Activated Chemical Defense in Marine Sponges—a Case Study on Aplysinella rhax
- 344 Downloads
Activated chemical defense, i.e., the rapid conversion of precursor molecules to defensive compounds following tissue damage, has been well documented for terrestrial and marine plants; but evidence for its presence in sessile marine invertebrates remains scarce. We observed a wound-activated conversion of psammaplin A sulfate to psammaplin A in tissue of the tropical sponge Aplysinella rhax. The conversion is rapid (requiring only seconds), the turnover rate increases with increasing wounding activity (e.g., ~20% after tissue stabbing vs. ~85% after tissue grinding), and is likely enzyme-catalyzed (no reaction in the absence of water and inhibition of the conversion by heat). Fish feeding assays with the pufferfish Canthigaster solandri, an omnivorous sponge predator, revealed an increased anti-feeding activity by the conversion product psammaplin A compared to the precursor psammaplin A sulfate. We propose that the wound-activated formation of psammaplin A in A. rhax is an activated defense targeted against predator species that are not efficiently repelled by the sponge’s constitutive chemical defense. Recent observations of conversion reactions also in other sponge species indicate that more activated defenses may exist in this phylum. Based on the findings of this study, we address the question whether activated defenses may be more common in sponges—and perhaps also in other sessile marine invertebrates—than hitherto believed.
KeywordsWound-activated bioconversion Aplysinella rhax Verongida Psammaplin A Direct induced defense Feeding deterrent
NMR and LC/MS analyses were conducted by T. Hemscheidt from the Department of Chemistry, University of Hawaii. D. Taitano and B. Antolin helped with the feeding assays and the compound extraction. L. Goldman and N. Pioppi assisted in sponge collection. We thank C. Kohlert-Schupp for interesting discussions, A. Kerr for critical proofreading of the manuscript and advice in statistical matters, as well as two anonymous reviewers whose comments greatly improved this manuscript. CT gratefully acknowledges support with a Fedodor Lynen Fellowship from the Alexander von Humboldt-Foundation, Bonn. This research was supported by NIH MBRS SCORE grant SO6-GM-44796-15 and SO6-GM-44796-16a to PS. This is University of Guam Marine Laboratory contribution number 613.
- Byun, D. S., Kim, D. S., Godber, J. S., Nam, S. W., Oh, M. J., Shim, H. S., and Kim, H. R. 2004. Isolation and characterization of marine bacterium producing arylsulfatase. J. Microbiol. Biotechnol. 14:1134–1141.Google Scholar
- Gahan, P. B. 1981. Cell senescence and death in plants, pp. 145–169, in I. D. Bowen, and R. A. Lockshin (eds.). Cell Death in Biology and PathologyChapman & Hall, London.Google Scholar
- Hällgren, J., and Öquist, G. 1990. Adaptations to low temperatures, pp. 265–293, in R. G. Alscher, and J. R. Cumming (eds.). Stress Responses in Plants: Adaptation and Acclimation MechanismsWiley, New York.Google Scholar
- Myers, R. F. 1991. Micronesian reef fishes. Coral, Barrigada, Guam.Google Scholar
- Richelle-Maurer, E., De Kluijver, M. J., Feio, S., Gaudencio, S., Gaspar, H., Gomez, R., Tavares, R., Van-Der-Vyver, G., and Soest, R. W. M. V. 2003. Localization and ecological significance of oroidin and sceptrin in the Caribbean sponge Agelas conifera. Biochem. Syst. Ecol. 31:1073–1091.CrossRefGoogle Scholar
- Thoms, C., and Schupp, P. J. 2007. Chemical defense strategies in sponges: a review, pp. 627–637, in M. R. Custódio, G. Lôbo-Hajdu, E. Hajdu, and G. Muricy (eds.). Porifera Research—Biodiversity, Innovation and Sustainability. Série Livros 28Museu Nacional, Rio de Janeiro.Google Scholar
- Weber, F. J., and Debont, J. A. M. 1996. Adaptation mechanisms of microorganisms to the toxic effects of organic solvents on membranes. Biochim. Biophys. Acta-Rev. Biomembr. 1286:225–245.Google Scholar
- Zar, J. H. 1999. Biostatistical analysis. Prentice-Hall, Upper Saddle River, New Jersey.Google Scholar