Localization of ‘Candidatus Endobugula sertula’ and the bryostatins throughout the life cycle of the bryozoan Bugula neritina

Abstract

'Candidatus Endobugula sertula,' the uncultivated c-proteobacterial symbiont of the marine bryozoan Bugula neritina, synthesizes bryostatins, complex polyketides that render B. neritina larvae unpalatable to predators. Although the symbiosis is well described, little is known about the locations of 'E. sertula' or the bryostatins throughout larval settlement, metamorphosis and early development. In this study, we simultaneously localized 'E. sertula' and the bryostatins in multiple stages of the B. neritina life cycle, using a novel bryostatin detection method based on its known ability to bind mammalian protein kinase C. Our results suggest that the bryostatins are deposited onto the exterior of B. neritina larvae during embryonic development, persist on the larval surface throughout metamorphosis and are shed prior to cuticle formation. During metamorphosis, 'E. sertula' remains adhered to the larval pallial epithelium and is incorporated into the preancestrula cystid tissue layer, which ultimately develops into a bud and gives rise to the next zooid in the colony. Colocalization of bryostatin signal with aggregates of 'E. sertula' in buds of ancestrulae suggested new synthesis of bryostatins in ancestrulae. In adult B. neritina colonies, symbiont microcolonies were observed in the funicular cords of rhizoids, which likely result in asexual transmission of 'E. sertula' to regenerated colonies. Furthermore, bryostatin signal was detected on the surface of the rhizoids of adult B. neritina colonies. Through simultaneous localization of the bryostatins and the 'E. sertula,' we determined how 'E. sertula' is transmitted, and identified shifts in bryostatin localization throughout the life cycle of the host B. neritina.

Symbiosis as a General Principle in Eukaryotic Evolution

“…Similarly, many grasses are protected from herbivory by alkaloids that are synthesized by clavicipitaceous fungal endophytes that ramify through the plant tissues (Fletcher and Harvey 1981), and the genetic basis of the fungal synthesis of one key alkaloid loline by the fungal endophyte in the grass Lolium has been established (Spiering et al 2005). Secondary metabolites synthesized by microbial symbionts have also been shown to contribute to the protection against predators and pathogens in multiple benthic marine animals, including sponges (Piel et al 2004b), bryozoans (Sharp et al 2007), and tunicates (Kwan et al 2012).…”

In an early branching metazoan, bacterial colonization of the embryo is controlled by maternal antimicrobial peptides

“…These bacteria may protect eggs and embryos from fungal infection. In the marine bryozoan Bugula neritina (34), a bacterial symbiont colonizes the early stages of development and produces complex polyketides, making the larvae stages unpalatable to predators (34). In squids, during spawning, bacterial symbionts secreted onto the egg jelly by the adult accessory nidamental gland may function to protect the released eggs (35,36).…”

Primary screening of potentially bio-active substances in the lyophilisate of Pectinatella magnifica biomass

“…The next steps and procedures should be aimed at confirming the presence of bio-active substances in subsequent treatments, their possible identification and finally, comparing their effects with substances known from marine Bryozoa (among many sources e.g. Davidson and Haygood 1999;Davidson et al 2001;Sharp et al 2007;Ariza et al 2011). …”

“…The antibacterial activity and/or cytotoxicity are regarded as the most significant properties of these substances. Also, dermal allergy, anthelmintic activity or prevention of cell division had been identified in some substances (Sharp et al 2007). Bryostatins considered as the most important bio-active substances were first discovered in the marine bryozoan Bugula neritina (Davidson et al 2001;Manning et al 2005;Schmidt 2005;Sun and Alkon 2006;Mayer and Gustafson 2008) ), and bryostatin 1 has been proposed as a potential drug for treatment of leukaemia, lymphomas, melanomas and solid tumours (Davidson and Haygood 1999;Davidson et al 2001), traumatic brain injury (Zohar et al 2011), depression, Alzheimer's disease and other CNS disorders (Sun and Alkon 2006;Paul et al 2007).…”