A near-complete genome assembly of Anomia chinensis provides insights into bivalve phylogenomic evolution and mitochondrial UAA stop-to-Tyr codon reassignment in metazoans

Abstract Background The genetic code is evolutionarily conserved but can undergo lineage-specific alterations. Although mitochondrial UAA stop-to-Tyr codon reassignment has evolved independently in several metazoan lineages, its molecular basis remains poorly understood. As more species are sequenced, an increasing number of UAA stop-to-Tyr codon reassignments are being reported in new metazoan lineages, providing an important opportunity to integrate these cases and explore the molecular basis and evolutionary history of this reassignment. Results We generated a near-complete genome assembly of the cementing bivalve Anomia chinensis , a member of the understudied bivalve superfamily Anomioidea (Bivalvia, Mollusca), comprising 572.90 Mb with a contig N50 of 79.37 Mb and 7 chromosomes. A genome-based phylogeny reconstructed from the major lineages of Pteriomorphia supported that Pectinida is not monophyletic. We also reconstructed the bivalve ancestral linkage groups (BiLGs, n = 20) and performed macrosynteny analysis, which revealed that, within Pteriomorphia, cementing bivalves in the intertidal zone exhibited significantly lower conservation of ancestral karyotypes compared to other groups. Furthermore, we presented the first evidence of mitochondrial UAA stop-to-Tyr codon reassignment in bivalves. We further revealed the genetic basis underlying this reassignment in metazoan mitochondrial genomes, which generally requires the co-evolution of mtRF1a and tRNAs. Conclusions In this study, we provided essential genomic resources for A. chinensis and reconstructed the BiLGs of bivalves, advancing our understanding of bivalve phylogeny and chromosomal macrosynteny evolution. Importantly, the parallel mutations identified in mtRF1a and tRNA Tyr GUA in both hemichordates and mollusks may offer valuable insights into genetic code reprogramming of mitochondria in metazoans, and potentially across a broader range of cellular life.