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Top-Down Control of Diesel-Degrading Prokaryotic Communities

  • Environmental Microbiology
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Abstract

Biostimulation through the addition of inorganic nutrients has been the most widely practiced bioremediation strategy in oil-polluted marine waters. However, little attention has so far been paid to the microbial food web and the impact of top-down control that directly or indirectly influences the success of the bioremediation. We designed a mesocosm experiment using pre-filtered (<50 μm) surface seawater from the Bay of Banyuls-sur-Mer (North-Western Mediterranean Sea) and examined the top-down effect exerted by heterotrophic nanoflagellates (HNF) and virus-like particles (VLP) on prokaryotic abundance, activity and diversity in the presence or absence of diesel fuel. Prokaryotes, HNF and VLP abundances showed a predator–prey succession, with a co-development of HNF and VLP. In the polluted system, we observed a stronger impact of viral lysis on prokaryotic abundances than in the control. Analysis of the diversity revealed that a bloom of Vibrio sp. occurred in the polluted mesocosm. That bloom was rapidly followed by a less abundant and more even community of predation-resistant bacteria, including known hydrocarbon degraders such as Oleispira spp. and Methylophaga spp. and opportunistic bacteria such as Percisivirga spp., Roseobacter spp. and Phaeobacter spp. The shift in prokaryotic dominance in response to viral lysis provided clear evidence of the ‘killing the winner’ model. Nevertheless, despite clear effects on prokaryotic abundance, activity and diversity, the diesel degradation was not impacted by top-down control. The present study investigates for the first time the functioning of a complex microbial network (including VLP) using a nutrient-based biostimulation strategy and highlights some key processes useful for tailoring bioremediation.

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Acknowledgments

This study was part of the IBISCUS project, funded by the Continental and Coastal Ecosphere (EC2CO) program from the Centre National de la Recherche Scientifique (CNRS) and Institut des Sciences de l’Univers (INSU). We would like to thank C. Aria-Casters and M.P.A. Guigui for their contributions to the manuscript.

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Authors and Affiliations

  1. UPMC Univ Paris 06, UMR 7621, Laboratoire d’Océanographie Microbienne, Observatoire Océanologique, Sorbonne Universités, 66650, Banyuls-sur-mer, France

    Caroline Sauret, Pascal Conan, Mireille Pujo-Pay & Jean-François Ghiglione

  2. Laboratoire d’Océanographie Microbienne, UMR 7621, Observatoire Océanologique, CNRS, Avenue Fontaulé, Banyuls-sur-Mer, 66650, France

    Caroline Sauret, Pascal Conan, Mireille Pujo-Pay & Jean-François Ghiglione

  3. Department of Oceanography and Center for Microbial Oceanography: Research and Education, University of Hawaii at Mãnoa, Honolulu, HI, 96822, USA

    Daniela Böttjer

  4. Campus de Luminy, Centre d’Océanologie de Marseille, Marseille Cedex 9, 13 288, France

    Agathe Talarmin & Catherine Guigue

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  1. Caroline Sauret
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  2. Daniela Böttjer
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  3. Agathe Talarmin
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  4. Catherine Guigue
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  5. Pascal Conan
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  6. Mireille Pujo-Pay
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  7. Jean-François Ghiglione
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Correspondence to Jean-François Ghiglione.

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Sauret, C., Böttjer, D., Talarmin, A. et al. Top-Down Control of Diesel-Degrading Prokaryotic Communities. Microb Ecol 70, 445–458 (2015). https://doi.org/10.1007/s00248-015-0596-5

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