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Evolution, radiation and chemotaxonomy of Lamellodysidea, a demosponge genus with anti-plasmodial metabolites

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Abstract

Sponges of the family Dysideidae (Dictyoceratida) are renowned for their diversity of secondary metabolites, and its genus Lamellodysidea, particularly Lamellodysidea herbacea, is the most studied taxon biochemically. Despite its importance, the taxonomic status of L. herbacea—whether it is a distinct species or a species complex—has never been assessed. Recent biochemical profiling revealed anti-plasmodial activity of brominated compounds in Lamellodysidea of the Pacific. Here, we present a comparative chemotaxonomic and molecular analysis of selected Dysideidae from the Pacific and the Indian Ocean (New Caledonia, Great Barrier Reef, Fiji, Mayotte, Guam, Palau). We investigated the phylogenetic relationships between the populations and assessed their bioactive (PBDE) compounds in order to unravel the taxonomic status of this commercially important group of sponges and assessed patterns of dispersal and biochemical variation. The molecular phylogeny was based on the internal transcribed ribosomal spacer and compared against a PBDE phylogeny for several specimens. Molecular data revealed a diversity of Indo-Pacific L. herbacea populations, also reflected by different PBDE compound profiles. Molecular and biochemical data also revealed a Lamellodysidea species new to science. Several specimens misidentified as Lamellodysidea were detected based on their position on different clades in the molecular phylogeny and their production of different halogenated compounds (brominated vs. chlorinated). The direct comparison of molecular and biochemical data also provided evidence for the occurrence of a host switch event and support for the theory that abiotic factors, such as sedimentation, affect the chemical constituents produced in L. herbacea.

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Acknowledgments

DE acknowledges financial support of the European Union under a Marie-Curie outgoing fellowship (MOIF-CT-2004 Contract No 2882). MC thanks the French Embassy in Suva (Fiji) and the Agence Française de Développement through the CRISP (Coral Reef Initiative in the South Pacific) project for financial support. The governments of the Solomon and Fiji Islands allowed us to collect, while the respective Fisheries Departments assisted us with the conduction of the field work. GW is grateful for a grant from the German Science Foundation (DFG). GW and DE appreciate funding from the GeoBio-CenterLMU for support of sponge barcoding, and together with JH gratefully acknowledge the financial support of the Marine Barcoding of Life (MarBOL) initiative with funding from the Alfred P Sloan Foundation, New York. We thank the IRD-SEOH center in Noumea, New Caledonia, for their help in collecting samples and Bob Thacker for fruitful discussions. Two anonymous reviewers provided us with very detailed suggestions for the improvements of the manuscript, and they are warmly thanked here.

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Authors and Affiliations

  1. Department of Earth and Environmental Sciences and GeoBio-Center, Ludwig-Maximilians-University Munich (LMU), Munich, Germany

    Dirk Erpenbeck & Gert Wörheide

  2. Biodiversity Program, Queensland Museum, South Brisbane, QLD, Australia

    Dirk Erpenbeck, John N. A. Hooper & Patricia Sutcliffe

  3. Laboratoire de Chimie Des Biomolécules et de l’Environnement EA 4215, Université de Perpignan, Perpignan, France

    Isabelle Bonnard, Mayuri Chandra & Bernard Banaigs

  4. IRD, UMR 152, Pharmacochimie et Pharmacologie pour le Développement, Toulouse, France

    Mayuri Chandra & Pierre Perio

  5. School of Natural Sciences, NUI Galway, Galway, Ireland

    Carsten Wolff

  6. Bayerische Staatssammlung für Paläontologie und Geologie, Munchen, Germany

    Gert Wörheide

  7. IRD, UMR 7138, Systématique, Adaptation, Evolution, Tahiti, French Polynesia

    Cécile Debitus & Sylvain Petek

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  1. Dirk Erpenbeck
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  2. John N. A. Hooper
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  3. Isabelle Bonnard
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  4. Patricia Sutcliffe
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Correspondence to Dirk Erpenbeck.

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Communicated by S. Uthicke.

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Erpenbeck, D., Hooper, J.N.A., Bonnard, I. et al. Evolution, radiation and chemotaxonomy of Lamellodysidea, a demosponge genus with anti-plasmodial metabolites. Mar Biol 159, 1119–1127 (2012). https://doi.org/10.1007/s00227-012-1891-z

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