The genome of a hadal sea cucumber reveals novel adaptive strategies to deep-sea environments

Shao, Guangming; He, Tianliang; Mu, Yinnan; Mu, Pengfei; Ao, Jingqun; Lin, Xihuang; Ruan, Lingwei; Wang, YuGuang; Gao, Yuan; Liu, Dinggao; Zhang, Liangsheng; Chen, Xinhua

doi:10.1016/j.isci.2022.105545

Cited by 10 publications

(14 citation statements)

References 142 publications

(240 reference statements)

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“…Yap genome helped to identify the potential adaptation mechanisms of these animals to the deep-sea habitat. The authors found in this species an expansion and a positive selection for genes such as translation initiation factors, ribosomal proteins, and genes associated with DNA repair, suggesting that increased protein synthesis inhibition coupled with DNA protection are necessary for deep-sea species adaptation [ 135 ]. The sequencing of C. heheva genome, another deep-sea species, showed an expansion of the aerolysin-like protein family (pore-forming proteins mostly studied in bacteria and able to damage membranes of target cells generating transmembrane pores) and a positive selection of several hypoxia-related genes, suggesting an important contribution of these genes to hypoxic environment adaptation [ 172 ].…”

Section: Genomic-transcriptomic Information and Cellular And Molecula...mentioning

confidence: 99%

Sea cucumbers: an emerging system in evo-devo

Perillo,

Sepe,

Paganos

et al. 2024

EvoDevo

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A challenge for evolutionary developmental (evo-devo) biology is to expand the breadth of research organisms used to investigate how animal diversity has evolved through changes in embryonic development. New experimental systems should couple a relevant phylogenetic position with available molecular tools and genomic resources. As a phylum of the sister group to chordates, echinoderms extensively contributed to our knowledge of embryonic patterning, organ development and cell-type evolution. Echinoderms display a variety of larval forms with diverse shapes, making them a suitable group to compare the evolution of embryonic developmental strategies. However, because of the laboratory accessibility and the already available techniques, most studies focus on sea urchins and sea stars mainly. As a comparative approach, the field would benefit from including information on other members of this group, like the sea cucumbers (holothuroids), for which little is known on the molecular basis of their development. Here, we review the spawning and culture methods, the available morphological and molecular information, and the current state of genomic and transcriptomic resources on sea cucumbers. With the goal of making this system accessible to the broader community, we discuss how sea cucumber embryos and larvae can be a powerful system to address the open questions in evo-devo, including understanding the origins of bilaterian structures.

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Section: Genomic-transcriptomic Information and Cellular And Molecula...mentioning

confidence: 99%

Sea cucumbers: an emerging system in evo-devo

Perillo,

Sepe,

Paganos

et al. 2024

EvoDevo

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“…Compared with other echinoderms ( Supplemental Table S3 ), the repetitive gene percentage of C. heheva (Kairei vent) in this study is more than that in the Haima cold seep (56.64%) [ 21 ] and only less than that of Paelopatides sp. Yap (73.93%) [ 23 ], and the percentage of shallow water A. japonicus is only 27.20% [ 55 , 64 ]. After repeat masking, protein-coding genes annotated used a combination of ab initio , homology-based, and transcript evidence–predicted approaches, and a total of 32,434 were successfully identified (Table 3 ).…”

Section: Resultsmentioning

confidence: 99%

“…Phospholipids, with a hydrophilic phosphate group head and hydrophobic fatty acid tails, constitute a significant component that forms the lipid bilayers [ 71 ]. Changes in lipid composition modulate membrane fluidity, especially the proportion of unsaturated fatty acids [ 19 , 23 , 70–72 ]. In our results, lipid metabolisms were activated to respond to high hydrostatic pressure, including essential fatty acids of arachidonic acid (AA) metabolism, linoleic acid (LA) metabolism, alpha-linolenic acid (ALA) metabolism, and so on (Fig.…”

Section: Resultsmentioning

confidence: 99%

“…Among various deep-sea fauna, DNA repair, degenerated ossicles, protein activity protection, and cell cycle maintenance have evolved to high hydrostatic pressure adaptation [ 5 , 19–21 ]. The white body color, unpigmented skin, scales, and long-wavelength light sensors of marine fauna were ubiquitous in the light-limited deep sea [ 6 , 19 , 20 , 22 , 23 ]. Gathering knowledge about the genetic basis of adaptation to deep-sea extreme environments is particularly interesting.…”

Section: Data Descriptionmentioning

confidence: 99%

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A high-quality chromosomal genome assembly of the sea cucumber Chiridota heheva and its hydrothermal adaptation

Pu,

Zhou,

Liu

et al. 2024

GigaScience

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Background Chiridota heheva is a cosmopolitan holothurian well adapted to diverse deep-sea ecosystems, especially chemosynthetic environments. Besides high hydrostatic pressure and limited light, high concentrations of metal ions also represent harsh conditions in hydrothermal environments. Few holothurian species can live in such extreme conditions. Therefore, it is valuable to elucidate the adaptive genetic mechanisms of C. heheva in hydrothermal environments. Findings Herein, we report a high-quality reference genome assembly of C. heheva from the Kairei vent, which is the first chromosome-level genome of Apodida. The chromosome-level genome size was 1.43 Gb, with a scaffold N50 of 53.24 Mb and BUSCO completeness score of 94.5%. Contig sequences were clustered, ordered, and assembled into 19 natural chromosomes. Comparative genome analysis found that the expanded gene families and positively selected genes of C. heheva were involved in the DNA damage repair process. The expanded gene families and the unique genes contributed to maintaining iron homeostasis in an iron-enriched environment. The positively selected gene RFC2 with 10 positively selected sites played an essential role in DNA repair under extreme environments. Conclusions This first chromosome-level genome assembly of C. heheva reveals the hydrothermal adaptation of holothurians. As the first chromosome-level genome of order Apodida, this genome will provide the resource for investigating the evolution of class Holothuroidea.

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“…These habitats provide a dramatically different ecological niche from those that rely on photosynthesis for primary production, and as such provide us with very distinctive ecological and evolutionary systems to those commonly studied. Our knowledge of metazoan genomic adaptations to these extreme environments has mainly derived from genome analyses of annelids [1], crustaceans [2], molluscs [3][4][5][6][7], echinoderms [8,9] and fishes [10][11][12]. The phylum Cnidaria contains over 10 000 species of animals including sea anemones, corals and jellyfishes, and its members play important ecological roles in both shallow-water and deep-sea habitats throughout the world.…”

Section: Introductionmentioning

confidence: 99%

The genome of the deep-sea anemone Actinernus sp. contains a mega-array of ANTP-class homeobox genes

Law,

Yu,

Nong

et al. 2023

Proc. R. Soc. B.

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Members of the phylum Cnidaria include sea anemones, corals and jellyfish, and have successfully colonized both marine and freshwater habitats throughout the world. The understanding of how cnidarians adapt to extreme environments such as the dark, high-pressure deep-sea habitat has been hindered by the lack of genomic information. Here, we report the first chromosome-level deep-sea cnidarian genome, of the anemone Actinernus sp., which was 1.39 Gbp in length and contained 44 970 gene models including 14 806 tRNA genes and 30 164 protein-coding genes. Analyses of homeobox genes revealed the longest chromosome hosts a mega-array of Hox cluster, HoxL, NK cluster and NKL homeobox genes; until now, such an array has only been hypothesized to have existed in ancient ancestral genomes. In addition to this striking arrangement of homeobox genes, analyses of microRNAs revealed cnidarian-specific complements that are distinctive for nested clades of these animals, presumably reflecting the progressive evolution of the gene regulatory networks in which they are embedded. Also, compared with other sea anemones, circadian rhythm genes were lost in Actinernus sp., which likely reflects adaptation to living in the dark. This high-quality genome of a deep-sea cnidarian thus reveals some of the likely molecular adaptations of this ecologically important group of metazoans to the extreme deep-sea environment. It also deepens our understanding of the evolution of genome content and organization of animals in general and cnidarians in particular, specifically from the viewpoint of key developmental control genes like the homeobox-encoding genes, where we find an array of genes that until now has only been hypothesized to have existed in the ancient ancestor that pre-dated both the cnidarians and bilaterians.

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The genome of a hadal sea cucumber reveals novel adaptive strategies to deep-sea environments

Cited by 10 publications

References 142 publications

Sea cucumbers: an emerging system in evo-devo

Sea cucumbers: an emerging system in evo-devo

A high-quality chromosomal genome assembly of the sea cucumber Chiridota heheva and its hydrothermal adaptation

The genome of the deep-sea anemone Actinernus sp. contains a mega-array of ANTP-class homeobox genes

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