Marine Biology

, 165:14 | Cite as

Symbiont-dependent sexual reproduction in marine colonial invertebrate: morphological and molecular evidence

  • Meril Mathew
  • Thomas Schwaha
  • Andrew N. Ostrovsky
  • Nicole B. Lopanik
Original paper

Abstract

The benefits of mutualistic associations between prokaryotes and their eukaryotic hosts lead to the evolution of adaptations that encourage the relationship in subsequent generations of the host. Symbiont-dependent host reproduction may play a key role in the maintenance of the association and persistence of the microbial symbiont in the host population. Recently, sexual reproduction in the marine bryozoan, Bugula neritina, was reported to be influenced by its defensive symbiont, “Candidatus Endobugula sertula”. It was proposed that the symbiont-produced predation-deterrent compound acts as a signal to affect female reproductive processes in the host colony. An anatomical comparison of female reproductive structures and oogenesis between symbiotic and symbiont-reduced colonies was performed. Colonies of two cryptic species of B. neritina, Type S and N, were collected in North Carolina and Virginia, USA over several seasons November 2014–December 2015. Relative expression of genes regulating the female reproductive processes in the host was also assessed. Interestingly, no anatomical or molecular differences were found although there were fewer sexual zooids in symbiont-reduced colonies. The lack of difference in oogenesis indicates that the symbiont does not affect female structures and functions in the zooid, but potentially influences early differentiation of female germinal cells. Histological investigation revealed previously undescribed ‘funicular bodies’ containing bacteria in the symbiotic colonies. However, the bacteria associated with the ‘funicular bodies’ and funicular strands in the symbiotic colonies were morphologically different, thus raising the question if the symbiont exists in pleomorphic forms depending on the tissue environment it is localized.

Notes

Acknowledgements

We thank Niels Lindquist (The University of North Carolina-Chapel Hill’s Institute of Marine Sciences) for allowing us generous use of both wet and dry laboratory facilities. We thank staff at the various collection sites for allowing us access to the property for sample collection. We thank Dr. Robert Simmons, Director, Biological Imaging Core Facility at Georgia State University for mentoring and training MM on tissue processing and preparation for microscopy study. We also thank Jonathan Linneman for help in collection of B. neritina colonies and experimental data. We are thankful to two reviewers for comments that significantly improved the manuscript.

Compliance with ethical standards

Funding

This research was supported by the Georgia State University Research Foundation (to NBL). AO is/was financially supported by the Austrian Science Fund (FWF), stand-alone project P27933-B29 (studies on embryonic brooding), Russian Foundation for Basic Research (RFFI), research Grant 16-04-00243-a (studies on oogenesis), and Saint Petersburg State University, research Grants 1.38.233.2015 and 1.42.1099.2016 (studies on bacterial symbionts).

Conflict of interest

The authors declare that they have no conflict of interest.

Ethical approval

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

Human and animal rights

This article does not contain any studies with human participants performed by any of the authors.

Supplementary material

227_2017_3266_MOESM1_ESM.pdf (165 kb)
Supplementary material 1 (PDF 165 kb)

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Copyright information

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Authors and Affiliations

  1. 1.Department of BiologyGeorgia State UniversityAtlantaUSA
  2. 2.Department of Integrative Zoology, Faculty of Life SciencesUniversity of ViennaViennaAustria
  3. 3.Department of Invertebrate Zoology, Faculty of BiologySaint Petersburg State UniversitySaint PetersburgRussia
  4. 4.Department of Palaeontology, Faculty of Earth Sciences, Geography and AstronomyGeozentrum, University of ViennaViennaAustria
  5. 5.School of Earth and Atmospheric Sciences, School of Biological SciencesGeorgia Institute of TechnologyAtlantaUSA

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