The interactive effects of ocean acidification and warming on bioeroding sponge Spheciospongia vesparium microbiome indicated by metatranscriptomics

Global climate change will cause coral reefs decline and is expected to increase the reef erosion potential of bioeroding sponges. Microbial symbionts are essential for the overall fitness and survival of sponge holobionts in changing ocean environments. However, we rarely know about the impacts of ocean warming and acidification on bioeroding sponge microbiome. Here, the structural and functional changes of the bioeroding sponge Spheciospongia vesparium microbiome, as well as its recovery potential, were investigated at the RNA level in a laboratory system simulating 32 °C and pH 7.7. Based on metatranscriptome analysis, acidification showed no significant impact, while warming or simultaneous warming and acidification disrupted the sponge microbiome. Warming caused microbial dysbiosis and recruited potentially opportunistic and pathogenic members of Nesiotobacter, Oceanospirillaceae, Deltaproteobacteria, Epsilonproteobacteria, Bacteroidetes and Firmicutes. Moreover, warming disrupted nutrient exchange and molecular interactions in the sponge holobiont, accompanied by stimulation of virulence activity and anaerobic metabolism including denitrification and dissimilatory reduction of nitrate and sulfate to promote sponge necrosis. Particularly, the interaction between acidification and warming alleviated the negative effects of warming and enhanced the Rhodobacteraceae-driven ethylmalonyl-CoA pathway and sulfur-oxidizing multienzyme system. The microbiome could not recover during the experiment period after warming or combined stress was removed. This study suggests that warming or combined warming and acidification will irreversibly destabilize the S. vesparium microbial community structure and function, and provides insight into the molecular mechanisms of the interactive effects of acidification and warming on the sponge microbiome.