A sponge/dinoflagellate association in the haplosclerid sponge Haliclona sp.: cellular origin of cytotoxic alkaloids by Percoll density gradient fractionation

Abstract

Light-microscopic and electron-microscopic studies of the tropical marine sponge Haliclona sp. (Order: Haplosclerida; Family: Haliclonidae) from Heron Island, Great Barrier Reef, have revealed that this sponge is characterized by the presence of dinoflagellates and by nematocysts. The dinoflagellates are 7-10 micrometer in size, intracellular, and contain a pyrenoid with a single stalk, whereas the single chloroplast is branched, curved, and lacks grana. Mitochondria are present, and the nucleus is oval and has distinct chromosomal structure. The dinoflagellates are morphologically similar to Symbiodinium microadriaticum, the common intracellular symbiont of corals, although more detailed biochemical and molecular studies are required to provide a precise taxonomic assignment. The major sponge cell types found in Haliclona sp. are spongocytes, choanocytes, and archaeocytes; groups of dinoflagellates are enclosed within large vacuoles in the archaeocytes. The occurrence of dinoflagellates in marine sponges has previously been thought to be restricted to a small group of sponges including the excavating hadromerid sponges; the dinoflagellates in these sponges are usually referred to as symbionts. The role of the dinoflagellates present in Haliclona sp. as a genuine symbiotic partner requires experimental investigation. The sponge grows on coral substrates, from which it may acquire the nematocysts, and shows features, such as mucus production, which are typical of some excavating sponges. The cytotoxic alkaloids, haliclonacyclamines A and B, associated with Haliclona sp. are shown by Percoll density gradient fractionation to be localized within the sponge cells rather than the dinoflagellates. The ability to synthesize bioactive compounds such as the haliclonacyclamines may help Haliclona sp. to preserve its remarkable ecological niche.

Sponge-Associated Microorganisms: Evolution, Ecology, and Biotechnological Potential

“…24). Many researchers have employed cell separation techniques for this purpose (27,28,99,103,120,314,315,332,416,417). A major breakthrough in this area came with the realization that chemically fixed sponge and microbial cells retain their natural products in a form amenable to chemical analyses, such as high-performance liquid chromatography and nuclear magnetic resonance spectroscopy (416).…”

“…Density gradient centrifugation provides yet another opportunity for separating sponge and microbial cells. In this case, dissociated sponge tissue is placed above a density gradient (consisting of, e.g., Ficoll or Percoll), and following centrifugation, various cell fractions are formed based on differing densities (103,120,121,315). Individual fractions can then be examined chemically and microscopically to correlate the occurrence of compounds with specific cell types.…”

“…Sponge-inhabiting dinoflagellates (120,152,153,338,339,355,382,454,477) and diatoms (16,47,51,53,65,113,305,390,409,454) have been reported, with the latter seemingly most prevalent in polar regions (16,51,53,113,305,409,454). Freshwater sponges often contain endosymbiotic microalgae, primarily zoochlorellae (30,108,109,331,333,475,488).…”

Pyrosequencing reveals highly diverse and species-specific microbial communities in sponges from the Red Sea

“…They have attracted substantial research interest because of their ecological importance and their production of a wide range of bioactive compounds for pharmacological use (Vogel, 2008). One striking characteristic of sponges is their association with a remarkable array of microorganisms, including archaea (Preston et al, 1996), bacteria , cyanobacteria (Thacker and Starnes, 2003), unicellular algae (Vacelet, 1982), dinoflagellates (Garson et al, 1998) and fungi (Maldonado et al, 2005), which can constitute up to 60% of the tissue volume in some sponge species (Vacelet and Donadey, 1977;Hentschel et al, 2003) and exceed a density of 10 9 microbial cells per ml of sponge tissue ). The extraordinary highly abundant and diverse microorganisms in sponges have led to ecological questions on their role, consistency and specificity of their association, and it is still enigmatic how the association is established and maintained.…”

Comparative morphometry, biochemical and elemental composition of three marine sponges (Petrosiidae) from Gulf of Mannar, India

“…As the demand for pharmacologically potent natural products is constantly increasing, attempts for the biotechnological production of sponge tissues are being made. Several studies suggest secondary metabolite production by sponge symbionts (Molinski, 1993;Oclarit et al, 1994;Bewley et al, 1996;Hentschel et al, 2001), whereas others indicate their production by sponge cells (Uriz et al, 1996 a,b;Garson et al, 1998;Turon et al, 2000). Sponges possess strong regenerative capacities (Simpson, 1984), and pieces of live sponge tissue are able to grow and regenerate into healthy sponges.…”