Abstract
Sponges of the genus Aplysina are among the most common benthic animals on reefs of the Caribbean, and display a wide diversity of morphologies and colors. Tissues of these sponges lack mineralized skeletal elements, but contain a dense spongin skeleton and an elaborate series of tyrosine-derived brominated alkaloid metabolites that function as chemical defenses against predatory fishes, but do not deter some molluscs. Among the earliest marine natural products to be isolated and identified, these metabolites remain the subject of intense interest for commercial applications because of their activities in vari- ous bioassays. In this study, crude organic extracts from 253 sponges from ten morphotypes among the species Aplysina archeri, Aplysina bathyphila, Aplysina cauliformis, Aplysina fistularis, Aplysina fulva, A. insularis, and Aplysina lacunosa were analyzed by liquid chromatography-mass spectrometry (LC-MS) to characterize the pattern of intra- and interspecific variabilities of the twelve major secondary metabolites present therein. Patterns across Aplysina species ranged from the presence of mostly a single compound, fistularin-3, in A. cauliformis, to a mixture of metabolites present in the other species. These patterns did not support the biotransformation hypothesis for conversion of large molecular weight molecules to smaller ones for the purpose of enhanced defense. Discriminant analyses of the metabolite data revealed strong taxonomic patterns that support a close relationship between A. fistularis, A. fulva and A. insu- laris, while two morphotypes of A. cauliformis (lilac creeping vs. brown erect) were very distinct. Two morphotypes of A. lacunosa, one with hard tissue consistency, the other soft and thought to belong to a separate genus (Suberea), had very similar chemical profiles. Of the twelve metabolites found among samples, variation in fistularin-3, dideoxyfistularin-3 and hydroxyaerothionin provided the most pre- dictive influence in decreasing order. Except for one morphotype, weak relationships were found from within-morphotype analyses of metabolite concentrations as a function of geographic location (Florida, N Bahamas, S Bahamas) and depth (<10 m, 10–20 m, >20 m). Our data suggest that metabolite profiles are strongly influenced by sponge phenotype rather than by the diverse microbiome which many Aplysina species share.
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Acknowledgments
This paper has been submitted in honor of the memory of Prof. Rosângela Epifanio. We thank the staff of the NOAA/National Undersea Research Center at Key Largo, Florida and the crew of the RV ‘Seward Johnson’. This research was supported by the National Science Foundation (CHE-9807098 to WF and OCE-9711255, 0095724, 1029515 to JRP) and by the National Undersea Research Program at the University of North Carolina, Wilmington (NA 96RU-0260). Financial support for graduate studies at Scripps Institution of Oceanography was provided to MP with fellowships from the Instituto Colombiano para el Desarrollo de la Ciencia y Tecnologia Francisco Jose de Caldas (COLCIENCIAS-Colombia) and the Fulbright Commission. We are grateful to the State of Florida and the Government of the Bahamas for permission to collect sponge samples.
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MP, JRP and WF designed the study. MP performed the field collections and laboratory analyses. JEB devised and performed the statistical analyses. JRP wrote the first draft, and all authors contributed to the critical reading and editing of the manuscript. All authors read the final manuscript and approved the submission.
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Puyana, M., Pawlik, J., Blum, J. et al. Metabolite variability in Caribbean sponges of the genus Aplysina. Rev. Bras. Farmacogn. 25, 592–599 (2015). https://doi.org/10.1016/j.bjp.2015.08.002
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DOI: https://doi.org/10.1016/j.bjp.2015.08.002