Dichotomy between Regulation of Coral Bacterial Communities and Calcification Physiology under Ocean Acidification Conditions

Ocean acidification (OA) threatens the growth and function of coral reef ecosystems. A key component to coral health is the microbiome, but little is known about the impact of OA on coral microbiomes. A submarine CO(2) vent at Maug Island in the Northern Mariana Islands provides a natural pH gradient to investigate coral responses to long-term OA conditions. Three coral species (Pocillopora eydouxi, Porites lobata, and Porites rus) were sampled from three sites where the mean seawater pH is 8.04, 7.98, and 7.94. We characterized coral bacterial communities (using 16S rRNA gene sequencing) and determined pH of the extracellular calcifying fluid (ECF) (using skeletal boron isotopes) across the seawater pH gradient. Bacterial communities of both Porites species stabilized (decreases in community dispersion) with decreased seawater pH, coupled with large increases in the abundance of Endozoicomonas, an endosymbiont. P. lobata experienced a significant decrease in ECF pH near the vent, whereas P. rus experienced a trending decrease in ECF pH near the vent. In contrast, Pocillopora exhibited bacterial community destabilization (increases in community dispersion), with significant decreases in Endozoicomonas abundance, while its ECF pH remained unchanged across the pH gradient. Our study shows that OA has multiple consequences on Endozoicomonas abundance and suggests that Endozoicomonas abundance may be an indicator of coral response to OA. We reveal an interesting dichotomy between two facets of coral physiology (regulation of bacterial communities and regulation of calcification), highlighting the importance of multidisciplinary approaches to understanding coral health and function in a changing ocean. IMPORTANCE Ocean acidification (OA) is a consequence of anthropogenic CO(2) emissions that is negatively impacting marine ecosystems such as coral reefs. OA affects many aspects of coral physiology, including growth (i.e., calcification) and disrupting associated bacterial communities. Coral-associated bacteria are important for host health, but it remains unclear how coral-associated bacterial communities will respond to future OA conditions. We document changes in coral-associated bacterial communities and changes to calcification physiology with long-term exposure to decreases in seawater pH that are environmentally relevant under midrange IPCC emission scenarios (0.1 pH units). We also find species-specific responses that may reflect different responses to long-term OA. In Pocillopora, calcification physiology was highly regulated despite changing seawater conditions. In Porites spp., changes in bacterial communities do not reflect a breakdown of coral-bacterial symbiosis. Insights into calcification and host-microbe interactions are critical to predicting the health and function of different coral taxa to future OA conditions.