Standing on the shoulders of microbes: microbiome thermal priming buffers the effects of heatwaves on clams by preventing stress overreaction

Abstract In the context of rapidly accelerating global warming, the rising frequency of heatwaves is driving large-scale ecological shifts, profoundly affecting organismal physiology and ecosystem functioning. Thermal tolerance is a key determinant of species resilience. Evidence from diverse model systems indicates that this tolerance can be enhanced through thermal priming, a pre-adaptive process in which organisms are exposed to sublethal heat stress. Beyond intrinsic host factors, the adaptive potential of host-associated microbiomes is increasingly recognised as a critical role in shaping organismal thermal resilience. However, the extent to which microbiomes alone can enhance host thermal tolerance remains largely unknown. Here, we used the Manila clam (Ruditapes philippinarum), one of the most widely farmed bivalves, as a model system to test whether thermal pre-adaptation of the microbiome is sufficient to improve host thermal tolerance. Clams were thermally primed, their microbiota isolated, and subsequently transplanted into non-acclimated individuals, which were then exposed to simulated heatwave conditions. By integrating microbial community profiling, host physiological measurements, and transcriptomic analyses, we demonstrate that transplantation of a microbiome from animals previously exposed to heat stress is sufficient to enhance host resilience during subsequent heat stress. This effect arises from adaptive shifts in microbiome composition that promote energy conservation and survival through elevated antioxidant activity and a broad downregulation of host transcriptional pathways, placing the host in an energy-efficient, stress-mitigating state. Our findings provide novel insights into holobiont-level adaptive mechanisms to stress adaptation and hold practical potential for developing microbiome-based interventions to enhance thermal tolerance in aquaculture systems.