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Biogeochemical insights into microbe–mineral–fluid interactions in hydrothermal chimneys using enrichment culture

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Abstract

Active hydrothermal chimneys host diverse microbial communities exhibiting various metabolisms including those involved in various biogeochemical cycles. To investigate microbe–mineral–fluid interactions in hydrothermal chimney and the driver of microbial diversity, a cultural approach using a gas-lift bioreactor was chosen. An enrichment culture was performed using crushed active chimney sample as inoculum and diluted hydrothermal fluid from the same vent as culture medium. Daily sampling provided time-series access to active microbial diversity and medium composition. Active archaeal and bacterial communities consisted mainly of sulfur, sulfate and iron reducers and hydrogen oxidizers with the detection of Thermococcus, Archaeoglobus, Geoglobus, Sulfurimonas and Thermotoga sequences. The simultaneous presence of active Geoglobus sp. and Archaeoglobus sp. argues against competition for available carbon sources and electron donors between sulfate and iron reducers at high temperature. This approach allowed the cultivation of microbial populations that were under-represented in the initial environmental sample. The microbial communities are heterogeneously distributed within the gas-lift bioreactor; it is unlikely that bulk mineralogy or fluid chemistry is the drivers of microbial community structure. Instead, we propose that micro-environmental niche characteristics, created by the interaction between the mineral grains and the fluid chemistry, are the main drivers of microbial diversity in natural systems.

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Acknowledgments

We want to thank all the shipboard cruise party for their work and support during the BIG cruise: officers, crew and technicians of the R/V L’Atalante, the DSV Nautile team and the on-board scientific team. This cruise was funded by IFREMER (France) and has benefited from a work permit in Mexican waters (DAPA/2/281009/3803, October 28th, 2009). We also acknowledge the anonymous reviewers for their constructive suggestions and comments. We are grateful to Carole Decker and Jean-Claude Caprais for their assistance with hydrogen sulfide measurement. Yoan Germain is thanked for clean laboratory assistance and Karine Estève for her help during the cruise. We also thank Pierre-Marie Sarradin for provide us the PEPITO’s temperature data. This work was supported by Ifremer, the GIS Europôle Mer, UEB, CNRS, and has benefited from state aid managed by the Agence Nationale de la Recherche under the program “Investments for the Future” with the reference ANR-10-LabX-19-01.

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  1. Nolwenn Callac

    Present address: Department of Geological Sciences, Stockholm University, Svante Arrhenius väg 8, SE-106 91, Stockholm, Sweden

Authors and Affiliations

  1. Laboratoire de Microbiologie des Environnements Extrêmes, Université de Bretagne Occidentale, UEB, IUEM, UMR 6197, Place Nicolas Copernic, 29280, Plouzané, France

    Nolwenn Callac, Françoise Lesongeur, Patricia Pignet & Anne Godfroy

  2. Laboratoire de Microbiologie des Environnements Extrêmes, Ifremer, UMR6197, 29280, Plouzané, France

    Nolwenn Callac, Françoise Lesongeur, Patricia Pignet & Anne Godfroy

  3. Laboratoire de Microbiologie des Environnements Extrêmes, CNRS, UMR 6197, 29280, Plouzané, France

    Nolwenn Callac, Françoise Lesongeur, Patricia Pignet & Anne Godfroy

  4. Université de Bretagne Occidentale, Domaines Océaniques IUEM, UMR6538, Place Nicolas Copernic, 29280, Plouzané, France

    Nolwenn Callac & Céline Liorzou

  5. Ifremer, Centre de Brest, 29280, Plouzané, France

    Olivier Rouxel, Sandrine Chéron & Yves Fouquet

  6. Université de Bretagne Occidentale, IUEM, UMS3113, Place Nicolas Copernic, 29280, Plouzané, France

    Claire Bollinger

  7. Laboratoire Géobiosphère Actuelle et Primitive, IPGP, UMR7154, 75238, Paris, France

    Céline Rommevaux-Jestin

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  1. Nolwenn Callac
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Correspondence to Nolwenn Callac.

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Communicated by H. Atomi.

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Callac, N., Rouxel, O., Lesongeur, F. et al. Biogeochemical insights into microbe–mineral–fluid interactions in hydrothermal chimneys using enrichment culture. Extremophiles 19, 597–617 (2015). https://doi.org/10.1007/s00792-015-0742-5

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