Microbiome-mediated polyphosphate accumulation enhances the resilience of sponge holobionts to future climate scenarios

Abstract Ocean warming is threatening the stability of marine ecosystems, yet the mechanisms underlying the resilience of foundational species like sponges remain poorly understood. Polyphosphate (PolyP), a key player in marine phosphorus burial, is hypothesized to play an important role in sponge stress adaptation. Here, we demonstrated that microbiome-mediated PolyP dynamics were closely associated with sponge adaptation to thermal stress. Field investigation of three sponge species (Spongia sp., Tedania sp., Haliclona simulans) revealed marked interspecific differences in PolyP accumulation, with Spongia sp. maintaining the highest PolyP levels. Strong seasonal fluctuations in sponge PolyP content, peaking in June and reaching a minimum in January, correlated with ambient temperature. We found that this variation was regulated by ppk1 gene expression levels rather than by altering the microbial composition. The ppk1-harboring microbial assemblages exhibited host specificity, and phylogenetic analysis uncovered sponge-specific clades of ppk1 genes. Laboratory warming experiments further confirmed the functional link: under acute heat stress, both the ppk1 gene of the symbiotic microorganisms and the inorganic pyrophosphatase (ppa) gene in the host were upregulated in Spongia sp. PolyP likely provide an energy source for the host, maintaining holobiont stability and leading to low mortality. Conversely, H. simulans, with limited PolyP supply, ultimately suffered 100% mortality. Our results establish a link whereby sponge-associated microbes, via ppk1 expression, modulate PolyP accumulation to support host oxidative phosphorylation and mitigate thermal stress. This microbiome-mediated physiological pathway contributes to our understanding of sponge climate resilience, offering new functional insights into holobiont persistence in a warming ocean.