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Microbiome functioning depends on individual and interactive effects of the environment and community structure

The ISME Journalvolume 13pages111 (2019) | Download Citation

Abstract

How ecosystem functioning changes with microbial communities remains an open question in natural ecosystems. Both present-day environmental conditions and historical events, such as past differences in dispersal, can have a greater influence over ecosystem function than the diversity or abundance of both taxa and genes. Here, we estimated how individual and interactive effects of microbial community structure defined by diversity and abundance, present-day environmental conditions, and an indicator of historical legacies influenced ecosystem functioning in lake sediments. We studied sediments because they have strong gradients in all three of these ecosystem properties and deliver important functions worldwide. By characterizing bacterial community composition and functional traits at eight sites fed by discrete and contrasting catchments, we found that taxonomic diversity and the normalized abundance of oxidase-encoding genes explained as much variation in CO2 production as present-day gradients of pH and organic matter quantity and quality. Functional gene diversity was not linked to CO2 production rates. Surprisingly, the effects of taxonomic diversity and normalized oxidase abundance in the model predicting CO2 production were attributable to site-level differences in bacterial communities unrelated to the present-day environment, suggesting that colonization history rather than habitat-based filtering indirectly influenced ecosystem functioning. Our findings add to limited evidence that biodiversity and gene abundance explain patterns of microbiome functioning in nature. Yet we highlight among the first time how these relationships depend directly on present-day environmental conditions and indirectly on historical legacies, and so need to be contextualized with these other ecosystem properties.

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Acknowledgements

We thank J. Wolstenholme for fieldwork, D. Baulcombe and I. Henderson for offering lab space, G. Jones and M. Meyer for assisting with sample processing, S. Dickens and P. Marriot for help with sequencing, and three anonymous reviewers for comments that improved an earlier draft. Support for this work came from NERC Standard Grant NE/L006561/1 and Gatsby Fellowship GAT2962 to A.J.T.

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Affiliations

  1. Ecosystems and Global Change Group, Department of Plant Sciences, University of Cambridge, Downing Street, CB2 3EA, Cambridge, UK

    • Chloé Orland
    • , Erik J. S. Emilson
    •  & Andrew J. Tanentzap
  2. Natural Resources Canada, Great Lakes Forestry Centre, 1219 Queen St. E., Sault. Ste. Marie, ON, P6A 2E5, Canada

    • Erik J. S. Emilson
  3. Vale Living with Lakes Centre, Laurentian University, 935 Ramsey Lake Road, Sudbury, ON, Canada, P3E 2C6

    • Nathan Basiliko
    • , Nadia C. S. Mykytczuk
    •  & John M. Gunn

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The authors declare that they have no conflict of interest.

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Correspondence to Chloé Orland.

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DOI

https://doi.org/10.1038/s41396-018-0230-x