Host matters: coral reef fish species show distinct skin microbiome responses to upwelling-driven environmental changes

Disentangling the drivers structuring microbiomes can help predict organisms’ responses to rapid environmental change. However, despite microbial communities being important for both host and environmental health, large gaps remain in our understanding of how host-associated microbiomes are structured and respond to different stimuli, especially in marine environments. Here, we leverage a seasonal upwelling gradient in Panama’s Tropical Eastern Pacific, investigating how the diversity and composition of ten coral reef fish species’ skin microbiomes compare between regions and seasons that experience different environmental conditions. Fish skin microbiomes varied greatly within and among host species and were distinct from the microbiomes of the surrounding seawater. All species had diverse skin microbiomes, with a dominance of Proteobacteria (65%), Bacteroidota (13%), and Cyanobacteria (6%). Host species and trophic group played a greater role in determining fish skin microbiome structure than seasonal and regional environmental variation, despite water microbiomes responding strongly to both season and region. Nevertheless, three out of five trophic groups: the herbivores, carnivores, and planktivore, also displayed significant changes in their microbiomes during upwelling, albeit to a lesser extent than water samples, whereas the invertivores’ and omnivore’s microbiomes did not change significantly. We performed differential abundance (DA) analyses on these fish and compared microbial taxa that changed between seasons and regions in fish versus water samples. While water communities had thousands of significant DA taxa, fish had around 40 times fewer (n = 17 to 73) and only shared 47 DA taxa with the water samples. Differences between these microbial communities likely arise from both host selection via fishes’ immune system and the skin mucus serving as an environmental filter. However, neither host-associated nor environmental predictors fully explained the variation in microbiome composition, highlighting its complexity. Our results show how ecological differences between host species may elicit distinct microbiome responses to environmental changes, with potential cascading effects on ecosystem dynamics under global climate change. Further characterization of marine microbial communities, as well as additional physicochemical and host-related parameters, will be key to monitoring and predicting how these communities will respond to the increasingly rapid and widespread environmental changes our oceans are facing.