Single-cell ecology of coral-algal symbiosis breakdown

Abstract Background The symbiosis between corals and dinoflagellate algae is disrupted by heat stress, leading to bleaching and subsequent coral mortality, devastating reef habitats. Despite its planetary-scale impact, bleaching is a cellular-level breakdown of a multi-partner symbiosis. While much is known about the physiological and genomic responses of corals to bleaching, our understanding of it at the cellular level, specifically the interactions between the coral host, algal symbionts, and their microbial communities, remains limited. By combining single-cell transcriptomics, marker gene metabarcoding (16S rRNA + 18S rRNA + ITS2), and photochemical measurements, we provide a granular view of the microbial ecology of symbiotic breakdown. Results In heat-stress experiments with the coral Orbicella faveolata , which hosts two co-dominant algal symbionts, we observed distinct transcriptomic responses between Durusdinium and Breviolum , particularly in transcripts involved in nitrogen cycling. Coral cell type-specific expression was also observed, notably between gastrodermal cells hosting either algal symbiont, where we see symbiont-specific suppression of host heat stress genes, and in coral gland cells, where mucocytes appear to play an active role in the bleaching response. Furthermore, for the first time, we show the concurrent shifts in the prokaryotic and microeukaryotic microbiomes during experimental heat stress. This was marked by a decrease in suspected nitrifying bacteria, concurrent with an increase in suspected denitrifiers and nitrate reducers, early in the heat-stress response. This higher nitrogen availability, which is theorized to decouple Symbiodiniaceae population regulation from control by the coral host, also leads to a bloom of other microbes such as chlorophytes, diatoms, and labyrinthulids which may further contribute to the negative feedback loops that characterize coral bleaching. Conclusions Using scRNA-seq and the latest metabarcoding methodologies, we provide a comprehensive view of the coral holobiont, in which all members are considered interconnected and important to the health of the entire microbial ecosystem. We found cell-type specific responses to bleaching, particularly within mucocytes and gastrodermal cells. Notably, a subpopulation of gland cells (mucocytes) showed a distinct increase during heat stress. We also saw an apparent symbiont-specific suppression of heat-stress-associated transcripts within coral gastrodermal cells. Other members of the holobiont also stood out during the bleaching process, including prokaryotes potentially important to nutrient cycling and previously overlooked protists. This study marks a starting point toward understanding the cellular dynamics of coral holobionts, shedding light on the mechanisms behind symbiosis breakdown, coral mortality, and ultimately, reef decline.