Strong Dispersal Limitation of Microbial Communities at Shackleton Glacier, Antarctica

ABSTRACT Microbial communities can be structured by both deterministic and stochastic processes, but the relative importance of these processes remains unknown. The ambiguity partly arises from an inability to disentangle soil microbial processes from confounding factors, such as aboveground plant c...

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Main Authors: Nathan P. Lemoine, Byron J. Adams, Melisa Diaz, Nicholas B. Dragone, André L. C. Franco, Noah Fierer, W. Berry Lyons, Ian D. Hogg, Diana H. Wall
Format: Article
Language:English
Published: American Society for Microbiology 2023-02-01
Series:mSystems
Subjects:
Online Access:https://journals.asm.org/doi/10.1128/msystems.01254-22
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author Nathan P. Lemoine
Byron J. Adams
Melisa Diaz
Nicholas B. Dragone
André L. C. Franco
Noah Fierer
W. Berry Lyons
Ian D. Hogg
Diana H. Wall
author_facet Nathan P. Lemoine
Byron J. Adams
Melisa Diaz
Nicholas B. Dragone
André L. C. Franco
Noah Fierer
W. Berry Lyons
Ian D. Hogg
Diana H. Wall
author_sort Nathan P. Lemoine
collection DOAJ
description ABSTRACT Microbial communities can be structured by both deterministic and stochastic processes, but the relative importance of these processes remains unknown. The ambiguity partly arises from an inability to disentangle soil microbial processes from confounding factors, such as aboveground plant communities or anthropogenic disturbance. In this study, we characterized the relative contributions of determinism and stochasticity to assembly processes of soil bacterial communities across a large environmental gradient of undisturbed Antarctic soils. We hypothesized that harsh soils would impose a strong environmental selection on microbial communities, whereas communities in benign soils would be structured largely by dispersal. Contrary to our expectations, dispersal was the dominant assembly mechanism across the entire soil environmental gradient, including benign environments. The microbial community composition reflects slowly changing soil conditions and dispersal limitation of isolated sites. Thus, stochastic processes, as opposed to deterministic, are primary drivers of soil ecosystem assembly across space at our study site. This is especially surprising given the strong environmental constraints on soil microorganisms in one of the harshest environments on the planet, suggesting that dispersal could be a driving force in microbial community assembly in soils worldwide. IMPORTANCE Because of their diversity and ubiquity, microbes provide an excellent means to tease apart how natural communities are structured. In general, ecologists believe that stochastic assembly processes, like random drift and dispersal, should dominate in benign environments while deterministic processes, like environmental filtering, should be prevalent in harsh environments. To help resolve this debate, we analyzed microbial community composition in pristine Antarctic soils devoid of human influence or plant communities for eons. Our results demonstrate that dispersal limitation is a surprisingly potent force of community limitation throughout all soil conditions. Thus, dispersal appears to be a driving force of microbial community assembly, even in the harshest of conditions.
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spelling doaj.art-35a29c04106c429abe8a37e0c90100302023-02-23T14:01:37ZengAmerican Society for MicrobiologymSystems2379-50772023-02-018110.1128/msystems.01254-22Strong Dispersal Limitation of Microbial Communities at Shackleton Glacier, AntarcticaNathan P. Lemoine0Byron J. Adams1Melisa Diaz2Nicholas B. Dragone3André L. C. Franco4Noah Fierer5W. Berry Lyons6Ian D. Hogg7Diana H. Wall8Department of Biological Sciences, Marquette University, Milwaukee, Wisconsin, USADepartment of Biology, Evolutionary Ecology Laboratories, Monte L. Bean Museum, Brigham Young University, Provo, Utah, USASchool of Earth Sciences, Byrd Polar and Climate Research Center, The Ohio State University, Columbus, Ohio, USADepartment of Ecology and Evolutionary Biology, Cooperative Institute for Research in Environmental Sciences, University of Colorado at Boulder, Boulder, Colorado, USADepartment of Biology, Colorado State University, Fort Collins, Colorado, USADepartment of Ecology and Evolutionary Biology, Cooperative Institute for Research in Environmental Sciences, University of Colorado at Boulder, Boulder, Colorado, USASchool of Earth Sciences, Byrd Polar and Climate Research Center, The Ohio State University, Columbus, Ohio, USACanadian High Arctic Research Station, Polar Knowledge Canada, Cambridge Bay, Nunavut, CanadaDepartment of Biology, Colorado State University, Fort Collins, Colorado, USAABSTRACT Microbial communities can be structured by both deterministic and stochastic processes, but the relative importance of these processes remains unknown. The ambiguity partly arises from an inability to disentangle soil microbial processes from confounding factors, such as aboveground plant communities or anthropogenic disturbance. In this study, we characterized the relative contributions of determinism and stochasticity to assembly processes of soil bacterial communities across a large environmental gradient of undisturbed Antarctic soils. We hypothesized that harsh soils would impose a strong environmental selection on microbial communities, whereas communities in benign soils would be structured largely by dispersal. Contrary to our expectations, dispersal was the dominant assembly mechanism across the entire soil environmental gradient, including benign environments. The microbial community composition reflects slowly changing soil conditions and dispersal limitation of isolated sites. Thus, stochastic processes, as opposed to deterministic, are primary drivers of soil ecosystem assembly across space at our study site. This is especially surprising given the strong environmental constraints on soil microorganisms in one of the harshest environments on the planet, suggesting that dispersal could be a driving force in microbial community assembly in soils worldwide. IMPORTANCE Because of their diversity and ubiquity, microbes provide an excellent means to tease apart how natural communities are structured. In general, ecologists believe that stochastic assembly processes, like random drift and dispersal, should dominate in benign environments while deterministic processes, like environmental filtering, should be prevalent in harsh environments. To help resolve this debate, we analyzed microbial community composition in pristine Antarctic soils devoid of human influence or plant communities for eons. Our results demonstrate that dispersal limitation is a surprisingly potent force of community limitation throughout all soil conditions. Thus, dispersal appears to be a driving force of microbial community assembly, even in the harshest of conditions.https://journals.asm.org/doi/10.1128/msystems.01254-22community assemblystochasticitydeterminismnichedispersal
spellingShingle Nathan P. Lemoine
Byron J. Adams
Melisa Diaz
Nicholas B. Dragone
André L. C. Franco
Noah Fierer
W. Berry Lyons
Ian D. Hogg
Diana H. Wall
Strong Dispersal Limitation of Microbial Communities at Shackleton Glacier, Antarctica
mSystems
community assembly
stochasticity
determinism
niche
dispersal
title Strong Dispersal Limitation of Microbial Communities at Shackleton Glacier, Antarctica
title_full Strong Dispersal Limitation of Microbial Communities at Shackleton Glacier, Antarctica
title_fullStr Strong Dispersal Limitation of Microbial Communities at Shackleton Glacier, Antarctica
title_full_unstemmed Strong Dispersal Limitation of Microbial Communities at Shackleton Glacier, Antarctica
title_short Strong Dispersal Limitation of Microbial Communities at Shackleton Glacier, Antarctica
title_sort strong dispersal limitation of microbial communities at shackleton glacier antarctica
topic community assembly
stochasticity
determinism
niche
dispersal
url https://journals.asm.org/doi/10.1128/msystems.01254-22
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