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Influence of symbiont-produced bioactive natural products on holobiont fitness in the marine bryozoan, Bugula neritina via protein kinase C (PKC)

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Abstract

Marine invertebrates are a major source of bioactive natural products, many of which are produced by associated microbes. These compounds protect the invertebrate host against predators, competitors, or pathogens by affecting the cellular processes of the host’s adversary, but knowledge about the interaction of the host itself with these symbiont-produced natural products is limited. For example, larvae of the marine bryozoan, Bugula neritina, are defended from predation by the bryostatins, polyketides synthesized by its uncultured endosymbiont, “Candidatus Endobugula sertula.” Bryostatins are potent modulators of the eukaryotic signaling protein, protein kinase C (PKC) that is involved in many cellular processes. In this study, we investigated how host reproduction responds to the absence of the symbiont and symbiont-produced bryostatins in colonies after antibiotic curing and in colonies with naturally reduced symbiont titers. The fecundity of the symbiont-reduced B. neritina colonies was significantly decreased, suggesting that host reproduction is dependent on the symbiont, and/or the bryostatins they produce. To assess the role of PKC in this response, Western blot analysis of protein extracts from symbiotic and symbiont-reduced B. neritina colonies revealed a difference in bryostatin-activated conventional PKCs, but none for bryostatin-independent PKCs. Similar results were observed for PKCs in symbiotic and naturally occurring symbiont-reduced colonies, as well as in the model invertebrate, Caenorhabditis elegans, exposed to bryostatin, suggesting that the bryostatins potentially modulate PKC activity in symbiotic B. neritina and bryostatin-exposed C. elegans. Analysis of the B. neritina transcriptome led to the identification of five PKC isozymes. Since PKCs have been reported to be involved in regulation of reproductive processes and oocyte maturation in various organisms, the findings of this study suggest that the symbiont-produced bryostatins are an important cue for reproduction in the host B. neritina via PKC activation.

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Acknowledgments

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 Casonya M. Johnson for guidance with the C. elegans experiments. We thank Lesley-Ann Hawthorn, Sam Chang, and the staff at the Integrated Genomics Facility, Georgia Regents University Cancer Center, for assistance in preparation and sequencing of cDNA library. We also thank Michelle Ventura and Jonathan Linneman for aid in collection of B. neritina colonies and experimental data. We would also like to thank two reviewers for their comments that significantly improved the manuscript.

Funding

This work was supported by the Georgia State University Research Foundation start-up funds and Illumina/GRU Cancer Center RNA-Seq program Grant to N.B.L.

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

    Meril Mathew, Kayla I. Bean & Nicole B. Lopanik

  2. Department of Computer Science, Georgia State University, Atlanta, GA, 30303, USA

    Yvette Temate-Tiagueu, Adrian Caciula & Alexander Zelikovsky

  3. Department of Computer Science and Engineering, University of Connecticut, Storrs, CT, 06269, USA

    Ion I. Mandoiu

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

    Nicole B. Lopanik

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Mathew, M., Bean, K.I., Temate-Tiagueu, Y. et al. Influence of symbiont-produced bioactive natural products on holobiont fitness in the marine bryozoan, Bugula neritina via protein kinase C (PKC). Mar Biol 163, 44 (2016). https://doi.org/10.1007/s00227-016-2818-x

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