021, 'Multiple energy sources and metabolic strategies sustain microbial diversity in Antarctic desert soils', Proceedings of the National Academy of Sciences of the United States of America, vol. 118, no. 45, art. e2025322118, pp. 1-10, doi : 10.1073/pnas.2025322118. 0027-8424 (print) 1091-6490 (online) doi:10.1073/pnas.2025322118 © 2021 the Author(s). Published by PNAS. Antarctica Actinobacteria Trace gas Metabolic water Hydrogen Article 2021 ftunivpretoria https://doi.org/10.1073/pnas.2025322118 2022-12-06T01:20:53Z Numerous diverse microorganisms reside in the cold desert soils of continental Antarctica, though we lack a holistic understanding of the metabolic processes that sustain them. Here, we profile the composition, capabilities, and activities of the microbial communities in 16 physicochemically diverse mountainous and glacial soils. We assembled 451 metagenome-assembled genomes from 18 microbial phyla and inferred through Bayesian divergence analysis that the dominant lineages present are likely native to Antarctica. In support of earlier findings, metagenomic analysis revealed that the most abundant and prevalent microorganisms are metabolically versatile aerobes that use atmospheric hydrogen to support aerobic respiration and sometimes carbon fixation. Surprisingly, however, hydrogen oxidation in this region was catalyzed primarily by a phylogenetically and structurally distinct enzyme, the group 1l [NiFe]-hydrogenase, encoded by nine bacterial phyla. Through gas chromatography, we provide evidence that both Antarctic soil communities and an axenic Bacteroidota isolate (Hymenobacter roseosalivarius) oxidize atmospheric hydrogen using this enzyme. Based on ex situ rates at environmentally representative temperatures, hydrogen oxidation is theoretically sufficient for soil communities to meet energy requirements and, through metabolic water production, sustain hydration. Diverse carbon monoxide oxidizers and abundant methanotrophs were also active in the soils. We also recovered genomes of microorganisms capable of oxidizing edaphic inorganic nitrogen, sulfur, and iron compounds and harvesting solar energy via microbial rhodopsins and conventional photosystems. Obligately symbiotic bacteria, including Patescibacteria, Chlamydiae, and predatory Bdellovibrionota, were also present. We conclude that microbial diversity in Antarctic soils reflects the coexistence of metabolically flexible mixotrophs with metabolically constrained specialists. DATA AVAILABILTY: All amplicon sequencing data, raw metagenomes, ... Article in Journal/Newspaper Antarc* Antarctic Antarctica University of Pretoria: UPSpace Antarctic Proceedings of the National Academy of Sciences 118 45 |
institution |
Open Polar |
collection |
University of Pretoria: UPSpace |
op_collection_id |
ftunivpretoria |
language |
English |
topic |
Antarctica Actinobacteria Trace gas Metabolic water Hydrogen |
spellingShingle |
Antarctica Actinobacteria Trace gas Metabolic water Hydrogen Ortiz, Maximiliano Leung, Pok Man Shelley, Guy Jirapanjawat, Thanavit Nauer, Philipp A. Van Goethem, Marc W. Bay, Sean K. Islam, Zahra F. Jordaan, Karen Vikram, Surendra Chown, Steven L. Hogg, Ian Makhalanyane, Thulani P. Grinter, Rhys Cowan, Don A. Greening, Chris Multiple energy sources and metabolic strategies sustain microbial diversity in Antarctic desert soils |
topic_facet |
Antarctica Actinobacteria Trace gas Metabolic water Hydrogen |
description |
Numerous diverse microorganisms reside in the cold desert soils of continental Antarctica, though we lack a holistic understanding of the metabolic processes that sustain them. Here, we profile the composition, capabilities, and activities of the microbial communities in 16 physicochemically diverse mountainous and glacial soils. We assembled 451 metagenome-assembled genomes from 18 microbial phyla and inferred through Bayesian divergence analysis that the dominant lineages present are likely native to Antarctica. In support of earlier findings, metagenomic analysis revealed that the most abundant and prevalent microorganisms are metabolically versatile aerobes that use atmospheric hydrogen to support aerobic respiration and sometimes carbon fixation. Surprisingly, however, hydrogen oxidation in this region was catalyzed primarily by a phylogenetically and structurally distinct enzyme, the group 1l [NiFe]-hydrogenase, encoded by nine bacterial phyla. Through gas chromatography, we provide evidence that both Antarctic soil communities and an axenic Bacteroidota isolate (Hymenobacter roseosalivarius) oxidize atmospheric hydrogen using this enzyme. Based on ex situ rates at environmentally representative temperatures, hydrogen oxidation is theoretically sufficient for soil communities to meet energy requirements and, through metabolic water production, sustain hydration. Diverse carbon monoxide oxidizers and abundant methanotrophs were also active in the soils. We also recovered genomes of microorganisms capable of oxidizing edaphic inorganic nitrogen, sulfur, and iron compounds and harvesting solar energy via microbial rhodopsins and conventional photosystems. Obligately symbiotic bacteria, including Patescibacteria, Chlamydiae, and predatory Bdellovibrionota, were also present. We conclude that microbial diversity in Antarctic soils reflects the coexistence of metabolically flexible mixotrophs with metabolically constrained specialists. DATA AVAILABILTY: All amplicon sequencing data, raw metagenomes, ... |
format |
Article in Journal/Newspaper |
author |
Ortiz, Maximiliano Leung, Pok Man Shelley, Guy Jirapanjawat, Thanavit Nauer, Philipp A. Van Goethem, Marc W. Bay, Sean K. Islam, Zahra F. Jordaan, Karen Vikram, Surendra Chown, Steven L. Hogg, Ian Makhalanyane, Thulani P. Grinter, Rhys Cowan, Don A. Greening, Chris |
author_facet |
Ortiz, Maximiliano Leung, Pok Man Shelley, Guy Jirapanjawat, Thanavit Nauer, Philipp A. Van Goethem, Marc W. Bay, Sean K. Islam, Zahra F. Jordaan, Karen Vikram, Surendra Chown, Steven L. Hogg, Ian Makhalanyane, Thulani P. Grinter, Rhys Cowan, Don A. Greening, Chris |
author_sort |
Ortiz, Maximiliano |
title |
Multiple energy sources and metabolic strategies sustain microbial diversity in Antarctic desert soils |
title_short |
Multiple energy sources and metabolic strategies sustain microbial diversity in Antarctic desert soils |
title_full |
Multiple energy sources and metabolic strategies sustain microbial diversity in Antarctic desert soils |
title_fullStr |
Multiple energy sources and metabolic strategies sustain microbial diversity in Antarctic desert soils |
title_full_unstemmed |
Multiple energy sources and metabolic strategies sustain microbial diversity in Antarctic desert soils |
title_sort |
multiple energy sources and metabolic strategies sustain microbial diversity in antarctic desert soils |
publisher |
National Academy of Sciences |
publishDate |
2021 |
url |
https://repository.up.ac.za/handle/2263/88530 https://doi.org/10.1073/pnas.2025322118 |
geographic |
Antarctic |
geographic_facet |
Antarctic |
genre |
Antarc* Antarctic Antarctica |
genre_facet |
Antarc* Antarctic Antarctica |
op_relation |
https://repository.up.ac.za/handle/2263/88530 Ortiz, M., Leung, P.M., Shelley, G. et al. 2021, 'Multiple energy sources and metabolic strategies sustain microbial diversity in Antarctic desert soils', Proceedings of the National Academy of Sciences of the United States of America, vol. 118, no. 45, art. e2025322118, pp. 1-10, doi : 10.1073/pnas.2025322118. 0027-8424 (print) 1091-6490 (online) doi:10.1073/pnas.2025322118 |
op_rights |
© 2021 the Author(s). Published by PNAS. |
op_doi |
https://doi.org/10.1073/pnas.2025322118 |
container_title |
Proceedings of the National Academy of Sciences |
container_volume |
118 |
container_issue |
45 |
_version_ |
1766277133791920128 |