Natural volcanic CO2 seeps reveal future trajectories for host-microbial associations in corals and sponges

Atmospheric carbon dioxide (CO2) levels are rapidly rising causing an increase in the partial pressure of CO2 (pCO(2)) in the ocean and a reduction in pH known as ocean acidification (OA). Natural volcanic seeps in Papua New Guinea expel 99% pure CO2 and thereby offer a unique opportunity to explore the effects of OA in situ. The corals Acropora millepora and Porites cylindrica were less abundant and hosted significantly different microbial communities at the CO2 seep than at nearby control sites <500m away. A primary driver of microbial differences in A. millepora was a 50% reduction of symbiotic Endozoicomonas. This loss of symbiotic taxa from corals at the CO2 seep highlights a potential hurdle for corals to overcome if they are to adapt to and survive OA. In contrast, the two sponges Coelocarteria singaporensis and Cinachyra sp. were similar to 40-fold more abundant at the seep and hosted a significantly higher relative abundance of Synechococcus than sponges at control sites. The increase in photosynthetic microbes at the seep potentially provides these species with a nutritional benefit and enhanced scope for growth under future climate scenarios (thus, flexibility in symbiosis may lead to a larger niche breadth). The microbial community in the apparently pCO(2)-sensitive sponge species S. massa was not significantly different between sites. These data show that responses to elevated pCO(2) are species-specific and that the stability and flexibility of microbial partnerships may have an important role in shaping and contributing to the fitness and success of some hosts.