Zhang L et al. , The genome of an apodid holothuroid (Chiridota ...

ECB-ART-50439

Commun Biol null;51:224. doi: 10.1038/s42003-022-03176-4.

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The genome of an apodid holothuroid (Chiridota heheva) provides insights into its adaptation to a deep-sea reducing environment.

Zhang L , He J , Tan P , Gong Z , Qian S , Miao Y , Zhang HY , Tu G , Chen Q , Zhong Q , Han G , He J , Wang M .

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Cold seeps and hydrothermal vents are deep-sea reducing environments that are characterized by lacking oxygen and photosynthesis-derived nutrients. Most animals acquire nutrition in cold seeps or hydrothermal vents by maintaining epi- or endosymbiotic relationship with chemoautotrophic microorganisms. Although several seep- and vent-dwelling animals hosting symbiotic microbes have been well-studied, the genomic basis of adaptation to deep-sea reducing environment in nonsymbiotic animals is still lacking. Here, we report a high-quality genome of Chiridota heheva Pawson & Vance, 2004, which thrives by extracting organic components from sediment detritus and suspended material, as a reference for nonsymbiotic animal's adaptation to deep-sea reducing environments. The expansion of the aerolysin-like protein family in C. heheva compared with other echinoderms might be involved in the disintegration of microbes during digestion. Moreover, several hypoxia-related genes (Pyruvate Kinase M2, PKM2; Phospholysine Phosphohistidine Inorganic Pyrophosphate Phosphatase, LHPP; Poly(A)-specific Ribonuclease Subunit PAN2, PAN2; and Ribosomal RNA Processing 9, RRP9) were subject to positive selection in the genome of C. heheva, which contributes to their adaptation to hypoxic environments.

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	Fig. 1. Collection of C. heheva.a Map showing the sampling site at the Haima cold seep of northern South China Sea (16° 73.228′ N, 110° 46.143′ E). b C. heheva at the sampling site (depth: 1385 m), where they cohabit with deep-sea mussels. C. heheva individuals are indicated by black arrows. Photo by Dr. Jian He.
	Fig. 2. Landscape of transposable elements in echinoderm genomes.a Comparison of the occurrence and composition of repetitive elements in the genomes of 7 echinoderms. b Comparison of the proportion of repetitive elements, retrotransposon, and long interspersed nuclear elements (LINEs) in the genomes of 7 echinoderms. The proportions of repetitive elements and LINEs are higher in the genome of C. heheva than that in other echinoderms. c Transposable element-accumulation profile in C. heheva genome. A recent burst of LINEs was observed in C. heheva.
	Fig. 3. Evolutionary history of C. heheva.a A species tree of 7 echinoderm species. In total, 988 single-copy orthologs were used to reconstruct the phylogenetic tree. The divergence time between species pairs was listed above each node, and 95% confidence interval of the estimated divergence time was denoted as blue bar. The numbers of protein families that were significantly expanded (red) and contracted (blue) (P < 0.05) in each species are denoted beside the species names. b Demographic history of C. heheva (blue) and A. japonicus (red). The changes of ancestral-population size of C. heheva and A. japonicus were inferred using the PSMC method. Time in history was estimated by assuming a generation time of 3 years and a mutation rate of 1.0 × 10−8.
	Fig. 4. Evolutionary relationships among C.heheva NLRs and other representative metazoan NLRs.The unrooted phylogenetic tree was reconstructed based on the NACHT-domain sequences using a maximum-likelihood method. The values near the nodes are ultrafast bootstrap (UFBoot) values. NLRs from different types of species are highlighted by branches of different colors. The species name is shown near the corresponding lineage.
	Fig. 5. Evolutionary relationship with aerolysin-like proteins (ALPs) from C. heheva and other species.The unrooted phylogenetic tree was reconstructed using a maximum-likelihood method. The values near the nodes are ultrafast bootstrap (UFBoot) values. ALPs from different types of species are highlighted by branches of different colors. The species name is shown near the corresponding lineage. ALPs from C. heheva do not cluster with ALPs from other echinoderms (A. japonicus, P. parvimensis), but with the ones from sea anemones (N. vectensis, E. diaphana).
	Fig. 6. A possible amino acid substitution of LHPP that contributed to hypoxic adaptation in C. heheva and cetaceans.The maximum-likelihood phylogenetic tree of cetaceans, C. heheva, and other echinoderms was reconstructed using 598 single-copy orthologs. C. heheva and cetaceans, which are tolerant to hypoxia, have the same amino acid substitution at position 118 of LHPP protein.

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