Published September 15, 2020 | Version v1
Journal article Open

On the way to specificity - Microbiome reflects sponge genetic cluster primarily in highly structured populations

  • 1. Department of Life Sciences, The Natural History Museum, London, UK
  • 2. Departamento de Ciencias de la Vida, EU- US Marine Biodiversity Group, Universidad de Alcalá, Alcalá de Henares, Spain & Departamento de Biología (Zoología), Universidad Autónoma de Madrid, Facultad de Ciencias, Madrid, Spain
  • 3. Department of Life Sciences, The Natural History Museum, London, UK & Department of Genetics, Microbiology and Statistics, Faculty of Biology, University of Barcelona, Barcelona, Spain
  • 4. Helmholtz Centre for Ocean Research Kiel, Research Unit Marine Symbioses, Kiel, Germany
  • 5. Department of Life Sciences, The Natural History Museum, London, UK & Department of Biodiversity and Evolutionary Biology, Museo Nacional de Ciencias Naturales de Madrid (CSIC), Madrid, Spain

Description

ABSTRACT

Most animals, including sponges (Porifera), have species‐specific microbiomes. Which genetic or environmental factors play major roles structuring the microbial community at the intraspecific level in sponges is, however, largely unknown. In this study, we tested whether geographic location or genetic structure of conspecific sponges influences their microbial assembly. For that, we used three sponge species with different rates of gene flow, and collected samples along their entire distribution range (two from the Mediterranean and one from the Southern Ocean) yielding a total of 393 samples. These three sponge species have been previously analysed by microsatellites or single nucleotide polymorphisms, and here we investigate their microbiomes by amplicon sequencing of the microbial 16S rRNA gene. The sponge Petrosia ficiformis, with highly isolated populations (low gene flow), showed a stronger influence of the host genetic distance on the microbial composition than the spatial distance. Host‐specificity was therefore detected at the genotypic level, with individuals belonging to the same host genetic cluster harbouring more similar microbiomes than distant ones. On the contrary, the microbiome of Ircinia fasciculata and Dendrilla antarctica ‐ both with weak population structure (high gene flow) ‐ seemed influenced by location rather than by host genetic distance. Our results suggest that in sponge species with high population structure, the host genetic cluster influence the microbial community more than the geographic location.

Notes

ACKNOWLEDGEMENTS This project has received funding from the European Union's Horizon 2020 Research and Innovation Programme under the Marie Skłodowska‐Curie Individual Fellowships Grant Agreement No. 796011 ('DeepSym'), and Grant Agreement No. 679849 ('SponGES'). We thank the team around Andre Franke at the Institute of Clinical Molecular Biology, Kiel, for sequencing support. We also want to thank Shaun Nielsen for support and guidance through data analysis. Finally, we want to acknowledge the anonymous reviewers for thoughtful comments that helped to improve this manuscript. AUTHOR CONTRIBUTIONS C.D.V., and A.R. conceived the study. A.R, S.T, and C.L. performed the fieldwork. C.D.V., K.B., and C.L. performed the laboratory work, and C.D.V. analysed the data. C.D.V., and A.R. drafted the first versions of the manuscript. All authors commented on and approved of later versions of the paper. DATA AVAILABILITY STATEMENT The raw sequences were deposited at the Sequence Read Archive (SRA) of the NCBI as BioProject with accession ID PRJNA593003. Population genetic data for Petrosia ficiformis is available thought https://doi.org/10.1594/PANGAEA.882098 (see Riesgo et al., 2019), for Ircinia fasciculata through https://doi.pangaea.de/10.1594/PANGAEA.860018 (see Riesgo et al., 2016), and SNPs data for each individual sample of Dendrilla antarctica is deposited in the NCBI SRA database, BioProject PRJNA531366, Biosamples SAMN11350306–SAMN11350367 (see Leiva et al., 2019).

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Additional details

Funding

SponGES – Deep-sea Sponge Grounds Ecosystems of the North Atlantic: an integrated approach towards their preservation and sustainable exploitation 679849
European Commission
DeepSym – Understanding the drivers of the genetic and functional structure of deep-sea sponge symbiont communities 796011
European Commission