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Phylogenetic characterization of marine microbial biofilms associated with mammal bones in temperate and polar areas

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Abstract

Mammal bones sustain rich chemoautotrophic microbial communities that are consumed by a range of marine invertebrates, with bacteria playing a fundamental role making the organic matter retained in the bones available to other organisms. Our major aim here is to characterize the phylogenetic diversity of bacteria associated with Mediterranean shallow-water bones (whale, pig, and cow) examined at two different times after colonization, and compare it to bacterial communities developing on whale bones in the Southern Ocean. We sequenced 16S amplicons for approximately 50 clones from each of the 5 bone samples studied here, resulting in 215 OTUs. Our preliminary microbial community analysis resulted into two groups. Cluster 1 with cow and whale bones from the Mediterranean (3 months) and whale bones from the Southern Ocean (1 year), characterized by abundant Epsilon-proteobacteria, usually the first colonizers in anaerobic environments. Cluster 2 with Mediterranean cow (9 months) and pig bones (12 months), characterized by abundant Thiotrichales. Among the Thiotrichales, two different species of Beggiatoa spp. appeared in two different bones in the Mediterranean samples, indicating that Beggiatoa spp. can occur in the same area. Our work confirms that microbial mats associated with mammal bones in the shallow waters of the Mediterranean and the Southern Ocean are highly diverse with a predominance of Gamma- and Epsilon-proteobacteria.

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Acknowledgments

Special thanks are given to L. Laria (CEPESMA) who provided some fresh whale vertebrae, as well as R. de Stephanis, P. Gauffier, J. Giménez, E. Fernández, and the institutions EBD-CSIC, CIRCE, and Junta de Andalucía who kindly provided some fresh whale vertebrae for our experiments. We also thank the Gabriel de Castilla Spanish Antarctic Base crews of the 2011-12 and 2012-13 seasons, for their help during deployment and recovery of the experiments. We are more than grateful to our colleagues who helped during the experiment preparation, the whale bone collection, and analysis of samples: O. Moreno, J. Cristobo, M. Ballesteros, M. Correa, J. Mora, B. Figuerola, C. Angulo-Preckler, J. Moles, L. Toll, L. Núñez-Pons, M. Garriga, C. Leiva, G. Carreras, M. Romero, C. Tidu, C. Campillo-Campbell, E. Bordallo, H. Salvadó, and members of the Mola Mola Diving Center. Three anonymous reviewers greatly improved an early version of the manuscript. Collection of microbial mats in Antarctica was done under the permit CPE-EIA-2011-7 issued by the Ministry of Science and Innovation of Spain. This work is part of the AntEco (State of the Antarctic Ecosystem) scientific research programme of SCAR.

Funding

This work was developed in the frame of the Systematics Research Fund 2013 grant to MB (Linnean Society of London and the Systematics Association), ACTIQUIM-II and ACTIQUIMWHALES research grants to CA (CTM2008-03135-E/ANT, CTM2010-17415/ANT; Spanish Government), and the Obra Social La Caixa research grant (CONV09002) to the environmental association S’Agulla Educació Mediambiental (ST and AR).

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Authors and Affiliations

  1. Departamento de Biología (Zoología), Facultad de Ciencias, Universidad Autónoma de Madrid, Calle Darwin 2, Cantoblanco, 28049, Madrid, Spain

    Sergi Taboada

  2. Department of Life Sciences, The Natural History Museum of London (NHM), Cromwell Road, London, SW7 5BD, UK

    Sergi Taboada & Ana Riesgo

  3. Departamento de Ciencias de la Vida, Universidad de Alcalá, Apdo. 20, 28805, Alcalá de Henares, Spain

    Sergi Taboada & Ana Riesgo

  4. Centro Austral de Investigaciones Científicas (CADIC-CONICET), Ushuaia, Argentina

    Maria Bas

  5. Biodiversity Research Institute (IrBIO), Universitat de Barcelona, Barcelona, Catalonia, Spain

    Maria Bas & Conxita Avila

  6. Department of Evolutionary Biology, Ecology and Environmental Science, Universitat de Barcelona, Barcelona, Catalonia, Spain

    Conxita Avila

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  1. Sergi Taboada
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  2. Maria Bas
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  3. Conxita Avila
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  4. Ana Riesgo
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Correspondence to Sergi Taboada.

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All applicable international, national, and/or institutional guidelines for the care and use of animals were followed by the authors.

Sampling and field studies

All necessary permits for sampling and observational field studies have been obtained by the authors from the competent authorities and are mentioned in the acknowledgements.

Data availability

Genetic sequence data generated in this study were deposited in GenBank with Accession Numbers MN566614–MN566757. All other data generated or analyzed during this study are included in this published article and its supplementary information files.

Author contribution

ST and MB conceived and designed research. ST and MB conducted experiments. AR and CA contributed with reagents and analytical tools. ST, MB and AR analyzed data and wrote the manuscript. All authors read and approved the manuscript.

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Communicated by A. J. Gooday

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Taboada, S., Bas, M., Avila, C. et al. Phylogenetic characterization of marine microbial biofilms associated with mammal bones in temperate and polar areas. Mar. Biodivers. 50, 60 (2020). https://doi.org/10.1007/s12526-020-01082-8

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