Unraveling the microRNA regulatory network underlying the planktonic-to-benthic transition in the Pacific oyster

The Pacific oyster, Crassostrea gigas , undergoes a critical developmental transition from planktonic larvae to sessile benthic juveniles, a process essential for both aquaculture productivity and the stability of marine ecosystems. While environmental and neuroendocrine cues regulating this transition have been extensively studied, the contribution of microRNAs (miRNAs) remains largely unexplored. In this study, we employed a high-resolution temporal sampling strategy to investigate oyster metamorphosis, identified 33 miRNAs associated with larval settlement and metamorphosis. Additionally, we uncovered 35 highly correlated miRNA-target gene pairs, revealing a complex post-transcriptional regulatory network. We further validated the expression pattern of the potential regulatory hub miRNA novel_mir_80 and confirmed its presence through whole-mount in situ hybridization using LNA-modified probes. Functional annotation of target genes highlighted key roles in adhesion, signal transduction, protein homeostasis, cytoskeleton remodeling, genome stability, and transcriptional and epigenetic regulation. These results underscore the pivotal role of miRNAs in orchestrating developmental reprogramming during the planktonic-benthic transition. Our findings not only expand current understanding of miRNA-mediated gene regulation in C. gigas , but also provide novel molecular targets with potential applications in oyster breeding and aquaculture management. • Established an oyster larval planktonic-benthic transition related miRNA database. • Identified 33 miRNAs associated with oyster larval settlement and metamorphosis. • Uncovered 35 miRNA-target pairs revealing post-transcriptional regulatory networks. • Validated the expression pattern of miRNA using LNA-modified probes. • Target genes regulate adhesion, signaling, cytoskeleton, and genome stability.