Abstract
Candidatus Endobugula sertula, the uncultivated -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.
| Original language | English (US) |
|---|---|
| Pages (from-to) | 693-702 |
| Number of pages | 10 |
| Journal | ISME Journal |
| Volume | 1 |
| Issue number | 8 |
| DOIs | |
| State | Published - Dec 2007 |
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Keywords
- Bryostatin localization
- Bryostatins
- Bugula neritina
- Invertebrate-bacterial symbiosis
- Larval development
ASJC Scopus subject areas
- Ecology, Evolution, Behavior and Systematics
Cite this
Localization of Candidatus Endobugula sertula and the bryostatins throughout the life cycle of the bryozoan Bugula neritina. / Sharp, Koty H.; Davidson, Seana K.; Haygood, Margo.
In: ISME Journal, Vol. 1, No. 8, 12.2007, p. 693-702.Research output: Contribution to journal › Article
}
TY - JOUR
T1 - Localization of Candidatus Endobugula sertula and the bryostatins throughout the life cycle of the bryozoan Bugula neritina
AU - Sharp, Koty H.
AU - Davidson, Seana K.
AU - Haygood, Margo
PY - 2007/12
Y1 - 2007/12
N2 - Candidatus Endobugula sertula, the uncultivated -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.
AB - Candidatus Endobugula sertula, the uncultivated -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.
KW - Bryostatin localization
KW - Bryostatins
KW - Bugula neritina
KW - Invertebrate-bacterial symbiosis
KW - Larval development
UR - http://www.scopus.com/inward/record.url?scp=36849004408&partnerID=8YFLogxK
UR - http://www.scopus.com/inward/citedby.url?scp=36849004408&partnerID=8YFLogxK
U2 - 10.1038/ismej.2007.78
DO - 10.1038/ismej.2007.78
M3 - Article
C2 - 18059493
AN - SCOPUS:36849004408
VL - 1
SP - 693
EP - 702
JO - ISME Journal
JF - ISME Journal
SN - 1751-7362
IS - 8
ER -