Metamorphosis of a Scleractinian Coral in Response to Microbial Biofilms

Abstract

Microorganisms have been reported to induce settlement and metamorphosis in a wide range of marine invertebrate species. However, the primary cue reported for metamorphosis of coral larvae is calcareous coralline algae (CCA). Herein we report the community structure of developing coral reef biofilms and the potential role they play in triggering the metamorphosis of a scleractinian coral. Two-week-old biofilms induced metamorphosis in less than 10% of larvae, whereas metamorphosis increased significantly on older biofilms, with a maximum of 41% occurring on 8-week-old microbial films. There was a significant influence of depth in 4-and 8-week biofilms, with greater levels of metamorphosis occurring in response to shallow-water communities. Importantly, larvae were found to settle and metamorphose in response to microbial biofilms lacking CCA from both shallow and deep treatments, indicating that microorganisms not associated with CCA may play a significant role in coral metamorphosis. A polyphasic approach consisting of scanning electron microscopy, fluorescence in situ hybridization (FISH), and denaturing gradient gel electrophoresis (DGGE) revealed that coral reef biofilms were comprised of complex bacterial and microalgal communities which were distinct at each depth and time. Principal-component analysis of FISH data showed that the Alphaproteobacteria, Betaproteobacteria, Gammaproteobacteria, and Cytophaga-Flavobacterium of Bacteroidetes had the largest influence on overall community composition. A low abundance of Archaea was detected in almost all biofilms, providing the first report of Archaea associated with coral reef biofilms. No differences in the relative densities of each subdivision of Proteobacteria were observed between slides that induced larval metamorphosis and those that did not. Comparative cluster analysis of bacterial DGGE patterns also revealed that there were clear age and depth distinctions in biofilm community structure; however, no difference was detected in banding profiles between biofilms which induced larval metamorphosis and those where no metamorphosis occurred. This investigation demonstrates that complex microbial communities can induce coral metamorphosis in the absence of CCA.

Larvae of Pocillopora damicornis (Anthozoa) settle and metamorphose in response to surface-biofilm bacteria

“…The same is true for P. damicornis in Australia (Harriott 1983). It has been shown that the biofilm bacterial communities can differ vastly among different CCA species (Johnson et al 1991) as well as among non-biological surfaces at different depths and times (Webster et al 2004). Therefore, different bacterial species may affect settlement of coral larvae differently.…”

“…Thus, the authors concluded that CCA might not be the sole inducer of coral settlement in these species. Microbial biofilms alone, in the absence of CCA, also induced settlement in larvae of A. microphthalma (Webster et al 2004). Golbuu & Richmond (2007) examined 2 species of corals in Guam and found that one (Goniastrea retiformis) preferentially settled on CCA, while the other (Stylaraea punctata) settled on biofilmed carbonate rubble.…”

“…Anthozoans, particularly corals, utilize a diverse range of cues. Cues can be associated with crustose coralline algae (CCA) (Morse et al 1988, 1996, Baird et al 2003, Baird & Morse 2004, Harrington et al 2004, Golbuu & Richmond 2007, Kitamura et al 2007, Ritson-Williams et al 2010, Price 2010 or marine bacteria and biofilms (Negri et al 2001, Webster et al 2004. Four species of Acropora (A. tenuis, A. millepora, A. palmata, and A. cervicornis) have been shown to preferentially settle on a particular species of CCA, Titanoderma prototypum (Harrington et al 2004, Ritson-Williams et al 2010, which is also preferred by other hard corals (Pocillopora spp.…”

Coral recruitment and potential recovery of eutrophied and blast fishing impacted reefs in Spermonde Archipelago, Indonesia

“…However, it is known that also surface conditioning, e.g. by biofilms, is important in the context of coral larvae settlement (Webster et al, 2004). The bacterial community structure of biofilms was investigated in a parallel study on the same settlement tiles (but not all sites) (Sawall et al, 2012).…”

“…One of the advantages of spawning during the calm season, which usually coincides with low precipitation, low river run-off and low nutrient supply to coastal waters, may be in the lower abundance of space competitors that are competitively superior in nutrient-enriched waters (algae, fast-growing ascidians, barnacles and other opportunistic fouling organisms; Birkeland, 1977;Glassom et al, 2004). Larval dispersal depends on the competency period of the larvae and the prevailing small (within reef) and large-scale currents (between reefs) (Sammarco and Andrews, 1989;Black et al, 1990) and larvae settlement and metamorphosis depend on the availability and suitability of substrate, which is supportive if heterogeneous, non-moving and biologically preconditioned (Fox et al, 2003;Webster et al, 2004;Petersen et al, 2005;Sawall et al, 2010). After metamorphosis and initial growth, survival may further dependent on water quality, light environment and abundance of potential space competitors and predators (Birkeland, 1977;Abelson et al, 2005;Ferse, 2008).…”