Abstract

We studied the long-term temporal dynamics of the aerobic anoxygenic phototrophic (AAP) bacteria, a relevant functional group in the coastal marine microbial food web, using high-throughput sequencing of the pufM gene coupled with multivariate, time series and co-occurrence analyses at the Blanes Bay Microbial Observatory (NW Mediterranean). Additionally, using metagenomics, we tested whether the used primers captured accurately the seasonality of the most relevant AAP groups. Phylogroup K (Gammaproteobacteria) was the greatest contributor to community structure over all seasons, with phylogroups E and G (Alphaproteobacteria) being prevalent in spring. Diversity indices showed a clear seasonal trend, with maximum values in winter, which was inverse to that of AAP abundance. Multivariate analyses revealed sample clustering by season, with a relevant proportion of the variance explained by day length, temperature, salinity, phototrophic nanoflagellate abundance, chlorophyll a, and silicate concentration. Time series analysis showed robust rhythmic patterns of co-occurrence, but distinct seasonal behaviors within the same phylogroup, and even within different amplicon sequence variants (ASVs) conforming the same operational taxonomic unit (OTU). Altogether, our results picture the AAP assemblage as highly seasonal and recurrent but containing ecotypes showing distinctive temporal niche partitioning, rather than being a cohesive functional group.

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Acknowledgements

We thank the people involved in maintaining the BBMO and those taking care of sampling, particularly Clara Cardelús and Vanessa Balagué. We would also like to thank Ramon Massana and Irene Forn for providing microscopy counts. We thank the Marbits bioinformatics platform at ICM-CSIC, particularly Ramiro Logares and Célio Dias for providing the metagenomic data and Anders Kristian Krabberød (University of Oslo) for help with network analyses. Access to the MareNostrum Supercomputer was granted to Ramiro Logares under agreement BCV-2017-3-0001. qPCR analyses was done at the Institute of Evolutionary Biology (Barcelona) thanks to José Luís Maestro. This research was funded by grant REMEI (CTM2015-70340-R) from the Spanish Ministry of Economy, Industry and Competitiveness and Grant 2017SGR/1568 from CIRIT-Generalitat de Catalunya to Consolidated Research Groups.

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Affiliations

  1. Department of Marine Biology and Oceanography, Institut de Ciències del Mar (ICM-CSIC), Pg Marítim de la Barceloneta, 37-49, Barcelona, Catalunya, Spain

    • Adrià Auladell
    • , Pablo Sánchez
    • , Josep M. Gasol
    •  & Isabel Ferrera
  2. Department of Genetics and Microbiology, Universitat Autònoma de Barcelona (UAB), Bellaterra, Catalunya, Spain

    • Olga Sánchez
  3. Centre for Marine Ecosystems Research, School of Science, Edith Cowan University, Joondalup, WA, Australia

    • Josep M. Gasol
  4. Centro Oceanográfico de Málaga, Instituto Español de Oceanografía, Fuengirola, Málaga, Spain

    • Isabel Ferrera

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Contributions

IF and JMG conceived the study; IF and OS designed and performed laboratory analyses; AA, PS, OS, and IF analyzed the data; AA and IF wrote the paper and all authors commented and revised it.

Conflict of interest

The authors declare that they have no conflict of interest.

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Correspondence to Adrià Auladell or Isabel Ferrera.

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https://doi.org/10.1038/s41396-019-0401-4