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Research Article

Fluvial network organization imprints on microbial co-occurrence networks

Stefanie Widder, Katharina Besemer, Gabriel A. Singer, View ORCID ProfileSerena Ceola, Enrico Bertuzzo, Christopher Quince, William T. Sloan, Andrea Rinaldo, and Tom J. Battin
PNAS September 2, 2014 111 (35) 12799-12804; first published August 18, 2014; https://doi.org/10.1073/pnas.1411723111
Stefanie Widder
aDivision of Computational Systems Biology, Department of Microbiology and Ecosystem Science, University of Vienna, A-1090 Vienna, Austria;
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Katharina Besemer
bDivision of Limnology, Department of Limnology and Oceanography, University of Vienna, A-1090 Vienna, Austria;
cWasserCluster Lunz GmbH, A-3293 Lunz am See, Austria;
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Gabriel A. Singer
bDivision of Limnology, Department of Limnology and Oceanography, University of Vienna, A-1090 Vienna, Austria;
dLeibniz-Institute of Freshwater Ecology and Inland Fisheries, D-12587 Berlin, Germany;
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Serena Ceola
eDipartimento di Ingegneria Civile, Chimica, Ambientale e dei Materiali, Università di Bologna, I-40136 Bologna, Italy;
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  • ORCID record for Serena Ceola
Enrico Bertuzzo
fLaboratory of Ecohydrology, School of Architecture, Ecole Polytechnique Fédérale de Lausanne, CH-1015 Lausanne, Switzerland;
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Christopher Quince
gSchool of Engineering, University of Glasgow, Glasgow G12 8QQ, United Kingdom; and
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William T. Sloan
gSchool of Engineering, University of Glasgow, Glasgow G12 8QQ, United Kingdom; and
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Andrea Rinaldo
fLaboratory of Ecohydrology, School of Architecture, Ecole Polytechnique Fédérale de Lausanne, CH-1015 Lausanne, Switzerland;
hDipartimento di Ingegneria Civile, Edile e Ambientale, Università di Padova, I-35131 Padova, Italy
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  • For correspondence: andrea.rinaldo@epfl.ch tom.battin@univie.ac.at
Tom J. Battin
bDivision of Limnology, Department of Limnology and Oceanography, University of Vienna, A-1090 Vienna, Austria;
cWasserCluster Lunz GmbH, A-3293 Lunz am See, Austria;
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  • For correspondence: andrea.rinaldo@epfl.ch tom.battin@univie.ac.at
  1. Contributed by Andrea Rinaldo, July 1, 2014 (sent for review March 10, 2014)

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Significance

Microbial communities orchestrate most biogeochemical processes on Earth. In streams and rivers, surface-attached and matrix-enclosed biofilms dominate microbial life. Despite the relevance of these biofilms for ecosystem processes (e.g., metabolism and nutrient cycling), it remains unclear how features inherent to stream and river networks affect the fundamental organization of biofilm communities in these ecosystems. We combined co-occurrence analyses of biofilms based on next-generation sequencing with a probabilistic hydrological model, and showed how fragementation of microbial co-occurrence networks change across stream networks. Our analyses offer potential insights into the response of microbial community organization and persistence to human pressures that increasingly change the hydrological regime and biodiversity dynamics in fluvial networks.

Abstract

Recent studies highlight linkages among the architecture of ecological networks, their persistence facing environmental disturbance, and the related patterns of biodiversity. A hitherto unresolved question is whether the structure of the landscape inhabited by organisms leaves an imprint on their ecological networks. We analyzed, based on pyrosequencing profiling of the biofilm communities in 114 streams, how features inherent to fluvial networks affect the co-occurrence networks that the microorganisms form in these biofilms. Our findings suggest that hydrology and metacommunity dynamics, both changing predictably across fluvial networks, affect the fragmentation of the microbial co-occurrence networks throughout the fluvial network. The loss of taxa from co-occurrence networks demonstrates that the removal of gatekeepers disproportionately contributed to network fragmentation, which has potential implications for the functions biofilms fulfill in stream ecosystems. Our findings are critical because of increased anthropogenic pressures deteriorating stream ecosystem integrity and biodiversity.

  • stream networks
  • hydrological regime

Footnotes

  • ↵1To whom correspondence may be addressed. Email: andrea.rinaldo{at}epfl.ch or tom.battin{at}univie.ac.at.
  • Author contributions: S.W., K.B., A.R., and T.J.B. designed research; S.W., K.B., G.A.S., S.C., E.B., C.Q., W.T.S., A.R., and T.J.B. performed research; S.W., G.A.S., S.C., E.B., and T.J.B. contributed new reagents/analytic tools; S.W., K.B., G.A.S., S.C., E.B., C.Q., W.T.S., and T.J.B. analyzed data; and S.W., A.R., and T.J.B. wrote the paper.

  • The authors declare no conflict of interest.

  • This article contains supporting information online at www.pnas.org/lookup/suppl/doi:10.1073/pnas.1411723111/-/DCSupplemental.

Freely available online through the PNAS open access option.

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Microbial co-occurrence in streams
Stefanie Widder, Katharina Besemer, Gabriel A. Singer, Serena Ceola, Enrico Bertuzzo, Christopher Quince, William T. Sloan, Andrea Rinaldo, Tom J. Battin
Proceedings of the National Academy of Sciences Sep 2014, 111 (35) 12799-12804; DOI: 10.1073/pnas.1411723111

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Microbial co-occurrence in streams
Stefanie Widder, Katharina Besemer, Gabriel A. Singer, Serena Ceola, Enrico Bertuzzo, Christopher Quince, William T. Sloan, Andrea Rinaldo, Tom J. Battin
Proceedings of the National Academy of Sciences Sep 2014, 111 (35) 12799-12804; DOI: 10.1073/pnas.1411723111
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