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Metabolic flexibility allows generalist bacteria to become dominant in a frequently disturbed ecosystem

Ya-Jou Chen, Pok Man Leung, Sean K. Bay, Philip Hugenholtz, Adam J. Kessler, Guy Shelley, David W. Waite, Perran L. M. Cook, Chris Greening
doi: https://doi.org/10.1101/2020.02.12.945220
Ya-Jou Chen
1School of Biological Sciences, Monash University, Clayton, VIC 3800, Australia
2Department of Microbiology, Biomedicine Discovery Institute, Clayton, VIC 3800, Australia
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Pok Man Leung
1School of Biological Sciences, Monash University, Clayton, VIC 3800, Australia
2Department of Microbiology, Biomedicine Discovery Institute, Clayton, VIC 3800, Australia
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Sean K. Bay
1School of Biological Sciences, Monash University, Clayton, VIC 3800, Australia
2Department of Microbiology, Biomedicine Discovery Institute, Clayton, VIC 3800, Australia
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Philip Hugenholtz
3Australian Centre for Ecogenomics, School of Chemistry and Molecular Biosciences, The University of Queensland, St Lucia, QLD 4072, Australia
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Adam J. Kessler
4Water Studies Centre, School of Chemistry, Monash University, Clayton, VIC 3800, Australia
5School of Earth, Atmosphere and Environment, Monash University, Clayton, VIC 3800, Australia
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Guy Shelley
1School of Biological Sciences, Monash University, Clayton, VIC 3800, Australia
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David W. Waite
3Australian Centre for Ecogenomics, School of Chemistry and Molecular Biosciences, The University of Queensland, St Lucia, QLD 4072, Australia
6School of Biological Sciences, University of Auckland, Auckland 1010, New Zealand
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Perran L. M. Cook
4Water Studies Centre, School of Chemistry, Monash University, Clayton, VIC 3800, Australia
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  • For correspondence: chris.greening@monash.edu perran.cook@monash.edu
Chris Greening
1School of Biological Sciences, Monash University, Clayton, VIC 3800, Australia
2Department of Microbiology, Biomedicine Discovery Institute, Clayton, VIC 3800, Australia
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  • For correspondence: chris.greening@monash.edu perran.cook@monash.edu
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Abstract

Ecological theory suggests that habitat disturbance differentially influences distributions of generalist and specialist species. While well-established for macroorganisms, this theory has rarely been explored for microorganisms. Here we tested these principles in permeable (sandy) sediments, ecosystems with much spatiotemporal variation in resource availability and other conditions. Microbial community composition and function was profiled in intertidal and subtidal sediments using 16S amplicon sequencing and metagenomics, yielding 135 metagenome-assembled genomes. Microbial abundance and composition significantly differed with sediment depth and, to a lesser extent, sampling date. Several generalist taxa were highly abundant and prevalent in all samples, including within orders Woeseiales and Flavobacteriales; genome reconstructions indicate these facultatively anaerobic taxa are highly metabolically flexible and adapt to fluctuations in resource availability by using different electron donors and acceptors. In contrast, obligately anaerobic taxa such as sulfate reducers (Desulfobacterales, Desulfobulbales) and proposed candidate phylum MBNT15 were less abundant overall and only thrived in more stable deeper sediments. We substantiated these findings by measuring three metabolic processes in these sediments; whereas the generalist-associated processes of sulfide oxidation and hydrogenogenic fermentation occurred rapidly at all depths, the specialist-associated process of sulfate reduction was restricted to deeper sediments. In addition, a manipulative experiment confirmed generalists outcompete specialist taxa during simulated habitat disturbance. Altogether, these findings suggest that metabolically flexible taxa become dominant in these highly dynamic environments, whereas metabolic specialism restricts bacteria to narrower niches. Thus, an ecological theory describing distribution patterns for macroorganisms likely extends to microorganisms. Such findings have broad ecological and biogeochemical ramifications.

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Posted February 13, 2020.
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Metabolic flexibility allows generalist bacteria to become dominant in a frequently disturbed ecosystem
Ya-Jou Chen, Pok Man Leung, Sean K. Bay, Philip Hugenholtz, Adam J. Kessler, Guy Shelley, David W. Waite, Perran L. M. Cook, Chris Greening
bioRxiv 2020.02.12.945220; doi: https://doi.org/10.1101/2020.02.12.945220
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Metabolic flexibility allows generalist bacteria to become dominant in a frequently disturbed ecosystem
Ya-Jou Chen, Pok Man Leung, Sean K. Bay, Philip Hugenholtz, Adam J. Kessler, Guy Shelley, David W. Waite, Perran L. M. Cook, Chris Greening
bioRxiv 2020.02.12.945220; doi: https://doi.org/10.1101/2020.02.12.945220

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