Extreme mitochondrial genome complexity in the calcaronean sponge <i>Sycon ciliatum</i> (Fabricius, 1780): fragmentation, gene duplication and mRNA editing

Abstract Mitochondrial genomes (mt-genomes) of calcaronean sponges are among the most unusual in Metazoa. They are fragmented into multiple linear chromosomes (mt-chromosomes) and often rely on insertional mRNA editing to generate functional transcripts. These unusual features have precluded complete characterization of calcaronean mt-genomes using short-read sequencing technologies. Here, we assembled and analyzed the mt-genome of Sycon ciliatum (Fabricius, 1780) using HiFi PacBio data generated by the Aquatic Symbiosis Genomics Project. The mt-genome comprised several megabases of sequence distributed across thousands of chromosomes. While most protein-coding genes were preset in multiple copies, three typical animal mitochondrial protein-coding genes (atp8, nad4L and nad6) and multiple tRNA isotypes were not detected, and only short fragments of mt-rRNA genes were identified. We confirmed that mitochondrial mRNA editing in S. ciliatum occurred through single or double uridine insertions at 200+ sites, and that editing patterns were largely predictable from primary sequence motifs. Unexpectedly, editing sites varied among gene copies and were frequently disrupted by point mutations, leading to substantial changes in encoded amino acid sequences. Most mt-chromosomes were associated with repetitive elements that may function in genome maintenance and recombination. Together, our results reveal a distinctive mode of mt-genome evolution and function, shaped by extreme genome fragmentation, extensive gene duplication and pervasive RNA editing. This article is part of the theme issue ‘Evolutionary genetics of mitochondria: on diverse and common evolutionary constraints across eukarya’.