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Airborne microbial transport limitation to isolated Antarctic soil habitats

Nature Microbiology volume 4, pages 925–932 (2019)Cite this article

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Abstract

Dispersal is a critical yet poorly understood factor underlying macroecological patterns in microbial communities1. Airborne microbial transport is assumed to occupy a central role in determining dispersal outcomes2,3, and extra-range dispersal has important implications for predicting ecosystem resilience and response to environmental change4. One of the most pertinent biomes in this regard is Antarctica, given its geographic isolation and vulnerability to climate change and human disturbance5. Here, we report microbial diversity in near-ground and high-altitude air above the largest ice-free Antarctic habitat, as well as that of underlying soil microbial communities. We found that persistent local airborne inputs were unable to fully explain Antarctic soil community assembly. Comparison with airborne microbial diversity from high-altitude and non-polar sources suggests that strong selection occurs during long-range atmospheric transport. The influence of selection during airborne transit and at sink locations varied between microbial phyla. Overall, the communities from this isolated Antarctic ecosystem displayed limited connectivity to the non-polar microbial pool, and alternative sources of recruitment are necessary to fully explain extant soil diversity. Our findings provide critical insights into the role of airborne transport limitation in determining microbial biogeographic patterns.

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Fig. 1: Antarctic air and soil habitats support distinct bacterial and fungal communities.
Fig. 2: Comparison of bacterial and fungal diversity from Antarctic and non-polar sources.
Fig. 3: Phylogenetic structuring of local and global pools for bacterial and fungal diversity.

Data availability

The data that support the findings of this study are available from the corresponding author upon request. All sequence data generated by this study have been submitted to the EMBL European Nucleotide Archive under BioProject PRJEB27416 with accession numbers ERS2573837 to ERS2573946.

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Acknowledgements

Field and logistical support was provided by Antarctica New Zealand. The research was funded by a grant from the New Zealand Ministry of Business, Innovation and Employment (UOWX1401) and Yale-NUS College Start-Up Fund. F.T.M. is supported by the European Research Council (BIODESERT project; ERC grant agreement number 647038).

Author information

Authors and Affiliations

  1. Yale-NUS College, National University of Singapore, Singapore, Singapore

    Stephen D. J. Archer & Stephen B. Pointing

  2. Institute for Applied Ecology New Zealand, Auckland University of Technology, Auckland, New Zealand

    Stephen D. J. Archer & Kevin C. Lee

  3. Institute for Global Food Security, School of Biological Sciences, Queen’s University Belfast, Belfast, UK

    Tancredi Caruso

  4. Department of Chemical Engineering, Kanazawa University, Kanazawa, Japan

    Teruya Maki

  5. International Centre for Terrestrial Antarctic Research, University of Waikato, Hamilton, New Zealand

    Charles K. Lee & S. Craig Cary

  6. Centre for Microbial Ecology and Genomics, University of Pretoria, Pretoria, South Africa

    Don A. Cowan

  7. Departamento de Biología y Geología, Física y Química Inorgánica, Escuela Superior de Ciencias Experimentales y Tecnología, Universidad Rey Juan Carlos, Móstoles, Spain

    Fernando T. Maestre

  8. Department of Biological Sciences, National University of Singapore, Singapore, Singapore

    Stephen B. Pointing

  9. Institute of Nature and Environmental Technology, Kanazawa University, Kanazawa, Japan

    Stephen B. Pointing

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Contributions

S.D.J.A. and S.B.P. conceived the study. C.K.L., S.C.C. and S.B.P. secured the research funding. S.D.J.A. and C.K.L. conducted the fieldwork. S.C.C. was the field event leader. T.M. developed and validated the helicopter sampling method. S.D.J.A. performed the laboratory experiments. S.D.J.A., K.C.L., T.C. and S.B.P. performed the data analysis and interpretation. D.A.C., F.T.M. and S.B.P. critically assessed and interpreted the findings. S.B.P. wrote the manuscript.

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Correspondence to Stephen B. Pointing.

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Supplementary Information

Supplementary Information

Supplementary Figure 1, legends for Supplementary Figures 2–4, Supplementary Figure 5, Supplementary legends for Figures 6–8, Supplementary Figure 9 and legends for Supplementary Datasets 1–6.

Reporting Summary

Supplementary Dataset 1

Taxonomic identity of bacteria by phylum in each air and soil sample. This raw data file accompanies Supplementary Figure 2.

Supplementary Dataset 2

Taxonomic identity of bacteria by class in each air and soil sample. This raw data file accompanies Supplementary Figure 3.

Supplementary Dataset 3

Taxonomic identity of bacteria by genus in each air and soil sample. This raw data file accompanies Supplementary Figure 4.

Supplementary Dataset 4

Taxonomic identity of fungi by phylum in each air and soil sample. This raw data file accompanies Supplementary Figure 6.

Supplementary Dataset 5

Taxonomic identity of fungi by class in each air and soil sample. This raw data file accompanies Supplementary Figure 7.

Supplementary Dataset 6

Taxonomic identity of fungi by genus in each air and soil sample. This raw data file accompanies Supplementary Figure 8.

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Archer, S.D.J., Lee, K.C., Caruso, T. et al. Airborne microbial transport limitation to isolated Antarctic soil habitats. Nat Microbiol 4, 925–932 (2019). https://doi.org/10.1038/s41564-019-0370-4

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