Genomic analysis of a scale worm provides insights into its adaptation to deep-sea hydrothermal vents.

Deep-sea polynoid scale worms endemic to hydrothermal vents have evolved an adaptive strategy to the chronic hypoxic environment, but its underlying molecular mechanisms remain elusive. Here, we assembled a chromosome-scale genome of a vent-endemic scale worm Branchipolynoe longqiensis (first annotated genome in the subclass Errantia) and annotated two shallow-water polynoid genomes aiming to elucidate the adaptive mechanisms. We present a genome-wide molecular phylogeny in Annelida and call for extensive taxonomy revision by including more genomes from key lineages. The B. longqiensis genome with a genome size of 1.86 Gb and 18 pseudo-chromosomes is larger than the genomes of two shallow-water polynoids, possibly due to the expansion of various transposable elements (TEs) and transposons. We revealed three inter-chromosomal rearrangements in B. longqiensis when compared to the other two polynoid genomes. The intron elongation and inter-chromosomal rearrangement can influence a number of biological processes, such as vesicle transport, microtubules, and transcription factors. Furthermore, the expansion of cytoskeleton-related gene families may favor the cell structure maintenance of B. longqiensis in the deep ocean. The expansion of synaptic vesicle exocytosis genes has possibly contributed to the unique complex structure of the nerve system in B. longqiensis. Finally, we uncovered an expansion of single-domain hemoglobin and an unique formation of tetra-domain hemoglobin via tandem duplications which may be related to the adaptation to a hypoxic environment.