Abstract
Polynoid scale worms (Polynoidae, Annelida) invaded deep-sea chemosynthesis-based ecosystems approximately 60 million years ago, but little is known about their genetic adaptation to the extreme deep-sea environment. In this study, we reported the first two transcriptomes of deep-sea polynoids (Branchipolynoe pettiboneae, Lepidonotopodium sp.) and compared them with the transcriptome of a shallow-water polynoid (Harmothoe imbricata). We determined codon and amino acid usage, positive selected genes, highly expressed genes and putative duplicated genes. Transcriptome assembly produced 98,806 to 225,709 contigs in the three species. There were more positively charged amino acids (i.e., histidine and arginine) and less negatively charged amino acids (i.e., aspartic acid and glutamic acid) in the deep-sea species. There were 120 genes showing clear evidence of positive selection. Among the 10% most highly expressed genes, there were more hemoglobin genes with high expression levels in both deep-sea species. The duplicated genes related to DNA recombination and metabolism, and gene expression were only enriched in deep-sea species. Deep-sea scale worms adopted two strategies of adaptation to hypoxia in the chemosynthesis-based habitats (i.e., rapid evolution of tetra-domain hemoglobin in Branchipolynoe or high expression of single-domain hemoglobin in Lepidonotopodium sp.).
Highlights
There has been great interest in understanding how animals have adapted to the extreme conditions in these habitats that are characterized by high pressure, darkness, variable temperatures and high concentrations of toxic substances[4,5,6,7,8,9]
To gain insight into the genetic basis of adaptation of deep-sea polynoids to extreme environmental conditions, we sequenced the transcriptomes of B. pettiboneae and Lepidonotopodium sp., and compared them with that of the shallow-water polynoid Harmothoe imbricata, which is in a clade of polynoids that is closest in phylogenetic relationship with all deep-sea polynoids[20]
The cleaned reads were used for the assembly and generated 153,339 contigs for B. pettiboneae, 225,709 contigs for Lepidonotopodium sp. and 98,806 contigs for H. imbricata
Summary
There has been great interest in understanding how animals have adapted to the extreme conditions in these habitats that are characterized by high pressure, darkness, variable temperatures and high concentrations of toxic substances[4,5,6,7,8,9]. More than 120 species in 53 genera of polynoids have been reported from various chemosynthesis-based habitats, including hydrothermal vents, cold seeps, sunken wood and whale carcasses[21,22]. These scale worms are believed to be the descendants of shallow-water species that invaded the deep sea ca. Previous studies have shown that Branchipolynoe spp. have some morphological and molecular adaptations that have allowed them to thrive in the deep-sea chemosynthesis habitats that often experience hypoxia[33,34], making them an excellent model for studies of adaptive evolution Their parapodia bear well-developed arborescent branchiae, which are used to facilitate gaseous exchange with the environment[35]. The findings will help us better understand how animals have adapted to deep-sea extreme environments
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