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

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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.

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Fig. 1

Adapted from Coleman and Dunphy (1994), Eckberg et al. (1996), Voronina and Wessel (2003), Levasseur et al. (2013) and Adhikari and Liu (2014)

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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.

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Authors and Affiliations

  1. Department of Biology, Georgia State University, Atlanta, GA, 30303, USA

    Meril Mathew

  2. Department of Integrative Zoology, Faculty of Life Sciences, University of Vienna, Althanstrasse 14, 1090, Vienna, Austria

    Thomas Schwaha

  3. Department of Invertebrate Zoology, Faculty of Biology, Saint Petersburg State University, Universitetskaya nab. 7/9, Saint Petersburg, 199034, Russia

    Andrew N. Ostrovsky

  4. Department of Palaeontology, Faculty of Earth Sciences, Geography and Astronomy, Geozentrum, University of Vienna, Althanstrasse 14, 1090, Vienna, Austria

    Andrew N. Ostrovsky

  5. School of Earth and Atmospheric Sciences, School of Biological Sciences, Georgia Institute of Technology, 311 Ferst Drive, Atlanta, GA, 30332-0340, USA

    Nicole B. Lopanik

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Correspondence to Nicole B. Lopanik.

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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).

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Mathew, M., Schwaha, T., Ostrovsky, A.N. et al. Symbiont-dependent sexual reproduction in marine colonial invertebrate: morphological and molecular evidence. Mar Biol 165, 14 (2018). https://doi.org/10.1007/s00227-017-3266-y

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