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Urbanization Constrains Skin Bacterial Phylogenetic Diversity in Wild Fish Populations and Correlates with the Proliferation of Aeromonads

  • Host Microbe Interactions
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Abstract

Changes in the state of rivers resulting from the activity and expansion of urban areas are likely to affect aquatic populations by increasing stress and disease, with the microbiota playing a potentially important intermediary role. Unraveling the dynamics of microbial flora is therefore essential to better apprehend the impact of anthropogenic disturbances on the health of host populations and the ecological integrity of hydrosystems. In this context, the present study simultaneously examined changes in the microbial communities associated with mucosal skin and gut tissues of eight fish species along an urbanization gradient in the Orge River (France). 16S rRNA gene metabarcoding revealed that the structure and composition of the skin microbiota varied substantially along the disturbance gradient and to a lesser extent according to fish taxonomy. Sequences affiliated with the Gammaproteobacteria, in particular the genus Aeromonas, prevailed on fish caught in the most urbanized areas, whereas they were nearly absent upstream. This rise of opportunistic taxa was concomitant with a decline in phylogenetic diversity, suggesting more constraining environmental pressures. In comparison, fish gut microbiota varied much more moderately with the degree of urbanization, possibly because this niche might be less directly exposed to environmental stressors. Co-occurrence networks further identified pairs of associated bacterial taxa, co-existing more or less often than expected at random. Few correlations could be identified between skin and gut bacterial taxa, supporting the assumption that these two microbial niches are disconnected and do not suffer from the same vulnerability to anthropic pressures.

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Data Availability

Raw sequencing data was deposited as FASTQ files in the European Nucleotide Archive (http://www.ebi.ac.uk/ena) under the primary accession number PRJEB38775.

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Acknowledgments

The authors are grateful to B. Janvier for technical and laboratory assistance with the experiments.

Funding

This study was supported by funds from the PIREN-Seine research program and an internal call for proposals (UMR METIS).

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Authors and Affiliations

  1. Normandie Université, UNIROUEN, UNICAEN, UMR CNRS 6143 M2C, Rouen, France

    Yannick Colin, Thierry Berthe, Anne-Laure Vivant & Fabienne Petit

  2. Sorbonne Université, CNRS, EPHE, PSL, UMR METIS, Paris, F-75005, France

    Thierry Berthe, Noëlie Molbert, Elodie Guigon, Fabrice Alliot, Sylvie Collin, Aurélie Goutte & Fabienne Petit

  3. EPHE, PSL Research University, Sorbonne Université, CNRS, UMR METIS, Paris, F-75005, France

    Elodie Guigon, Fabrice Alliot & Aurélie Goutte

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The work presented here was carried out in collaboration with all authors. FP and AG defined the research theme. AG, FP, TB, EG, and FA defined sampling strategy and designed methods and experiments. FP, TB, NM, EG, and FA carried out the sampling processing and DNA extraction. Bioinformatic analyses and phylogenetic reconstruction were carried out by YC. Data have been analyzed and interpreted by all authors. YC wrote the article. All authors have contributed to, read, and approved the final manuscript.

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Correspondence to Yannick Colin.

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All applicable international, national, and/or institutional guidelines for the care and use of animals were followed. All procedures performed in studies involving animals were in accordance with the ethical standards of the institution or practice at which the studies were conducted.

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Colin, Y., Berthe, T., Molbert, N. et al. Urbanization Constrains Skin Bacterial Phylogenetic Diversity in Wild Fish Populations and Correlates with the Proliferation of Aeromonads. Microb Ecol 82, 523–536 (2021). https://doi.org/10.1007/s00248-020-01650-2

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