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Fundamental to holobiont biology is recognising how variation in microbial composition and function relates to host phenotypic variation. Sponges often exhibit considerable phenotypic plasticity and also harbour dense microbial communities that function to protect and nourish hosts. One of the most prominent sponge genera on Caribbean coral reefs isAgelas. Using a comprehensive set of morphological (growth form, spicule), chemical and molecular data on 13 recognised species ofAgelasin the Caribbean basin, we were able to define only five species (=clades) and found that many morphospecies designations were incongruent with phylogenomic and population genetic analyses. Microbial communities were also strongly differentiated between phylogenetic species, showing little evidence of cryptic divergence and relatively low correlation with morphospecies assignment. Metagenomic analyses also showed strong correspondence to phylogenetic species, and to a lesser extent, geographical and morphological characters. Surprisingly, the variation in secondary metabolites produced by sponge holobionts was explained by geography and morphospecies assignment, in addition to phylogenetic species, and covaried significantly with a subset of microbial symbionts. Spicule characteristics were highly plastic, under greater impact from geographical location than phylogeny. Our results suggest that while phenotypic plasticity is rampant inAgelas, morphological differences within phylogenetic species affect functionally important ecological traits, including the composition of the symbiotic microbial communities and metabolomic profiles.

 

Mesophotic coral reef ecosystems (MCEs) are characterized by gradients in irradiance, temperature and trophic resources. As depth increases on Caribbean mesophotic reefs, particulate organic matter increases while dissolved organic matter decreases, and the increase in particulate organic matter is directly related to the increase in sponge abundances and growth rates on MCEs. To further understand the trophic ecology of sponges, changes in microbiome composition and function, stable isotopic composition and proximate biochemical composition of 4 Caribbean reef sponges ( Amphimedon compressa , Agelas tubulata , Plakortis angulospiculatus and Xestospongia muta) were quantified along a shallow to mesophotic depth gradient on Grand Cayman Island. Increases in δ 15 N for all sponges were observed as depth increased, indicating an increasing reliance on heterotrophic food resources. Species-specific changes in symbiotic microbial community composition were also observed as depth increased, and the predicted functional genes associated with nitrogen and carbon cycling showed species-specific changes between depths. Regardless of species-specific changes in microbiome community structure or function, or whether sponges were classified as high microbial or low microbial abundance, sponges increased their consumption of particulate organic matter with increasing depth into the lower mesophotic zone. 

Sponges in the genus Agelas produce a diversity of bromopyrrole alkaloid secondary metabolites, some of which are known to inhibit predators and pathogens. Selective pressures on sponges to produce chemical defenses vary in time and space, often resulting in differences in the production of secondary metabolites. To characterize intraspecific variation in these compounds, we generated metabolomic profiles of the Caribbean sponge A. tubulata across spatial gradients, including multiple sites in Belize and Grand Cayman, and depths ranging from 15 to 61 m in Grand Cayman. Samples were also analyzed from a reciprocal transplant experiment across shallow (22 m) to mesophotic (61 m) reefs. We found quantitative, but not qualitative, differences in metabolite profiles across sites and depths, with 9 metabolites contributing to that variation. In addition, transplanting sponges across depths resulted in significant changes in concentrations of the metabolite sceptrin. Sponge extracts exhibited antibacterial activity against a panel of marine and human pathogens. Multiple regression analyses showed that different metabolites were associated with antibacterial activity against different pathogens. The strongest compound-specific relationship was a negative effect of oroidin on the growth of Serratia marcescens, and purified oroidin was found to inhibit S. marcescens growth in a dose-dependent manner. Overall, A. tubulata exhibits intraspecific variability in the production of antibacterial secondary metabolites across sites and depths that signals selective responses to its environment. Given the current increase in sponge densities, and incidence of disease on coral reefs, these data have implications for disease resistance and resilience of sponges in the Anthropocene.