Marine sponges often contain diverse and abundant microbial communities, including bacteria, archaea, microalgae, and fungi. In some cases, these microbial associates comprise as much as 40% of the sponge volume and can contribute significantly to host metabolism (e.g., via photosynthesis or nitrogen fixation). We review in detail the diversity of microbes associated with sponges, including extensive 16S rRNA-based phylogenetic analyses which support the previously suggested existence of a sponge-specific microbiota. These analyses provide a suitable vantage point from which to consider the potential evolutionary and ecological ramifications of these widespread, sponge-specific microorganisms. Subsequently, we examine the ecology of sponge-microbe associations, including the establishment and maintenance of these sometimes intimate partnerships, the varied nature of the interactions (ranging from mutualism to host-pathogen relationships), and the broad-scale patterns of symbiont distribution. The ecological and evolutionary importance of sponge-microbe associations is mirrored by their enormous biotechnological potential: marine sponges are among the animal kingdom's most prolific producers of bioactive metabolites, and in at least some cases, the compounds are of microbial rather than sponge origin. We review the status of this important field, outlining the various approaches (e.g., cultivation, cell separation, and metagenomics) which have been employed to access the chemical wealth of sponge-microbe associations.

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

The insoluble granular material of the acrosome vesicle of sea urchin sperm has been isolated and shown to be a single 30,500 dalton protein for which the name "bindin" is proposed. The data presented are consistent with the hypothesis that bindin is the adhesive responsible for the attachment of sperm to the vitelline layer of the egg. Experimental results suggest that bindin may act by binding to carbohydrate receptors of vitelline layer glycoproteins. The speculation is made that sperm bindins may be the general mechanism by which animal sperm attach to eggs.

https://www.pnas.org/content/pnas/74/6/2456.full.pdf

Isolation of bindin: the protein responsible for adhesion of sperm to sea urchin eggs

Marine sponges have been considered as a gold mine during the past 50 years, with respect to the diversity of their secondary metabolites. The biological effects of new metabolites from sponges have been reported in hundreds of scientific papers, and they are reviewed here. Sponges have the potential to provide future drugs against important diseases, such as cancer, a range of viral diseases, malaria, and inflammations. Although the molecular mode of action of most metabolites is still unclear, for a substantial number of compounds the mechanisms by which they interfere with the pathogenesis of a wide range of diseases have been reported. This knowledge is one of the key factors necessary to transform bioactive compounds into medicines. Sponges produce a plethora of chemical compounds with widely varying carbon skeletons, which have been found to interfere with pathogenesis at many different points. The fact that a particular disease can be fought at different points increases the chance of developing selective drugs for specific targets.

/pdf/marine-sponges-as-pharmacy-1k32yowllo.pdf

Marine sponges as pharmacy.

Sponges are host organisms for various symbiotic microorganisms such as archaea, bacteria, cyano-bacteria and microalgae. Sponges are also sources of a wide variety of useful natural products like cyto-toxins, antifouling agents, antibiotics, and anti-inflammatory and antiviral compounds. Symbioticmicroorganisms in sponges can be sources of various natural products, because metabolites previouslyascribed to sponges have recently been demonstrated to be biosynthesized by symbionts. If a symbioticmicroorganism from which some natural products are derived can be cultured, the microorganismcould be used in a mass production of the bioactive compounds. We summarize recent research on iso-lation and cultivation of sponge-symbiotic microorganisms and the symbiotic relationship. Key words: bioactive compound, natural products, symbiotic microorganism, sponges, symbiosisWhy sponge-symbiotic microorganisms?Sponges (Phylum Porifera) are very fertile host animalsfor diverse symbiotic microorganisms. Sponges are sim-ple multicellular invertebrates attached to solid substratesin benthic habitats. All sponges are filter feeders; numer-ous tiny pores on the surface allow water to enter and cir-culate through a series of canals where microorganismsand organic particles are filtered out and eaten. Sincesponges are efficient filter feeders, any microorganismsthat can resist the sponge digestive process and immuneresponse can successfully inhabit sponges (126). Sponges have been excellent sources for natural prod-ucts that are bioactive compounds (Table 1). Their bio-activity includes enzyme inhibitors, cell division-inhibitors,antiviral, antifungal, antimicrobial, anti-inflammatory, anti-tumor, cytotoxic or cardiovascular properties (79). Reportsof the isolation of natural products from marine spongeshave been published from the early 1950's (4), and researchactivities on this topic have continued to increase (79).Nowadays, several papers on new natural products fromsponges are published monthly; and Faulkner (27) haspublished surveys on many more natural products recentlyisolated from sponges. Many of these natural products have interesting bio-medical potential, pharmaceutical relevance and diverseapplications (44, 46). For example, arabinose-nucleosideswith antiviral and anticancer activity isolated from spongeCryptotethya crypta, are used clinically; manoalide obtainedfrom sponge Luffariella variabilis is a candidate for newdrugs with anti-inflammatory activity (68). Also, metab-olites previously ascribed to sponges have been recentlydemonstrated to be biosynthesized by symbionts. If somecompounds are derived from a symbiotic microorganism,culturing the microorganism could provide an improvedsource of the bioactive compound (97). Thus, we havefocused on sponge-symbiotic microorganisms as a sourceof various natural products in this review.What microorganisms live in sponges?Various microorganisms have been found in sponges (Table2). They include a diverse range of archaea, heterotrophicbacteria, cyanobacteria, green algae, red algae, crypto-phytes, dinoflagellates and diatoms (22, 70, 88, 96). Thesymbiotic microbial community is highly novel and diverse,and species composition shows temporal and geographicvariation (121). However, only very little information existsabout the taxonomic affiliation of sponge-symbiotic micro-organisms (32). One host sponge can possess diverse symbionts. Forexample, sponge Theonella swinhoei supports unicellularheterotrophic bacteria, unicellular cyanobacteria and fila-mentous heterotrophic bacteria at the same time (7). Asponge belonging to Aplysina includes heterogeneous bac-teria Bacillus sp., Micrococcus sp., Arthrobacter sp., Vibriosp., Pseudoalteromonas sp., and so on (46). Sponge Rho-

Microbial Symbiosis in Marine Sponges

In spite of the fact that cells from the phylum Porifera (sponges) contain high levels of telomerase activity, no successful approach to cultivate sponge cells has yet been described. Telomerase is the enzyme which catalyzes the addition of new telomeres onto chromosome ends which have been lost after each round of DNA synthesis. One reason may be seen in the observation that after dissociation the cells lose their telomerase activity. In addition, no nutrients and metabolites have been identified that would stimulate sponge cells to divide. We report here the culture conditions required for the formation of multicellular aggregates from Suberites domuncula from dissociated single cells; they are termed primmorphs. These aggregates, formed in seawater supplemented with antibiotics, have a tissue-like appearance; they have been cultured for more than 5 mo. Cross sections through the primmorphs revealed an organized zonation into a distinct unicellular epithelium-like layer of pinacocytes and a central zone composed primarily of spherulous cells. After their association into primmorphs, the cells turn from the telomerase-negative state to the telomerase-positive state. Important is the finding that a major fraction of the cells in the primmorphs undergo DNA synthesis and hence have the capacity to divide. By applying the BrdU (5-bromo-2'-deoxy-uridine)-labeling and detection assay it is demonstrated that up to 33.8 % of the cells in the primmorphs are labeled with BrdU after an incubation period of 12 h. It is proposed that the primmorph system described here is a powerful novel model system to study basic mechanisms of cell proliferation and cell death; it can also be used in aquaculture, for the production of bioactive compounds and as a bioindicator system.

/pdf/establishment-of-a-primary-cell-culture-from-a-sponge-2xtuijvoht.pdf

Establishment of a primary cell culture from a sponge: primmorphs from Suberites domuncula

From the marine sponge Halichondria panicea a lectin was isolated and characterized The homogeneous lectin (composed of protein to 807% and of neutral carbohydrates to 141%) had a molecular weight of 78,000 (determined by gel filtration) and consisted of four subunits with a molecular weight of 21,000 each (determined by gel electrophoresis in the presence of sodium dodecyl sulfate) The hemagglutinating activity was only slightly dependent upon ionic strength and incubation temperature and did not require divalent cations, but it was inhibited by reagents for thiol groups The Halichondria lectin was completely inhibited in hemagglutination competition experiments in the presence of fetuin, D-galacturonic acid, D-glucuronic acid, polygalacturonic acid, or L-fucose The purified Halichondria lectin did not cause reaggregation of dissociated H panicea cells From the same sponge species bacteria were isolated and identified as Pseudomonas insolita These bacteria were cultivated in marine broth 2216 Under these culture conditions the bacteria grew only in the presence of the homologous lectin; the lectin-caused effect was not abolished by D-glucuronic acid or D-galacturonic acid However, after addition of a polysaccharide-containing fraction isolated from P insolita, the lectin-caused, growth-promoting effect was abolished Other lectins were found to exhibit no growth-promoting effect On the basis of colony counts, P insolita was the predominant bacterial species in the sponge extract; 19 X 10(6) Pseudomonas colonies were measured in extracts isolated from 1 g of sponge The assumption of an interrelationship between the sponge and the bacterium is supported by the results indicating that the Halichondria lectin has no effect on the growth of such bacteria isolated from six other marine sponge species Evidence is presented which indicates that the Halichondria lectin is not utilized during growth of the Pseudomonas species Lectin activity was detected on the surface of mucoid cells from H panicea From the data obtained the possibility is discussed that the Halichondria lectin is a basis for a symbiotic relationship between the sponge and the bacterium Images

Lectin, a possible basis for symbiosis between bacteria and sponges.

SUMMARY An aggregation receptor from the siliceous sponge Geodia cydonium has been isolated and purified in an almost pure form. It sediments at about 2-6 s, has a buoyant density of 151 g/ml in CsCl and elutes from Sephadex G-50 at a V,jV0 value of i - 3ii . Chemical analysis revealed that the receptor consists of 81 % neutral carbohydrate and 7-5% protein. The activity of the receptor is rapidly destroyed by Na-periodate. The receptor is released from the cell surface after removal of Ca 2+ from the medium or after incubation of the cells with trypsin. The depleted cells can be charged again with isolated receptor molecules. The binding of the receptor molecules on the cell surface is prevented in the presence of trypsin. For optimal binding, physiological salt concentrations with respect to NaCl (540 mM NaCl) and Ca !+ ions are necessary. The receptor whose isolation is described in this report, is involved in secondary aggregation processes, which are initiated by a soluble aggregation factor. The primary aggregation of the cells is not influenced by the receptor. Time-course studies with receptor-depleted cells revealed that new aggregation receptor molecules are formed during the aggregation process. By competition experiments it could be shown that high concentrations of soluble aggregation receptor molecules inhibit secondary aggregation. The soluble receptor molecules can compete with surface-bound receptor molecules only if these are not linked with the aggregation factor.

Species-specific aggregation factor in sponges vi. aggregation receptor from the cell surface

Collagen, isolated from the sponge Geodia cydonium in the absence of denaturing agents, had the typical amino acid composition and was associated with the carbohydrates galactose and glucose. The resulting individual fibrils with a diameter of 23 nm, displayed a 19.5 nm periodicity with one intraperiod band. A collagen assembly factor (CAF) was identified in and partially purified from the extracellular space. The CAF reacted with antibodies against intact Geodia cells but not with antibodies against Geodia lectin and Geodia aggregation factor. In the presence of the CAF, the collagen fibrils reconstituted collagen bundles in an ordered sequence of events, which were followed by electron-microscopical and biochemical methods. Bundle formation was not dependent on the presence of the homologous lectin, glycoconjugates or aggregation factor. Homologous cells (Geodia archaeocytes) were determined to attach only to those Geodia collagen substrates that contained CAF. The attachment of these cells did not require fibronectin or Geodia lectin. Homologous glycoconjugates or NaOH-treated collagen inhibited cell attachment. Collagen from the sponge Chondrosia reniformis, even in the presence of Geodia CAF, was no appropriate substrate for Geodia cell attachment. Whether collagen is a component of cell-matrix interactions in sponge systems also in vivo is discussed.

Attachment of sponge cells to collagen substrata: effect of a collagen assembly factor.

Cell aggregation of the marine sponge Geodia cydonium. Identification of lectin-producing cells.

Aggregation of sponge cells: stage dependent, distinct adhesion mechanisms in Cliona celata.

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