Regulation of ion transport and energy metabolism enables certain coral genotypes to maintain calcification under experimental ocean acidification

Abstract

The ocean absorbs about one-third of anthropogenic carbon dioxide (Sabine et al., 2004), resulting in a decrease in oceanic pH. As pH drops, the concentration of carbonate ions decreases. Together, carbonate ion availability and pH exert a strong influence over the rates of calcification in organisms that use calcite or aragonite for skeletal, test, and shell formation (Georgian, DeLeo, et al., 2016;Melatunan, Calosi, Rundle, Widdicombe, & Moody, 2013;Waldbusser et al., 2015). The aragonite saturation horizon (ASH) is the boundary between waters saturated and undersaturated with respect to aragonite and is a potential boundary between net calcification and net dissolution of coral skeleton. The ASH currently lies between approximately 200 and 2,000 m in the world's ocean . This is deeper than the depth range that corals with photosynthetic symbionts can live, but nearly all cold-water AbstractCold-water corals (CWCs) are important foundation species in the world's largest ecosystem, the deep sea. They support a rich faunal diversity but are threatened by climate change and increased ocean acidification. As part of this study, fragments from three genetically distinct Lophelia pertusa colonies were subjected to ambient pH (pH = 7.9) and low pH (pH = 7.6) for six months. RNA was sampled at two, 4.5, and 8.5 weeks and sequenced. The colony from which the fragments were sampled explained most of the variance in expression patterns, but a general pattern emerged where upregulation of ion transport, required to maintain normal function and calcification, was coincident with lowered expression of genes involved in metabolic processes; RNA regulation and processing in particular. Furthermore, there was no differential expression of carbonic anhydrase detected in any analyses, which agrees with a previously described lack of response in enzyme activity in the same corals. However, one colony was able to maintain calcification longer than the other colonies when exposed to low pH and showed increased expression of ion transport genes including proton transport and expression of genes associated with formation of microtubules and the organic matrix, suggesting that certain genotypes may be better equipped to cope with ocean acidification in the future. While these genotypes exist in the contemporary gene pool, further stresses would reduce the genetic variability of the species, which would have repercussions for the maintenance of existing populations and the ecosystem as a whole. K E Y W O R D S coral, deep sea, ocean acidification, RNAseq, stress response, transcriptomics S U PP O RTI N G I N FO R M ATI O N Additional supporting information may be found online in the Supporting Information section.

Editorial: Fitness of Marine Calcifiers in the Future Acidifying Ocean

“…Although calcifiers can exhibit compensatory responses (e.g., phenotypic plasticity) to counter the impacts of climate change (Leung et al, 2017;Peck et al, 2018;Glazier et al, 2020;Wang et al, 2020), trade-offs against other biological processes are often incurred. For instance, the coral Galaxea fascicularis can accommodate OA by sustaining photosynthetic performance, but the nitrogen fixation machinery is compromised as a trade-off, possibly affecting coral resilience to OA (Zheng et al).…”

Ocean Acidification Mitigates the Negative Effects of Increased Sea Temperatures on the Biomineralization and Crystalline Ultrastructure of Mytilus

“…Here, the notable decreases in shell length and width under the elevated temperature and pCO 2 (20 • C × 1000 ppm) scenario support these previous findings, suggesting depression of some energetically expensive processes (i.e., soft tissue maintenance) and up-regulation of other physiological and biochemical functions. The observed increases in shell length and width under elevated pCO 2 and ambient temperature conditions (17 • C × 1000 ppm) also suggests that mussels may have some capacity to up-regulate biomineralization to maintain or grow shell material under OA (Bibby et al, 2007;Melatunan et al, 2013;Coleman et al, 2014, but see Leung et al, 2020; a process that may be driven by an up-regulation of ion and proton transport genes associated with organic matrix formation (Glazier et al, 2020).…”

“…A link between ultrastructure disruption and reduced expression of calcification proteins under elevated pCO 2 has been proposed (e.g., Huning et al, 2013;Fitzer et al, 2014b), although shell matrix protein candidate genes and the expression of carbonic anhydrase -the latter of which catalyzes the interconversion of bicarbonate and CO 2 -appear less affected by elevated CO 2 (Huning et al, 2013). Furthermore, our understanding of the interaction between protein expression, functioning, and CaCO 3 formation remains limited (see Glazier et al, 2020 for a recent study in corals). A number of models have been proposed including: changes in epitaxial growth, the formation of "mineral bridges" between crystals, or alteration of the c-axis (0001 plane) orientation during the earlier stages of crystal formation (Choi and Kim, 2000;Checa et al, 2006;Fryda et al, 2010;Olson et al, 2013;Maier et al, 2014).…”

Ocean acidification induces distinct transcriptomic responses across life history stages of the sea urchin Heliocidaris erythrogramma

“…Genetic variation that influences gene expression during development could, in principle, provide genotypes that facilitate adaptation to OA in natural populations (Glazier et al., 2020; Goncalves et al., 2016; Pespeni et al., 2013; Runcie et al., 2016). A previous study found that development and settlement success of H. erythrogramma under OA conditions were both strongly influenced by male parent (Foo et al., 2016).…”

“…Genetic variation that influences gene expression during development could, in principle, provide genotypes that facilitate adaptation to OA in natural populations (Glazier et al, 2020;Goncalves et al, 2016;Pespeni et al, 2013;Runcie et al, 2016).…”