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Variability in antimicrobial chemical defenses in the Caribbean sponge Agelas tubulata: implications for disease resistance and resilience

Amelia Clayshulte Abraham, Deborah J. Gochfeld, Bharathi Avula, Keir J. Macartney, Michael P. Lesser, Marc Slattery*

*Corresponding author:

ABSTRACT: 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, Agelas tubulata, across spatial gradients, including multiple sites in Belize and Grand Cayman, and depths ranging from 15-61 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 nine 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.