Metagenomic shifts in mucus, tissue and skeleton of the coral Balanophyllia europaea living along a natural CO2 gradient

Abstract

Using the Mediterranean coral Balanophyllia europaea naturally growing along a pH gradient close to Panarea island (Italy) as a model, we explored the role of host-associated microbiomes in coral acclimatization to ocean acidification (OA). Coral samples were collected at three sites along the gradient, mimicking seawater conditions projected for 2100 under different IPCC (The Intergovernmental Panel on Climate Change) scenarios, and mucus, soft tissue and skeleton associated microbiomes were characterized by shotgun metagenomics. According to our findings, OA induced functional changes in the microbiomes genetic potential that could mitigate the sub-optimal environmental conditions at three levels: i. selection of bacteria genetically equipped with functions related to stress resistance; ii. shifts in microbial carbohydrate metabolism from energy production to maintenance of cell membranes and walls integrity; iii. gain of functions able to respond to variations in nitrogen needs at the holobiont level, such as genes devoted to organic nitrogen mobilization. We hence provided hypotheses about the functional role of the coral associated microbiome in favoring host acclimatation to OA, remarking on the importance of considering the crosstalk among all the components of the holobiont to unveil how and to what extent corals will maintain their functionality under forthcoming ocean conditions.

Acclimatization of a coral-dinoflagellate mutualism at a CO2 vent

“…Many corals harbor bacteria capable of fixing N 2 gas (diazotrophs) 53 and a growing body of literature indicates that ocean acidification may promote the enrichment of dinitrogen fixing bacterial communities in natural microbiomes 8 , 54 , 55 . Indeed, recent work at our study site found that the prevalence of genes associated with N 2 fixation, as well as the production of N storage molecules, increases in the B. europaea microbiome under low pH conditions 56 . Increased assimilation of diazotroph-derived N by the coral is supported by our isotopic data (Fig.…”

“…Likewise, it has been hypothesized that photosynthetically fixed carbon supplied by the dinoflagellates may serve as an energy source for N 2 fixation in cyanobacterial symbionts in corals 60 , suggesting that in zooxanthellate corals, photosynthesis and N 2 fixation may be, in some cases, interdependent. Moreover, enhanced N 2 fixation by diazotrophs living in association with the coral tissue/mucus 56 may partially explain the observed increase in dinoflagellate symbiont cell densities in B. europaea at the low pH Sites 65 , and viceversa. Enhanced translocation of photosynthetically fixed carbon as a result of high dinoflagellate symbiont cell densities may help sustain the high costs of diazotroph N 2 fixation under increased acidification.…”

Microbiome-assisted restoration of degraded marine habitats: a new nature-based solution?

“…Transplant-induced coral diseases could combine with the adverse effects of climate change, thus hampering successful restoration. Despite it has been reported that the coral microbiome can acclimatize to climate-driven changing conditions (including pH acidification, and heatwaves) enriching its functions related to nitrogen metabolism, host nutrition, and increased resistance (Biagi et al, 2020;Palladino et al, 2022;Prada et al, 2023), monitoring microbiome changes in restoration projects could be useful for predicting the effects of multiple stressors.…”

Emerging Technologies for the Discovery of Novel Diversity in Cyanobacteria and Algae and the Elucidation of Their Valuable Metabolites

“…Metagenomic studies have demonstrated that microorganisms significantly impact the health of coral reef ecosystems [40], and that toxic cyanobacteria can cause coral disease and potential harm to reef ecosystems [41]. Furthermore, metagenomic investigations have identified variations in the coral microbiome in response to environmental change, including pollution [42] and carbon dioxide gradients [43]. Lichens represent another important example of symbiotic associations.…”