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Microbial Ecology

, Volume 77, Issue 1, pp 25–36 | Cite as

Stable and Enriched Cenarchaeum symbiosum and Uncultured Betaproteobacteria HF1 in the Microbiome of the Mediterranean Sponge Haliclona fulva (Demospongiae: Haplosclerida)

  • Erika García-Bonilla
  • Pedro F. B. Brandão
  • Thierry Pérez
  • Howard JuncaEmail author
Environmental Microbiology

Abstract

Sponges harbor characteristic microbiomes derived from symbiotic relationships shaping their lifestyle and survival. Haliclona fulva is encrusting marine sponge species dwelling in coralligenous accretions or semidark caves of the Mediterranean Sea and the near Atlantic Ocean. In this work, we characterized the abundance and core microbial community composition found in specimens of H. fulva by means of electron microscopy and 16S amplicon Illumina sequencing. We provide evidence of its low microbial abundance (LMA) nature. We found that the H. fulva core microbiome is dominated by sequences belonging to the orders Nitrosomonadales and Cenarchaeales. Seventy percent of the reads assigned to these phylotypes grouped in a very small number of high-frequency operational taxonomic units, representing niche-specific species Cenarchaeum symbiosum and uncultured Betaproteobacteria HF1, a new eubacterial ribotype variant found in H. fulva. The microbial composition of H. fulva is quite distinct from those reported in sponge species of the same Haliclona genus. We also detected evidence of an excretion/capturing loop between these abundant microorganisms and planktonic microbes by analyzing shifts in seawater planktonic microbial content exposed to healthy sponge specimens maintained in aquaria. Our results suggest that horizontal transmission is very likely the main mechanism for symbionts’ acquisition by H. fulva. So far, this is the first shallow water sponge species harboring such a specific and predominant assemblage composed of these eubacterial and archaeal ribotypes. Our data suggests that this symbiotic relationship is very stable over time, indicating that the identified core microbial symbionts may play key roles in the holobiont functioning.

Keywords

Microbiome Cenarchaeales Nitrosomonadales Haliclona fulva LMA sponge Aquaria 

Notes

Acknowledgements

We would like to thank EcosNord-Colciencias research cooperation and mobility exchange program throughout the project (2012–2014 and 2015–2017), as well as Dr. Regis Guillaume and the French Embassy in Colombia. Erika García-Bonilla would like to acknowledge financial support given by Colciencias-Colfuturo, Doctoral Grant (Convocatoria 528-2011). We also would like to thank Prof. Olivier P. Thomas (National University of Ireland Galway) for his help in sponge collection and for his comments on the manuscript, as well as Prof. Andrés Pinzón (Universidad Nacional de Colombia) and Marcela Villegas-Plazas (Microbiomas Foundation) for providing bioinformatic and analytical resources and support. We also thank two anonymous reviewers for comments, corrections, and suggestions, which greatly improved the manuscript.

Supplementary material

248_2018_1201_MOESM1_ESM.docx (4.4 mb)
ESM 1 (DOCX 4514 kb)

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© Springer Science+Business Media, LLC, part of Springer Nature 2018

Authors and Affiliations

  1. 1.RG Microbial Ecology: Metabolism, Genomics & Evolution, Div Ecogenomics & HolobiontsMicrobiomas FoundationChíaColombia
  2. 2.Laboratorio de Microbiología Ambiental y Aplicada, Departamento de Química, Facultad de CienciasUniversidad Nacional de ColombiaBogotáColombia
  3. 3.Station Marine d’Endoume SME - IMBEInstitut Méditerranéen de Biodiversité et d’Ecologie Marine et ContinentaleMarseilleFrance

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