Core genes of biomineralization and cis-regulatory long non-coding RNA regulate shell growth in bivalves

Maoxiao Peng; João C R Cardoso; Gareth Pearson; Adelino Vm Canário; Deborah M Power

doi:10.1016/j.jare.2023.11.024

Core genes of biomineralization and cis-regulatory long non-coding RNA regulate shell growth in bivalves

J Adv Res. 2023 Nov 22:S2090-1232(23)00364-8. doi: 10.1016/j.jare.2023.11.024. Online ahead of print.

Authors

Maoxiao Peng¹, João C R Cardoso², Gareth Pearson³, Adelino Vm Canário⁴, Deborah M Power⁵

Affiliations

¹ Comparative Endocrinology and Integrative Biology, Centre of Marine Sciences, Universidade do Algarve, Campus de Gambelas, 8005-139 Faro, Portugal.
² Comparative Endocrinology and Integrative Biology, Centre of Marine Sciences, Universidade do Algarve, Campus de Gambelas, 8005-139 Faro, Portugal. Electronic address: jccardo@ualg.pt.
³ Biogeographical Ecology and Evolution, Centre of Marine Sciences, Universidade do Algarve, Campus de Gambelas, 8005-139 Faro, Portugal.
⁴ Comparative Endocrinology and Integrative Biology, Centre of Marine Sciences, Universidade do Algarve, Campus de Gambelas, 8005-139 Faro, Portugal; International Research Center for Marine Biosciences, Ministry of Science and Technology, Shanghai Ocean University, Shanghai, China; Key Laboratory of Exploration and Utilization of Aquatic Genetic Resources, Ministry of Education, Shanghai Ocean University, Shanghai, China.
⁵ Comparative Endocrinology and Integrative Biology, Centre of Marine Sciences, Universidade do Algarve, Campus de Gambelas, 8005-139 Faro, Portugal; International Research Center for Marine Biosciences, Ministry of Science and Technology, Shanghai Ocean University, Shanghai, China; Key Laboratory of Exploration and Utilization of Aquatic Genetic Resources, Ministry of Education, Shanghai Ocean University, Shanghai, China. Electronic address: dpower@ualg.pt.

PMID: 37995944
DOI: 10.1016/j.jare.2023.11.024

Abstract

Introduction: Bivalve molluscs are abundant in marine and freshwater systems and contribute essential ecosystem services. They are characterized by an exuberant diversity of biomineralized shells and typically have two symmetric valves (a.k.a shells), but oysters (Ostreidae), some clams (Anomiidae and Chamidae) and scallops (Pectinida) have two asymmetrical valves. Predicting and modelling the likely consequences of ocean acidification on bivalve survival, biodiversity and aquaculture makes understanding shell biomineralization and its regulation a priority.

Objectives: This study aimed to a) exploit the atypical asymmetric shell growth of some bivalves and through comparative analysis of the genome and transcriptome pinpoint candidate biomineralization-related genes and regulatory long non-coding RNAs (LncRNAs) and b) demonstrate their roles in regulating shell biomineralization/growth.

Methods: Meta-analysis of genomes, de novo generated mantle transcriptomes or transcriptomes and proteomes from public databases for six asymmetric to symmetric bivalve species was used to identify biomineralization-related genes. Bioinformatics filtering uncovered genes and regulatory modules characteristic of bivalves with asymmetric shells and identified candidate biomineralization-related genes and lncRNAs with a biased expression in asymmetric valves. A shell regrowth model in oyster and gene silencing experiments, were used to characterize candidate gene function.

Results: Shell matrix genes with asymmetric expression in the mantle of the two valves were identified and unique cis-regulatory lncRNA modules characterized in Ostreidae. LncRNAs that regulate the expression of the tissue inhibitor of metalloproteinases gene family (TIMPDR) and of the shell matrix protein domain family (SMPDR) were identified. In vitro and in vivo silencing experiments revealed the candidate genes and lncRNA were associated with divergent shell growth rates and modified the microstructure of calcium carbonate (CaCO₃) crystals.

Conclusion: LncRNAs are putative regulatory factors of the bivalve biomineralization toolbox. In the Ostreidae family of bivalves biomineralization-related genes are cis-regulated by lncRNA and modify the planar growth rate and spatial orientation of crystals in the shell.

Keywords: Bivalve; LncRNA cis-regulation; Mantle transcriptomes; Shell asymmetry; Shell biomineralization toolbox.