Microbial pollution disables the chemical defenses of sea fans

In coastal ecosystems, chemically rich species like gorgonians rely on specialized metabolites and symbiotic microbes for health and defense. In the Southwestern Atlantic, the elephant ear coral Phyllogorgia dilatata builds structurally complex forests and provides habitat for several species. Recent declines in cover have been linked to widespread disease, fouling, and necrosis. The loss of chemical defense due to anthropic perturbation has never been reported in the marine environment. We investigated whether pollution-driven stress could lead to a dysfunctional holobiont and impairment of its chemical defense. Using chromatography coupled to high-resolution mass spectrometry and molecular networking, we profiled secondary metabolites and used 16S rRNA gene amplicon sequencing to characterize microbial communities, relating these data to visual surveys of P. dilatata gorgonian forests. Defense compounds were found only in colonies far from pollution sources and correlated with bacteria associated with healthier environments. In contrast, pathogenic and sewage-associated bacteria dominated near the polluted site, where defenseless colonies of P. dilatata showed more disease and impaired health. Our results indicate that microbial pollution affects the capacity to modulate the microbiome through the use of infochemicals and leads to disruption of symbiosis and loss of chemical defense. A: Sea fans with a healthy aspect (fan integrity, active polyps and usual pigmentation) from the control site, far from microbial pollution, had higher diterpene content and chemical redundancy of cembranoid compounds, while maintaining a healthier microbiome. Colonies inhabiting the rocky reefs in proximity to the runoff were dysfunctional, devoid of cembranoid diterpenes, and exposed to fouling, corallivores and pathogens. • Pollution disrupts the holobiont of the gorgonian Phyllogorgia dilatata . • Chemical defenses occur only in colonies distant from pollution sources. • Polluted sites show shifts to pathogenic and sewage-associated bacteria. • Metabolomics and microbiome data reveal impaired symbiosis under stress. • Microbial pollution reduces infochemical-based microbiome regulation.