Greater Mitochondrial Energy Production Provides Resistance to Ocean Acidification in “Winning” Hermatypic Corals

Abstract

Coral communities around the world are projected to be negatively affected by ocean acidification. Not all coral species will respond in the same manner to rising CO2 levels. Evidence from naturally acidified areas such as CO2 seeps have shown that although a few species are resistant to elevated CO2, most lack sufficient resistance resulting in their decline. This has led to the simple grouping of coral species into “winners” and “losers,” but the physiological traits supporting this ecological assessment are yet to be fully understood. Here using CO2 seeps, in two biogeographically distinct regions, we investigated whether physiological traits related to energy production [mitochondrial electron transport systems (ETSAs) activities] and biomass (protein contents) differed between winning and losing species in order to identify possible physiological traits of resistance to ocean acidification and whether they can be acquired during short-term transplantations. We show that winning species had a lower biomass (protein contents per coral surface area) resulting in a higher potential for energy production (biomass specific ETSA: ETSA per protein contents) compared to losing species. We hypothesize that winning species inherently allocate more energy toward inorganic growth (calcification) compared to somatic (tissue) growth. In contrast, we found that losing species that show a higher biomass under reference pCO2 experienced a loss in biomass and variable response in area-specific ETSA that did not translate in an increase in biomass-specific ETSA following either short-term (4–5 months) or even life-long acclimation to elevated pCO2 conditions. Our results suggest that resistance to ocean acidification in corals may not be acquired within a single generation or through the selection of physiologically resistant individuals. This reinforces current evidence suggesting that ocean acidification will reshape coral communities around the world, selecting species that have an inherent resistance to elevated pCO2.

Simplification, not “tropicalization”, of temperate marine ecosystems under ocean warming and acidification

“…Although the drastic decline in calcification rates observed in the laboratory for the fast‐growing coral A. solitaryensis may be overestimated due to the high p CO 2 used in the OAW treatment during the incubation experiment performed in July 2016, the results obtained in the laboratory and field surveys both support the fact that colonization by fast‐growing species such as Acroporids will be limited by ocean acidification and only the slow‐growing coral species, such as Poritids which are already established at these latitudes, could persist under future ocean acidification. These results are similar to observations made under laboratory conditions (Brown & Edmunds, 2016) and at the tropical natural analogues for ocean acidification in Papua New Guinea, where Poritid corals are some of the few corals remaining in acidified areas (Fabricius et al, 2011) demonstrating physiological traits that could contribute to their resistance to OA (Agostini et al, 2021). No difference in the photosynthetic rates was observed for both species of corals between colonies transplanted at the ocean warming alone and the combined warming and acidification analogues.…”

“…We conducted field surveys to characterize the existing coral and kelp communities at these three locations and we carried out transplantation experiments of kelp (to assess herbivory) and of two hermatypic corals (to study their growth, photosystem efficiency and metabolic rates) at these natural analogues for future conditions. One of the coral species, Acropora solitaryensis , represents a fast‐growing, branching species that possesses complex morphology but is vulnerable to OA (Agostini et al, 2021) and has shown a rapid poleward expansion over the last few decades (Yamano et al, 2011). The other species, Porites heronensis , is a slow‐growing, encrusting species that provide relatively low complexity, although it is resistant to OA (Agostini et al, 2021).…”

“…One of the coral species, Acropora solitaryensis , represents a fast‐growing, branching species that possesses complex morphology but is vulnerable to OA (Agostini et al, 2021) and has shown a rapid poleward expansion over the last few decades (Yamano et al, 2011). The other species, Porites heronensis , is a slow‐growing, encrusting species that provide relatively low complexity, although it is resistant to OA (Agostini et al, 2021). We expected that increased temperature would favour the growth and metabolism of corals but that this gain would be negated by combined ocean warming and acidification for the most vulnerable species.…”

Genetic and physiological traits conferring tolerance to ocean acidification in mesophotic corals

“…Different strategies to allocate energy toward skeletal or tissue growth are at the base of the different resistances of corals to acidification (Agostini et al, 2021). Models on tissue physiological processes indicate that, for corals, a thinner tissue layer favors a strong diffusion gradient between the coral epidermis and the water column (Jokiel, 2011; Jokiel et al, 2016).…”

“…Interestingly, mesophotic corals and corals inhabiting naturally acidic areas share some similarities in their physiological traits and gene expression patterns. In fact, corals from both environments possess low tissue biomass (i.e., protein content per coral surface area), which in OA‐resistant species results in a higher potential for energy production (Agostini et al, 2021) and a higher flexibility in allocating energy toward skeletal growth (Agostini et al, 2021; Wall et al, 2017). Moreover, the regulation of the expression of carbonic anhydrases seems to be a crucial mechanism to control inorganic carbon concentrations within cells in both mesophotic corals and corals from naturally acidic areas (Kenkel et al, 2018; Malik et al, 2020; Teixidó et al, 2020).…”