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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Published inProceedings of the National Academy of Sciences - PNAS Vol. 118; no. 45; pp. 1 - 10
Main Authors 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 D., Makhalanyane, Thulani P., Grinter, Rhys, Cowan, Don A., Greening, Chris
Format Journal Article
LanguageEnglish
Published United States National Academy of Sciences 09.11.2021
Subjects
Aerobes
Aerobic microorganisms
Aerobic respiration
Antarctic Regions
Autotrophic Processes
Bayesian analysis
Biodiversity
Biological Sciences
Carbon fixation
Carbon monoxide
Coexistence
Desert Climate
Desert soils
Deserts
Energy harvesting
Energy requirements
Energy sources
Enzymes
Gas chromatography
Gases - metabolism
Genomes
Germfree
Glacial soils
Hydrogen
Hydrogenase
Hydrogenase - metabolism
Ice Cover - microbiology
Iron compounds
Metabolism
Metagenome
Metagenomics
Methanotrophic bacteria
Microbial activity
Microbiota
Microorganisms
Nickel compounds
Oxidation
Oxidation-Reduction
Oxidizing agents
Phototrophic Processes
Phylogeny
Physical Sciences
Sandy soils
Soil Microbiology
Soil microorganisms
Solar energy
Sulfur
Antarctic Regions
Antarctica
actinobacteria
Antarctica
metabolic water
hydrogen
trace gas
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Summary: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.
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Author contributions: M.O., S.L.C., I.D.H., D.A.C., and C.G. conceived the study; D.A.C. and C.G. supervised the study; M.O., P.M.L., D.A.C., and C.G. designed experiments; P.M.L., G.S., and T.J. performed experiments; M.O., P.M.L., G.S., T.J., P.A.N., R.G., D.A.C., and C.G. analyzed data; M.O., P.M.L., R.G., D.A.C., and C.G. wrote the manuscript with input from all authors; I.D.H. and D.A.C. were responsible for the original sampling campaign; M.O. and D.A.C. were responsible for preliminary metagenomic analysis; P.M.L. and C.G. were responsible for metagenomic sequencing, assembly, and annotation; P.M.L., G.S., S.K.B., and C.G. were responsible for community analysis; P.M.L. was responsible for Bayesian divergence analysis; M.O., P.M.L., S.K.B., D.A.C., and C.G. were responsible for enzyme phylogenetic analysis; P.M.L., R.G., and C.G. were responsible for genetic analysis; R.G. and C.G. were responsible for molecular modeling; G.S., T.J., and Z.F.I. were responsible for pure culture experiment; P.M.L., G.S., and C.G. were responsible for biogeochemical analysis; P.M.L., P.A.N., and C.G. were responsible for thermodynamic modeling; P.M.L., M.W.V.G., S.K.G., and C.G. were responsible for geographical and physicochemical analysis; and M.W.V.G., K.J., S.V., and T.P.M. provided theoretical and logistical support.
1M.O. and P.M.L. contributed equally to this work.
Edited by Mary K. Firestone, University of California, Berkeley, CA, and approved September 20, 2021 (received for review December 9, 2020)
ISSN:0027-8424
1091-6490
1091-6490
DOI:10.1073/pnas.2025322118