Role of the bicarbonate transporter SLC4γ in stony-coral skeleton formation and evolution

Abstract

Coral reefs are highly diverse ecosystems of immense ecological, economic, and aesthetic importance built on the calcium-carbonate-based skeletons of stony corals. The formation of these skeletons is threatened by increasing ocean temperatures and acidification, and a deeper understanding of the molecular mechanisms involved may assist efforts to mitigate the effects of such anthropogenic stressors. In this study, we focused on the role of the predicted bicarbonate transporter SLC4γ, which was suggested in previous studies to be a product of gene duplication and to have a role in coral-skeleton formation. Our comparative-genomics study using 30 coral species and 15 outgroups indicates that SLC4γ is present throughout the stony corals, but not in their non-skeleton-forming relatives, and apparently arose by gene duplication at the onset of stony-coral evolution. Our expression studies show that SLC4γ , but not the closely related and apparently ancestral SLC4β , is highly upregulated during coral development coincident with the onset of skeleton deposition. Moreover, we show that juvenile coral polyps carrying CRISPR/Cas9-induced mutations in SLC4γ are defective in skeleton formation, with the severity of the defect in individual animals correlated with their frequencies of SLC4γ mutations. Taken together, the results suggest that the evolution of the stony corals involved the neofunctionalization of the newly arisen SLC4γ for a unique role in the provision of concentrated bicarbonate for calcium-carbonate deposition. The results also demonstrate the feasibility of reverse-genetic studies of ecologically important traits in adult corals.

Photosynthesis and other factors affecting the establishment and maintenance of cnidarian–dinoflagellate symbiosis

“…Given that algal loss under these conditions is a slow process that spans months (see Results), further careful research will be needed to determine whether it represents an active expulsion process or simply host-cell renewal in the absence of algal proliferation. In addition, answering questions about the determinants of initial algal uptake will depend both on a clear understanding of the precise stage(s) at which the discrimination among particular strains actually takes place (which will require additional experimentation at the level of resolution used here) and on the application of genetic methods [101,102] to test rigorously whether particular molecules and interactions really have the roles proposed for them. Among the high-priority targets for gene knockdowns or knockouts are the glucose transporter GLC8 [7,47,49,86] and the sterol transporter NPC2 [11,47].…”

Clustered Regularly Interspaced Short Palindromic Repeat/CRISPR-Associated Protein and Its Utility All at Sea: Status, Challenges, and Prospects

“…Meanwhile, to investigate the effects of heat stress and acidification on the calcium carbonate skeletons of stony corals, CRISPR/Cas9 was used to mutate SLC4γ (bicarbonate transporter) in A. millepora juveniles. The results showed defective skeleton formation, manifesting the essential role of SLC4γ on skeleton formation in young coral colonies [ 240 ]. In addition, in the early-branching metazoan Nematostella vectensis , the native red fluorescent protein gene ( NvFP-7R ) was successfully disrupted using CRISPR/Cas9 through the use of microinjection [ 241 ].…”

Microinjection, gene knockdown, and CRISPR-mediated gene knock-in in the hard coral,Astrangia poculata

“…Recent advances in the techniques available for genetic manipulation have enabled the ability to perturb and analyze gene function in a broad range of animal phyla (Crawford et al, 2020; Oulhen et al, 2022; Presnell and Browne, 2021; Tinoco et al, 2023). These advancements make it possible to interrogate the evolution of development in taxa representing extreme variation in animal body plans.…”