Endozoicomonas provides corals with steroid hormones during thermal stress

Abstract

The coral microbiome is believed to play a critical role in sustaining corals and enabling adaptation to thermal stress. A ubiquitous group of coral-associated bacteria, known as Endozoicomonas, are hypothesized to provide essential metabolites to corals, though the exact roles these bacteria play during ambient or thermal stress conditions are largely unknown. We demonstrate that while Endozoicomonas synthesizes the iron-binding siderophore aerobactin in vitro, this trait may be suppressed in hospite. Integrated metagenomics, metabolomics, and lab validations reveal that within the coral holobiont Endozoicomonas is the only microbe capable of metabolizing coral-derived testosterone and converting ubiquitous cholesterol into testosterone and progesterone, important steroids that accumulate within the coral holobiont during thermal stress. Provision of testosterone and progesterone to corals during thermal stress induced transcriptional reprogramming of the coral innate immune response, promoting cellular survival and suggesting active microbial involvement in immune priming and stress resilience. These findings highlight a previously unrecognized mechanism of microbial contribution to coral resilience. Lastly, the capacity of bacteria to synthesize eukaryotic steroids implies deep evolutionary connections between microbial metabolism and the origin of steroid-mediated processes in early eukaryogenesis.