Symbiont-dependent sexual reproduction in marine colonial invertebrate: morphological and molecular evidence
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.
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
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 220.127.116.115 and 1.42.1099.2016 (studies on bacterial symbionts).
Conflict of interest
The authors declare that they have no conflict of interest.
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.
- Best MA, Thorpe JP (2002) Use of radioactive labelled food to assess the role of the funicular system in the transport of metabolites in the cheilostome bryozoan Membranipora membranacea (L.). In: Jackson PNW, Buttler CJ, Jones MS (eds) Bryozoan studies 2001. AA Balkema Publishers, Lisse/Abingdon/Exton/Tokyo, pp 29–35Google Scholar
- Dorée M, Hunt T (2002) From Cdc2 to Cdk1: when did the cell cycle kinase join its cyclin partner? J Cell Sci 115:2461–2464Google Scholar
- Haygood MG, Davidson SK (1997) Small-subunit rRNA genes and in situ hybridization with oligonucleotides specific for the bacterial symbionts in the larvae of the bryozoan Bugula neritina and proposal of “Candidatus endobugula sertula”. Appl Environ Microbiol 63:4612–4616Google Scholar
- Haygood MG, Schmidt EW, Davidson SK, Faulkner DJ (1999) Microbial symbionts of marine invertebrates: opportunities for microbial biotechnology. J Mol Microbiol Biotechnol 1:33–43Google Scholar
- Kalive M, Faust JJ, Koeneman BA, Capco DG (2010) Involvement of the PKC family in regulation of early development. Mol Reprod Dev 77:95–104Google Scholar
- Labbe J, Capony J, Caput D, Cavadore J, Derancourt J, Kaghad M, Lelias J, Picard A, Doree M (1989) MPF from starfish oocytes at first meiotic metaphase is a heterodimer containing one molecule of cdc2 and one molecule of cyclin B. EMBO J 8:3053Google Scholar
- Lutaud G (1969) La nature des corps funiculaires des cellularines, bryozoaires chilostomes. Arch Zool Exp Gen 110:2–30Google Scholar
- Lutaud G (1985) Preliminary experiments on interzooidal metabolic transfer in anascan bryozoans. In: Nielsen C, Larwood GP (eds) Bryozoa: Ordovician to Recent. Olsen and Olsen, Fredensborg, pp 183–191Google Scholar
- Mawatari S (1951) The natural history of a common fouling bryozoan, Bugula neritina (Linnaeus). Misc Rep Res Inst Nat Resour 20:47–54Google Scholar
- Ostrovsky AN (2013b) From incipient to substantial: evolution of placentotrophy in a phylum of aquatic colonial invertebrates. Evolution 67:1368–1382Google Scholar
- Reed C (1991) Bryozoa. In: Giese ACPJ, Pearse VB (eds) Reprod Mar Invertebr. The Boxwood Press, Pacific Grove, pp 85–245Google Scholar
- Silén L (1945) The main features of the development of the ovum, embryo and ooecium in the ooecioferous Bryozoa Gymnolaemata. Ark Zool 35A:1–34Google Scholar
- Sudek S, Lopanik NB, Waggoner LE, Hildebrand M, Anderson C, Liu H, Patel A, Sherman DH, Haygood MG (2007) Identification of the putative bryostatin polyketide synthase gene cluster from “Candidatus Endobugula sertula”, the uncultivated microbial symbiont of the marine bryozoan Bugula neritina. J Nat Prod 70:67–74CrossRefGoogle Scholar
- Vermeij GJ (1978) Biogeography and adaptation: patterns of marine life. Harvard University Press, CambridgeGoogle Scholar
- Woollacott R, Zimmer R (1972) Origin and structure of the brood chamber in Bugula neritina (Bryozoa). Mar Biol 16:165–170Google Scholar
- Wourms J (1987) Oogenesis. In: Giese A, Pearse JS, Pearse VB (eds) Reproduction of marine invertebrates: general aspects: seeking unity in diversity. Boxwood Press, Pacific Grove, pp 50–178Google Scholar