Elevational Constraints on the Composition and Genomic Attributes of Microbial Communities in Antarctic Soils
Antarctic soils represent an ideal system to study how environmental properties shape the taxonomic and functional diversity of microbial communities given the relatively low diversity of Antarctic soil microbial communities and the pronounced environmental gradients that occur across soils located...
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| Published in | mSystems Vol. 7; no. 1; p. e0133021 |
|---|---|
| Main Authors | , , , , , , , , |
| Format | Journal Article |
| Language | English |
| Published |
United States
American Society for Microbiology
22.02.2022
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| Subjects | |
| Online Access | Get full text |
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| Abstract | Antarctic soils represent an ideal system to study how environmental properties shape the taxonomic and functional diversity of microbial communities given the relatively low diversity of Antarctic soil microbial communities and the pronounced environmental gradients that occur across soils located in reasonable proximity to one another. Moreover, the challenging environmental conditions typical of most Antarctic soils present an opportunity to investigate the traits that allow soil microbes to persist in some of the most inhospitable habitats on Earth.
The inland soils found on the Antarctic continent represent one of the more challenging environments for microbial life on Earth. Nevertheless, Antarctic soils harbor unique bacterial and archaeal (prokaryotic) communities able to cope with extremely cold and dry conditions. These communities are not homogeneous, and the taxonomic composition and functional capabilities (genomic attributes) of these communities across environmental gradients remain largely undetermined. We analyzed the prokaryotic communities in soil samples collected from across the Shackleton Glacier region of Antarctica by coupling quantitative PCR, marker gene amplicon sequencing, and shotgun metagenomic sequencing. We found that elevation was the dominant factor explaining differences in the structures of the soil prokaryotic communities, with the drier and saltier soils found at higher elevations harboring less diverse communities and unique assemblages of cooccurring taxa. The higher-elevation soil communities also had lower maximum potential growth rates (as inferred from metagenome-based estimates of codon usage bias) and an overrepresentation of genes associated with trace gas metabolism. Together, these results highlight the utility of assessing community shifts across pronounced environmental gradients to improve our understanding of the microbial diversity found in Antarctic soils and the strategies used by soil microbes to persist at the limits of habitability.
IMPORTANCE
Antarctic soils represent an ideal system to study how environmental properties shape the taxonomic and functional diversity of microbial communities given the relatively low diversity of Antarctic soil microbial communities and the pronounced environmental gradients that occur across soils located in reasonable proximity to one another. Moreover, the challenging environmental conditions typical of most Antarctic soils present an opportunity to investigate the traits that allow soil microbes to persist in some of the most inhospitable habitats on Earth. We used cultivation-independent methods to study the bacterial and archaeal communities found in soil samples collected from across the Shackleton Glacier region of the Transantarctic Mountains. We show that those environmental characteristics associated with elevation have the greatest impact on the structure of these microbial communities, with the colder, drier, and saltier soils found at higher elevations sustaining less diverse communities that were distinct from those in more hospitable soils with respect to their composition, genomic attributes, and overall life-history strategies. Notably, the harsher conditions found in higher-elevation soils likely select for taxa with lower maximum potential growth rates and an increased reliance on trace gas metabolism to support growth. |
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| AbstractList | The inland soils found on the Antarctic continent represent one of the more challenging environments for microbial life on Earth. Nevertheless, Antarctic soils harbor unique bacterial and archaeal (prokaryotic) communities able to cope with extremely cold and dry conditions. These communities are not homogeneous, and the taxonomic composition and functional capabilities (genomic attributes) of these communities across environmental gradients remain largely undetermined. We analyzed the prokaryotic communities in soil samples collected from across the Shackleton Glacier region of Antarctica by coupling quantitative PCR, marker gene amplicon sequencing, and shotgun metagenomic sequencing. We found that elevation was the dominant factor explaining differences in the structures of the soil prokaryotic communities, with the drier and saltier soils found at higher elevations harboring less diverse communities and unique assemblages of cooccurring taxa. The higher-elevation soil communities also had lower maximum potential growth rates (as inferred from metagenome-based estimates of codon usage bias) and an overrepresentation of genes associated with trace gas metabolism. Together, these results highlight the utility of assessing community shifts across pronounced environmental gradients to improve our understanding of the microbial diversity found in Antarctic soils and the strategies used by soil microbes to persist at the limits of habitability.
IMPORTANCE
Antarctic soils represent an ideal system to study how environmental properties shape the taxonomic and functional diversity of microbial communities given the relatively low diversity of Antarctic soil microbial communities and the pronounced environmental gradients that occur across soils located in reasonable proximity to one another. Moreover, the challenging environmental conditions typical of most Antarctic soils present an opportunity to investigate the traits that allow soil microbes to persist in some of the most inhospitable habitats on Earth. We used cultivation-independent methods to study the bacterial and archaeal communities found in soil samples collected from across the Shackleton Glacier region of the Transantarctic Mountains. We show that those environmental characteristics associated with elevation have the greatest impact on the structure of these microbial communities, with the colder, drier, and saltier soils found at higher elevations sustaining less diverse communities that were distinct from those in more hospitable soils with respect to their composition, genomic attributes, and overall life-history strategies. Notably, the harsher conditions found in higher-elevation soils likely select for taxa with lower maximum potential growth rates and an increased reliance on trace gas metabolism to support growth. The inland soils found on the Antarctic continent represent one of the more challenging environments for microbial life on Earth. Nevertheless, Antarctic soils harbor unique bacterial and archaeal (prokaryotic) communities able to cope with extremely cold and dry conditions. These communities are not homogeneous, and the taxonomic composition and functional capabilities (genomic attributes) of these communities across environmental gradients remain largely undetermined. We analyzed the prokaryotic communities in soil samples collected from across the Shackleton Glacier region of Antarctica by coupling quantitative PCR, marker gene amplicon sequencing, and shotgun metagenomic sequencing. We found that elevation was the dominant factor explaining differences in the structures of the soil prokaryotic communities, with the drier and saltier soils found at higher elevations harboring less diverse communities and unique assemblages of cooccurring taxa. The higher-elevation soil communities also had lower maximum potential growth rates (as inferred from metagenome-based estimates of codon usage bias) and an overrepresentation of genes associated with trace gas metabolism. Together, these results highlight the utility of assessing community shifts across pronounced environmental gradients to improve our understanding of the microbial diversity found in Antarctic soils and the strategies used by soil microbes to persist at the limits of habitability. IMPORTANCE Antarctic soils represent an ideal system to study how environmental properties shape the taxonomic and functional diversity of microbial communities given the relatively low diversity of Antarctic soil microbial communities and the pronounced environmental gradients that occur across soils located in reasonable proximity to one another. Moreover, the challenging environmental conditions typical of most Antarctic soils present an opportunity to investigate the traits that allow soil microbes to persist in some of the most inhospitable habitats on Earth. We used cultivation-independent methods to study the bacterial and archaeal communities found in soil samples collected from across the Shackleton Glacier region of the Transantarctic Mountains. We show that those environmental characteristics associated with elevation have the greatest impact on the structure of these microbial communities, with the colder, drier, and saltier soils found at higher elevations sustaining less diverse communities that were distinct from those in more hospitable soils with respect to their composition, genomic attributes, and overall life-history strategies. Notably, the harsher conditions found in higher-elevation soils likely select for taxa with lower maximum potential growth rates and an increased reliance on trace gas metabolism to support growth. ABSTRACT The inland soils found on the Antarctic continent represent one of the more challenging environments for microbial life on Earth. Nevertheless, Antarctic soils harbor unique bacterial and archaeal (prokaryotic) communities able to cope with extremely cold and dry conditions. These communities are not homogeneous, and the taxonomic composition and functional capabilities (genomic attributes) of these communities across environmental gradients remain largely undetermined. We analyzed the prokaryotic communities in soil samples collected from across the Shackleton Glacier region of Antarctica by coupling quantitative PCR, marker gene amplicon sequencing, and shotgun metagenomic sequencing. We found that elevation was the dominant factor explaining differences in the structures of the soil prokaryotic communities, with the drier and saltier soils found at higher elevations harboring less diverse communities and unique assemblages of cooccurring taxa. The higher-elevation soil communities also had lower maximum potential growth rates (as inferred from metagenome-based estimates of codon usage bias) and an overrepresentation of genes associated with trace gas metabolism. Together, these results highlight the utility of assessing community shifts across pronounced environmental gradients to improve our understanding of the microbial diversity found in Antarctic soils and the strategies used by soil microbes to persist at the limits of habitability. IMPORTANCE Antarctic soils represent an ideal system to study how environmental properties shape the taxonomic and functional diversity of microbial communities given the relatively low diversity of Antarctic soil microbial communities and the pronounced environmental gradients that occur across soils located in reasonable proximity to one another. Moreover, the challenging environmental conditions typical of most Antarctic soils present an opportunity to investigate the traits that allow soil microbes to persist in some of the most inhospitable habitats on Earth. We used cultivation-independent methods to study the bacterial and archaeal communities found in soil samples collected from across the Shackleton Glacier region of the Transantarctic Mountains. We show that those environmental characteristics associated with elevation have the greatest impact on the structure of these microbial communities, with the colder, drier, and saltier soils found at higher elevations sustaining less diverse communities that were distinct from those in more hospitable soils with respect to their composition, genomic attributes, and overall life-history strategies. Notably, the harsher conditions found in higher-elevation soils likely select for taxa with lower maximum potential growth rates and an increased reliance on trace gas metabolism to support growth. Antarctic soils represent an ideal system to study how environmental properties shape the taxonomic and functional diversity of microbial communities given the relatively low diversity of Antarctic soil microbial communities and the pronounced environmental gradients that occur across soils located in reasonable proximity to one another. Moreover, the challenging environmental conditions typical of most Antarctic soils present an opportunity to investigate the traits that allow soil microbes to persist in some of the most inhospitable habitats on Earth. The inland soils found on the Antarctic continent represent one of the more challenging environments for microbial life on Earth. Nevertheless, Antarctic soils harbor unique bacterial and archaeal (prokaryotic) communities able to cope with extremely cold and dry conditions. These communities are not homogeneous, and the taxonomic composition and functional capabilities (genomic attributes) of these communities across environmental gradients remain largely undetermined. We analyzed the prokaryotic communities in soil samples collected from across the Shackleton Glacier region of Antarctica by coupling quantitative PCR, marker gene amplicon sequencing, and shotgun metagenomic sequencing. We found that elevation was the dominant factor explaining differences in the structures of the soil prokaryotic communities, with the drier and saltier soils found at higher elevations harboring less diverse communities and unique assemblages of cooccurring taxa. The higher-elevation soil communities also had lower maximum potential growth rates (as inferred from metagenome-based estimates of codon usage bias) and an overrepresentation of genes associated with trace gas metabolism. Together, these results highlight the utility of assessing community shifts across pronounced environmental gradients to improve our understanding of the microbial diversity found in Antarctic soils and the strategies used by soil microbes to persist at the limits of habitability. IMPORTANCE Antarctic soils represent an ideal system to study how environmental properties shape the taxonomic and functional diversity of microbial communities given the relatively low diversity of Antarctic soil microbial communities and the pronounced environmental gradients that occur across soils located in reasonable proximity to one another. Moreover, the challenging environmental conditions typical of most Antarctic soils present an opportunity to investigate the traits that allow soil microbes to persist in some of the most inhospitable habitats on Earth. We used cultivation-independent methods to study the bacterial and archaeal communities found in soil samples collected from across the Shackleton Glacier region of the Transantarctic Mountains. We show that those environmental characteristics associated with elevation have the greatest impact on the structure of these microbial communities, with the colder, drier, and saltier soils found at higher elevations sustaining less diverse communities that were distinct from those in more hospitable soils with respect to their composition, genomic attributes, and overall life-history strategies. Notably, the harsher conditions found in higher-elevation soils likely select for taxa with lower maximum potential growth rates and an increased reliance on trace gas metabolism to support growth. The inland soils found on the Antarctic continent represent one of the more challenging environments for microbial life on Earth. Nevertheless, Antarctic soils harbor unique bacterial and archaeal (prokaryotic) communities able to cope with extremely cold and dry conditions. These communities are not homogeneous, and the taxonomic composition and functional capabilities (genomic attributes) of these communities across environmental gradients remain largely undetermined. We analyzed the prokaryotic communities in soil samples collected from across the Shackleton Glacier region of Antarctica by coupling quantitative PCR, marker gene amplicon sequencing, and shotgun metagenomic sequencing. We found that elevation was the dominant factor explaining differences in the structures of the soil prokaryotic communities, with the drier and saltier soils found at higher elevations harboring less diverse communities and unique assemblages of cooccurring taxa. The higher-elevation soil communities also had lower maximum potential growth rates (as inferred from metagenome-based estimates of codon usage bias) and an overrepresentation of genes associated with trace gas metabolism. Together, these results highlight the utility of assessing community shifts across pronounced environmental gradients to improve our understanding of the microbial diversity found in Antarctic soils and the strategies used by soil microbes to persist at the limits of habitability. Antarctic soils represent an ideal system to study how environmental properties shape the taxonomic and functional diversity of microbial communities given the relatively low diversity of Antarctic soil microbial communities and the pronounced environmental gradients that occur across soils located in reasonable proximity to one another. Moreover, the challenging environmental conditions typical of most Antarctic soils present an opportunity to investigate the traits that allow soil microbes to persist in some of the most inhospitable habitats on Earth. We used cultivation-independent methods to study the bacterial and archaeal communities found in soil samples collected from across the Shackleton Glacier region of the Transantarctic Mountains. We show that those environmental characteristics associated with elevation have the greatest impact on the structure of these microbial communities, with the colder, drier, and saltier soils found at higher elevations sustaining less diverse communities that were distinct from those in more hospitable soils with respect to their composition, genomic attributes, and overall life-history strategies. Notably, the harsher conditions found in higher-elevation soils likely select for taxa with lower maximum potential growth rates and an increased reliance on trace gas metabolism to support growth. The inland soils found on the Antarctic continent represent one of the more challenging environments for microbial life on Earth. Nevertheless, Antarctic soils harbor unique bacterial and archaeal (prokaryotic) communities able to cope with extremely cold and dry conditions. These communities are not homogeneous, and the taxonomic composition and functional capabilities (genomic attributes) of these communities across environmental gradients remain largely undetermined. We analyzed the prokaryotic communities in soil samples collected from across the Shackleton Glacier region of Antarctica by coupling quantitative PCR, marker gene amplicon sequencing, and shotgun metagenomic sequencing. We found that elevation was the dominant factor explaining differences in the structures of the soil prokaryotic communities, with the drier and saltier soils found at higher elevations harboring less diverse communities and unique assemblages of cooccurring taxa. The higher-elevation soil communities also had lower maximum potential growth rates (as inferred from metagenome-based estimates of codon usage bias) and an overrepresentation of genes associated with trace gas metabolism. Together, these results highlight the utility of assessing community shifts across pronounced environmental gradients to improve our understanding of the microbial diversity found in Antarctic soils and the strategies used by soil microbes to persist at the limits of habitability. IMPORTANCE Antarctic soils represent an ideal system to study how environmental properties shape the taxonomic and functional diversity of microbial communities given the relatively low diversity of Antarctic soil microbial communities and the pronounced environmental gradients that occur across soils located in reasonable proximity to one another. Moreover, the challenging environmental conditions typical of most Antarctic soils present an opportunity to investigate the traits that allow soil microbes to persist in some of the most inhospitable habitats on Earth. We used cultivation-independent methods to study the bacterial and archaeal communities found in soil samples collected from across the Shackleton Glacier region of the Transantarctic Mountains. We show that those environmental characteristics associated with elevation have the greatest impact on the structure of these microbial communities, with the colder, drier, and saltier soils found at higher elevations sustaining less diverse communities that were distinct from those in more hospitable soils with respect to their composition, genomic attributes, and overall life-history strategies. Notably, the harsher conditions found in higher-elevation soils likely select for taxa with lower maximum potential growth rates and an increased reliance on trace gas metabolism to support growth.The inland soils found on the Antarctic continent represent one of the more challenging environments for microbial life on Earth. Nevertheless, Antarctic soils harbor unique bacterial and archaeal (prokaryotic) communities able to cope with extremely cold and dry conditions. These communities are not homogeneous, and the taxonomic composition and functional capabilities (genomic attributes) of these communities across environmental gradients remain largely undetermined. We analyzed the prokaryotic communities in soil samples collected from across the Shackleton Glacier region of Antarctica by coupling quantitative PCR, marker gene amplicon sequencing, and shotgun metagenomic sequencing. We found that elevation was the dominant factor explaining differences in the structures of the soil prokaryotic communities, with the drier and saltier soils found at higher elevations harboring less diverse communities and unique assemblages of cooccurring taxa. The higher-elevation soil communities also had lower maximum potential growth rates (as inferred from metagenome-based estimates of codon usage bias) and an overrepresentation of genes associated with trace gas metabolism. Together, these results highlight the utility of assessing community shifts across pronounced environmental gradients to improve our understanding of the microbial diversity found in Antarctic soils and the strategies used by soil microbes to persist at the limits of habitability. IMPORTANCE Antarctic soils represent an ideal system to study how environmental properties shape the taxonomic and functional diversity of microbial communities given the relatively low diversity of Antarctic soil microbial communities and the pronounced environmental gradients that occur across soils located in reasonable proximity to one another. Moreover, the challenging environmental conditions typical of most Antarctic soils present an opportunity to investigate the traits that allow soil microbes to persist in some of the most inhospitable habitats on Earth. We used cultivation-independent methods to study the bacterial and archaeal communities found in soil samples collected from across the Shackleton Glacier region of the Transantarctic Mountains. We show that those environmental characteristics associated with elevation have the greatest impact on the structure of these microbial communities, with the colder, drier, and saltier soils found at higher elevations sustaining less diverse communities that were distinct from those in more hospitable soils with respect to their composition, genomic attributes, and overall life-history strategies. Notably, the harsher conditions found in higher-elevation soils likely select for taxa with lower maximum potential growth rates and an increased reliance on trace gas metabolism to support growth. ABSTRACTThe inland soils found on the Antarctic continent represent one of the more challenging environments for microbial life on Earth. Nevertheless, Antarctic soils harbor unique bacterial and archaeal (prokaryotic) communities able to cope with extremely cold and dry conditions. These communities are not homogeneous, and the taxonomic composition and functional capabilities (genomic attributes) of these communities across environmental gradients remain largely undetermined. We analyzed the prokaryotic communities in soil samples collected from across the Shackleton Glacier region of Antarctica by coupling quantitative PCR, marker gene amplicon sequencing, and shotgun metagenomic sequencing. We found that elevation was the dominant factor explaining differences in the structures of the soil prokaryotic communities, with the drier and saltier soils found at higher elevations harboring less diverse communities and unique assemblages of cooccurring taxa. The higher-elevation soil communities also had lower maximum potential growth rates (as inferred from metagenome-based estimates of codon usage bias) and an overrepresentation of genes associated with trace gas metabolism. Together, these results highlight the utility of assessing community shifts across pronounced environmental gradients to improve our understanding of the microbial diversity found in Antarctic soils and the strategies used by soil microbes to persist at the limits of habitability.IMPORTANCE Antarctic soils represent an ideal system to study how environmental properties shape the taxonomic and functional diversity of microbial communities given the relatively low diversity of Antarctic soil microbial communities and the pronounced environmental gradients that occur across soils located in reasonable proximity to one another. Moreover, the challenging environmental conditions typical of most Antarctic soils present an opportunity to investigate the traits that allow soil microbes to persist in some of the most inhospitable habitats on Earth. We used cultivation-independent methods to study the bacterial and archaeal communities found in soil samples collected from across the Shackleton Glacier region of the Transantarctic Mountains. We show that those environmental characteristics associated with elevation have the greatest impact on the structure of these microbial communities, with the colder, drier, and saltier soils found at higher elevations sustaining less diverse communities that were distinct from those in more hospitable soils with respect to their composition, genomic attributes, and overall life-history strategies. Notably, the harsher conditions found in higher-elevation soils likely select for taxa with lower maximum potential growth rates and an increased reliance on trace gas metabolism to support growth. |
| Author | Lyons, W. Berry Dragone, Nicholas B. Henley, Jessica B. Adams, Byron J. Hogg, Ian D. Fierer, Noah Diaz, Melisa Wall, Diana H. Holland-Moritz, Hannah |
| Author_xml | – sequence: 1 givenname: Nicholas B. orcidid: 0000-0002-8983-6482 surname: Dragone fullname: Dragone, Nicholas B. organization: Department of Ecology and Evolutionary Biology, University of Colorado—Boulder, Boulder, Colorado, USA, Cooperative Institute for Research in Environmental Science, Boulder, Colorado, USA – sequence: 2 givenname: Jessica B. surname: Henley fullname: Henley, Jessica B. organization: Cooperative Institute for Research in Environmental Science, Boulder, Colorado, USA – sequence: 3 givenname: Hannah surname: Holland-Moritz fullname: Holland-Moritz, Hannah organization: Department of Natural Resources and the Environment, University of New Hampshire, Durham, New Hampshire, USA – sequence: 4 givenname: Melisa surname: Diaz fullname: Diaz, Melisa organization: Department of Geology and Geophysics, Woods Hole Oceanographic Institution, Falmouth, Massachusetts, USA, Department of Applied Ocean Physics and Engineering, Woods Hole Oceanographic Institution, Falmouth, Massachusetts, USA – sequence: 5 givenname: Ian D. surname: Hogg fullname: Hogg, Ian D. organization: Canadian High Arctic Research Station, Polar Knowledge Canada, Cambridge Bay, Nunavut, Canada, School of Science, University of Waikato, Hamilton, New Zealand – sequence: 6 givenname: W. Berry surname: Lyons fullname: Lyons, W. Berry organization: School of Earth Sciences, The Ohio State University, Columbus, Ohio, USA, Byrd Polar and Climate Research Center, The Ohio State University, Columbus, Ohio, USA – sequence: 7 givenname: Diana H. surname: Wall fullname: Wall, Diana H. organization: Department of Biology, Colorado State University, Fort Collins, Colorado, USA, School of Global Environmental Sustainability, Colorado State University, Fort Collins, Colorado, USA – sequence: 8 givenname: Byron J. surname: Adams fullname: Adams, Byron J. organization: Department of Biology, Evolutionary Ecology Laboratories, Brigham Young University, Provo, Utah, USA, Monte L. Bean Museum, Brigham Young University, Provo, Utah, USA – sequence: 9 givenname: Noah orcidid: 0000-0002-6432-4261 surname: Fierer fullname: Fierer, Noah organization: Department of Ecology and Evolutionary Biology, University of Colorado—Boulder, Boulder, Colorado, USA, Cooperative Institute for Research in Environmental Science, Boulder, Colorado, USA |
| BackLink | https://www.ncbi.nlm.nih.gov/pubmed/35040702$$D View this record in MEDLINE/PubMed |
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| ContentType | Journal Article |
| Copyright | Copyright © 2022 Dragone et al. Copyright © 2022 Dragone et al. This work is published under https://creativecommons.org/licenses/by/4.0/ (the “License”). Notwithstanding the ProQuest Terms and Conditions, you may use this content in accordance with the terms of the License. Copyright © 2022 Dragone et al. 2022 Dragone et al. |
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| DOI | 10.1128/msystems.01330-21 |
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| Discipline | Biology |
| EISSN | 2379-5077 |
| Editor | Mackelprang, Rachel |
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| Keywords | Antarctica soil microbiology microbial ecology soils |
| Language | English |
| License | This is an open-access article distributed under the terms of the Creative Commons Attribution 4.0 International license. https://creativecommons.org/licenses/by/4.0 This is an open-access article distributed under the terms of the Creative Commons Attribution 4.0 International license. |
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| Snippet | Antarctic soils represent an ideal system to study how environmental properties shape the taxonomic and functional diversity of microbial communities given the... The inland soils found on the Antarctic continent represent one of the more challenging environments for microbial life on Earth. Nevertheless, Antarctic soils... ABSTRACTThe inland soils found on the Antarctic continent represent one of the more challenging environments for microbial life on Earth. Nevertheless,... ABSTRACT The inland soils found on the Antarctic continent represent one of the more challenging environments for microbial life on Earth. Nevertheless,... |
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| SubjectTerms | Antarctic Regions Antarctica Archaea Bacteria Carbon Environmental conditions Environmental Microbiology Genomes Genomics Glaciers Growth rate Life history Metabolism Metagenomics Metagenomics - methods microbial ecology Microbiomes Microbiota Nitrates Research Article Soil - chemistry Soil Microbiology Soil microorganisms soils Taxonomy |
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| Title | Elevational Constraints on the Composition and Genomic Attributes of Microbial Communities in Antarctic Soils |
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