Unveiling microbiome changes in Mediterranean octocorals during the 2022 marine heatwaves: quantifying key bacterial symbionts and potential pathogens.

BACKGROUND: Climate change has accelerated the occurrence and severity of heatwaves in the Mediterranean Sea and poses a significant threat to the octocoral species that form the foundation of marine animal forests (MAFs). As coral health intricately relies on the symbiotic relationships established between corals and microbial communities, our goal was to gain a deeper understanding of the role of bacteria in the observed tissue loss of key octocoral species following the unprecedented heatwaves in 2022. RESULTS: Using amplicon sequencing and taxon-specific qPCR analyses, we unexpectedly found that the absolute abundance of the major bacterial symbionts, Spirochaetaceae (C. rubrum) and Endozoicomonas (P. clavata), remained, in most cases, unchanged between colonies with 0% and 90% tissue loss. These results suggest that the impairment of coral health was not due to the loss of the main bacterial symbionts. However, we observed a significant increase in the total abundance of bacterial opportunists, including putative pathogens such as Vibrio, which was not evident when only their relative abundance was considered. In addition, there was no clear relation between bacterial symbiont loss and the intensity of thermal stress, suggesting that factors other than temperature may have influenced the differential response of octocoral microbiomes at different sampling sites. CONCLUSIONS: Our results indicate that tissue loss in octocorals is not directly caused by the decline of the main bacterial symbionts but by the proliferation of opportunistic and pathogenic bacteria. Our findings thus underscore the significance of considering both relative and absolute quantification approaches when evaluating the impact of stressors on coral microbiome as the relative quantification does not accurately depict the actual changes in the microbiome. Consequently, this research enhances our comprehension of the intricate interplay between host organisms, their microbiomes, and environmental stressors, while offering valuable insights into the ecological implications of heatwaves on marine animal forests. Video Abstract.

Nutrient starvation and nitrate pollution impairs the assimilation of dissolved organic phosphorus in coral-Symbiodiniaceae symbiosis.

Phosphorus (P) is an essential but limiting nutrient for coral growth due to low concentrations of dissolved inorganic concentrations (DIP) in reef waters. P limitation is often exacerbated when concentrations of dissolved inorganic nitrogen (DIN) increase in the reef. To increase their access to phosphorus, corals can use organic P dissolved in seawater (DOP). They possess phosphatase enzymes that transform DOP into DIP, which can then be taken up by coral symbionts. Although the concentration of DOP in reef waters is much higher than DIP, the dependence of corals on this P source is still poorly understood, especially with different concentrations of DIN in seawater. As efforts to predict the future of corals increase, improved knowledge of the P requirements of corals living under different DIN concentrations may be key to predicting coral health. In this study, we investigated P content and phosphatase activities (PAs) in Stylophora pistillata maintained under nutrient starvation, long-term nitrogen enrichment (nitrate or ammonium at 2 µM) and short-term (few hours) nitrogen pulses. Results show that under nutrient depletion and ammonium-enriched conditions, a significant increase in PAs was observed compared to control conditions, with no change in the N:P ratio of the coral tissue. On the contrary, under nitrate enrichment, there was no increase in PAs compared to control conditions, but an increase in the N:P ratio of the coral tissue. These results suggest that under nitrate enrichment, corals were unable to increase their ability to rely on DOP and replenish their cellular P content. An increase in cellular N:P ratio is detrimental to coral health as it increases the susceptibility of coral bleaching under thermal stress. These results provide an overall view of the P requirements of corals exposed to different nutrient conditions and improve our understanding of the effects of nitrogen enrichment on corals.