The gut microbiome and host molecular response of a grouper to acute and chronic heat stress

Globally, aquaculture and fisheries play an important role in providing animal protein for human consumption. However, climate change poses a significant threat to these industries, with marine heatwaves becoming increasingly frequent and severe. Especially the effect of heat stress on the important symbiotic relationship of a host and the intestinal microbiome is understudied. In this study, we investigated the impact of short-term acute heat stress (3 days, AHS) and a longer-term marine heatwave (21 days, MHW) of +3 °C on the microbial community and molecular response of commercially and culturally important juvenile Malabar grouper. Our findings indicate that both the AHS and MHW resulted in measurable effects on the fish, which are still detectable after a four-week recovery period. While the microbial richness in the stomach showed a decreasing trend post-heatwave, no significant increase in pathogenic Vibrio was observed. In contrast, the host transcriptome of the stomach, particularly in regard to the MHW, showed a response in the form of a downregulation of mitochondrial function and digestive processes. After recovery, these effects turn into an upregulation of tissue repair and extracellular matrix reorganisation. Contrastingly, the pyloric caeca showed minimal response to either treatment, suggesting maintenance of function during both AHS or an MHW. These findings highlight the variable response of the Malabar grouper to AHS and an MHW. While some aspects reveal resilience, such as the absence of increased Vibrio in the stomach and the stability of both microbiome and host transcriptome in the pyloric caeca, other indicators suggest negative impacts. Overall, the results indicate that while the fish can cope with AHS and a strong MHWin certain aspects, others can pose challenges. Understanding these complex dynamics is crucial for assessing the full impact of climate change on both wild and cultured populations of economically and culturally important mesopredators. • Malabar grouper were exposed to 3-day acute heat stress and a 3-week heatwave, and also sampled after recovery. • Stomach and pyloric caeca tissues were sequenced for bacterial communities and host molecular responses. • A +3 °C heat stress has limited effect on the microbial communities. • Strong molecular response of stomach tied to energy production during heatwave. • Upregulation of tissue repair in stomach after recovery period.