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

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. herbaceawhether it is a distinct species or a species complex-has never been assessed. Recent biochemical proWling revealed anti-plasmodial activity of brominated compounds in Lamellodysidea of the PaciWc. Here, we present a comparative chemotaxonomic and molecular analysis of selected Dysideidae from the PaciWc 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 IndoPaciWc L. herbacea populations, also reXected by diVerent PBDE compound proWles. Molecular and biochemical data also revealed a Lamellodysidea species new to science. Several specimens misidentiWed as Lamellodysidea were detected based on their position on diVerent clades in the molecular phylogeny and their production of diVerent 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, aVect the chemical constituents produced in L. herbacea.

Cryptic speciation and phylogeographic relationships in the elephant ear spongeIanthella basta(Porifera, Ianthellidae) from northern Australia

“…nov. aff. herbacea , and in this species each colour morph hosts a separate strain of the symbiotic cyanobacterium Oscillatoria (Thacker & Starnes, 2003; Erpenbeck et al ., 2012). Coloration in sponges is a highly variable trait influenced by environmental factors, predation pressure or the presence of symbiotic microorganisms (Thacker & Starnes, 2003; Reveillaud et al ., 2010; Freckelton et al ., 2012).…”

Evolutionary stability of antibiotic protection in a defensive symbiosis

“…12), rendering combination prophylaxes a common phenomenon in defensive symbioses. However, the long-term evolutionary stability of the beewolves' antibiotic mixture is unusual in light of many systems that exhibit dramatic changes in defensive chemistry, often through the dynamic acquisition of novel protective symbionts (27,(90)(91)(92)(93)(94)(95)(96). As discussed above, the lack of a specialized coevolving antagonist likely relaxed selection for fundamental changes in defensive chemistry in the beewolf symbiosis.…”

Defensive symbioses of animals with prokaryotic and eukaryotic microorganisms

“…Additional studies conrmed that the presence of unique symbiont strains in different sponge species of the family Dysideidae 48 conferred the characteristic chemical proles to their hosts and supported the occurrence of host switches and independent infection events. 49 Furthermore, D. herbacea individuals can harbor an additional symbiont of the genus Synechocystis, which produces the potent neurotoxin dysiherbaine 14. 50 In analogy to the Oscillatoria symbionts, Synechocystis strains vary in their ability to synthesize dysiherbaine, thereby resulting in different host chemotypes.…”