The Precursor Hypothesis of Sponge Kleptocnidism: Development of Nematocysts in Haliclona cnidata sp. nov. (Porifera, Demospongiae, Haplosclerida)

Abstract

Marine sponges thrive in benthic environments despite intense spatial competition and predator pressure. The sessile filter-feeders usually compensate their lack of physical defense and behavioral escape by a high level of bioactivity. In the stinging black sponge (Haliclona cnidata sp. nov.), these chemical defense mechanisms are complemented by "cellular weapons"-functional nematocysts likely acquired from cnidarians (kleptocnidism). Whereas, kleptocnidism might be facilitated by a close contact with cnidarian donors, preliminary investigations suggest that the stinging black sponge sustains nematocysts even if kept apart from cnidarians. As the underlying mechanisms causing this phenomenon remain unknown, the development of its nematocysts was studied in both presence and absence of potential cnidarian donors. First, we compared inherent nematocysts of adult sponge individuals with foreign nematocysts of co-cultivated cnidarians to identify potential donors. Second, we experimentally assessed the donor-independent and donor-dependent development of inherent and foreign nematocysts within cultures of sponge cell aggregates (SCAs). The inherent nematocysts comprised two specific types that both differed from those of the eight co-cultivated cnidarians. Specifically, we showed that the number of sponge-inherent nematocysts increased in SCAs over time in the absence of potential donors. Numbers of supplied foreign nematocysts, however, did not increase in the SCAs. We conclude that the observed increase of inherent nematocysts is due to the maturation of nematocyst precursor cells. Given these findings, we here propose the precursor hypothesis of sponge kleptocnidism. Accordingly, nematocyst precursors or immature nematocyte-nematocyst complexes might be initially acquired by sponges through filtration, maintained in sponge tissues, and nurtured to fully functioning nematocyte-nematocyst complexes. The underlying evolutionary processes are likely facilitated by bacteria-derived secondary metabolites and photosynthetically active dinoflagellates. Schellenberg et al. Precursor Hypothesis Sponge Kleptocnidism Due to a simple body plan and the in vitro proliferation capacity of sponge cells, H. cnidata sp. nov. may serve as a novel evolutionary model system to further assess fundamental research questions regarding kleptocnidism. This study not only sheds new light on kleptocnidism in sponges, it also calls for a holobiontic view at defense mechanisms that involves the actual sponge, cnidarian nematocysts, dinoflagellate endosymbionts, and a complex microbial community.Life Science Identifier (LSID): urn:lsid:zoobank.org:act

The Bacterial Microbiome of the Long-Term Aquarium Cultured High-Microbial Abundance Sponge Haliclona cnidata – Sustained Bioactivity Despite Community Shifts Under Detrimental Conditions

“…Such a color change can be induced by spongeassociated microbiota, e.g., through pigments of phototrophic symbionts including Cyanobacteria (Usher et al, 2004;Burgsdorf et al, 2015) or associated zooxanthellae (Rützler, 2002). The latter type of microbiota is known to occur in H. cnidata (Schellenberg et al, 2019). Additionally, evidence for Cyanobacteria were found as bacterial cells with thylakoid membranes were detected in bacteriocytes resembling Candidatus Synechococcus spongiarum (Usher, 2008) as well as the highly abundant autofluorescent rod-shaped cells that were arranged in aggregates.…”

“…Experiments were performed with the marine sponge Haliclona cnidata (Schellenberg et al, 2019), which has been in long-term culture at the Justus Liebig University Giessen (Giessen, Germany) since 2000. The model organism has been selected to assess bioactivity-based defense due to clear indication for a pronounced bioactivity (unpublished data).…”

“…The model organism has been selected to assess bioactivity-based defense due to clear indication for a pronounced bioactivity (unpublished data). The natural distribution of H. cnidata is unknown (Schellenberg et al, 2019), hence material was sampled from a tropical marine aquarium (4000 L closed water circulating tank system, a constant water temperature of 26 • C, 10:14 light:dark photoperiod, salinity of 32-33%). Water currents were created using a wavebox (10,000 L/h; Tunze, Penzberg, Germany) with a water flow through of 2000 L/h.…”

Transcriptomic response of Cinachyrella cf. cavernosa sponges to spatial competition

“…This phenomenon has been reported in other sponges like Haliclona spp. (Schellenberg et al, 2019;Russell, Degnan, Garson, & Skilleter, 2003). However, there is no other evidence of presence of nematocysts in the sponge Cinachyrella cf.…”

Contact-free modulation of stony coral productivity by sessile reef organisms

“…Because of its documented high bioactive potential and storage of functional nematocysts (39), we expected it to negatively affect stony coral productivity. One possible explanation for its positive effect may be a suspected symbiosis with Cnidaria (47), making its interactions in the reef more complex, and requiring follow-up work. Alternatively, increased productivity by corals could also be a defense mechanism, to avoid competition by the sponge.…”