Shao G et al. (2022), The genome of a hadal sea cucumber reveals nove...

ECB-ART-51139

iScience 2022 Dec 22;2512:105545. doi: 10.1016/j.isci.2022.105545.

Show Gene links Show Anatomy links

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

Shao G , He T , Mu Y , Mu P , Ao J , Lin X , Ruan L , Wang Y , Gao Y , Liu D , Zhang L , Chen X .

???displayArticle.abstract???
How organisms cope with coldness and high pressure in the hadal zone remains poorly understood. Here, we sequenced and assembled the genome of hadal sea cucumber Paelopatides sp. Yap with high quality and explored its potential mechanisms for deep-sea adaptation. First, the expansion of ACOX1 for rate-limiting enzyme in the DHA synthesis pathway, increased DHA content in the phospholipid bilayer, and positive selection of EPT1 may maintain cell membrane fluidity. Second, three genes for translation initiation factors and two for ribosomal proteins underwent expansion, and three ribosomal protein genes were positively selected, which may ameliorate the protein synthesis inhibition or ribosome dissociation in the hadal zone. Third, expansion and positive selection of genes associated with stalled replication fork recovery and DNA repair suggest improvements in DNA protection. This is the first genome sequence of a hadal invertebrate. Our results provide insights into the genetic adaptations used by invertebrate in deep oceans.

???displayArticle.pubmedLink??? 36444293
???displayArticle.pmcLink??? PMC9700323
???displayArticle.link??? iScience

???attribute.lit??? ???displayArticles.show???


	Figure 1. YHSC capture locations, phylogenetic position, and morphology(A) Location of the Yap Trench (left) and the sampling points () on a bathymetric map (right). YAP: Yap Trench; CIR: Caroline Islands Ridge; ST: Sorol Trough; WCR: West Caroline Rise; and PT: Palau Trench.(B) Bayesian inference tree based on three concatenated nuclear genes: 18S rRNA, 28S rRNA, and H3. The numbers at nodes represent the bootstrap scores.(C) Gross morphology of YHSC.
	Figure 2. The adaptive evolution of phospholipids in the cell membrane in the hadal environment(A) Phylogenetic tree constructed by FastTree (version 2.1.11) using the Jones-Taylor-Thorton (JTT) model of amino acid evolution based on protein sequences containing acyl-coenzyme A oxidase N-terminal (Acyl-CoA_ox_N) show that ACOX1 genes, encoding the rate-limiting enzyme in the DHA synthesis pathway, expanded in the YHSC genome.(B) DHA synthesis pathway. The ACOX1 in red refers to expansion in the YHSC genome, while the ACAA1 in green, encoding another rate-limiting enzyme, underwent expansion in the hadal snailfish P. swirei.16(C) DHA content in phospholipids from A. japonicus and the YHSC. ∗∗, p < 0.01 (Student’s t test) Statistical details can be found in the quantification and statistical analysis section.(D) The production of phosphatidylethanolamine (one of the most abundant components of the cell membrane) catalyzed by EPT1. EPT1 is a gene that experienced convergent evolution between the YHSC and P. swirei.(E) Multiple sequence alignment of EPT1. Amino acids unique to the YHSC or P. swirei are indicated by arrows.
	Figure 3. Adaptive changes in translation initiation factors and ribosomal proteins to combat protein synthesis inhibition induced by high pressure and low temperature in the hadal zone(A–C) Phylogenetic trees showing the expansion of genes for the translation initiation factors eIF4G1, eIF2Bδ, and eIF5A in the YHSC genome.(D) Model of the translation initiation pathways.57,58,59,60 Expanded genes are marked in red. (1) eIF2B promotes the exchange of GDP-GTP on eIF2, a rate-limiting step of translation initiation. Then, eIF2-GTP forms a ternary complex (eIF2-GTP-Met-tRNAiMet) together with initiator tRNA (Met-tRNAiMet). (2) The ternary complex was recruited to 40S subunits to form 43S complexes with other factors. (3) The eIF4F complex, consisting of eIF4E, eIF4A, and eIF4G1, bound to mRNA and mediated the unwinding of the mRNA cap-proximal region with the help of eIF4B, and mRNA was activated. (4) 43S complex attached to the activated mRNA and scans the 5′UTR of mRNA to the initiation codon - AUG. (5) eIF5B-mediated ribosomal subunits joining and displacement of translation initiation factors. (6) eEF1A carries aminoacyl-tRNA to the A site of the ribosome.61 (7) eIF5A mediated the formation of the first peptide bond.59,62(E and F) Phylogenetic trees based on protein sequences containing domains of Ribosomal_S5 (E), and Ribosomal_L4 (F) show the expansion of RPS2 and MRPL4 genes in the YHSC genome.(G) Alignment of the amino acid sequence of MRPS27. MRPS27 is a gene that experienced convergent positive selection between the YHSC and P. swirei. Amino acids unique to the YHSC or P. swirei are indicated by arrows.
	Figure 4. Enhanced DNA protection ability of the YHSC for hadal adaptationGenes in red and blue underwent the expansion and positive selection in the YHSC, while genes in green and yellow refer to expanded and positively selected genes in P. swirei.(A–C) Mechanisms for restoring stalled and collapsed replication forks.72,73 Upon encountering obstacles, the replication fork stalled, and the ssDNA is generated and covered by replication protein A (RPA) to avoid secondary structure formation. The stalled fork can be rescued through the fork recovery pathway by activating the downstream effector CHK172 (A) or REV1-mediated translesion synthesis74,75 (B). If the fork is not properly restarted, the replication fork collapses, one-ended double-strand breaks are induced76 and the fork is repaired by homologous recombination72 (C). (A) In the fork recovery pathway, the ssDNA-RPA complex recruits some proteins.72,77 Meanwhile, BRCA2 catalyzes the formation and stabilization of RAD51-ssDNA filaments, which protects nascent DNA from MRE11-mediated nucleolytic degradation.69,78 Then, CHK1 is activated with the help of G2E3,79 and the replication fork restarts after obstacle removal.69,71 (B) In the translesion synthesis pathway, RAD18 and RAD6 interact with the ssDNA-RPA complex and then ubiquitinate proliferating cell nuclear antigen (PCNA).80 REV1, which possesses a high affinity for ubiquitinated PCNA, is recruited to lesions and mediates translesion synthesis by interacting with Polζ and one of the three Y-family polymerases (Polι, Polη, and Polκ), and selecting the polymerases required for translesion synthesis.75,81 (C) In the homologous recombination pathway, the RAD51 filament facilitates strand invasion and homologous recombination after binding with RAD51AP1.72(D) Phylogeny based on proteins containing the BRCA2 repeat domain (BRCA2) showed expansion of BRCA2 in the YHSC genome.(E) A gene tree of G2E3 constructed by Orthofinder (version 2.3.8).(F) Phylogenetic tree based on protein sequences containing DEAD/DEAH box helicases (DEAD). RecQ family labeled with an arc was not further subdivided, as different members could not be distinguished from each other. Nevertheless, 49 genes from the YHSC were annotated as WRN, far more than those from other species.(G) Phylogeny built with proteins containing the impB/mucB/samB family C-terminal domain (IMS_C) showing the expansion of the REV1 gene.(H) Nucleotide excision repair pathway. In the presence of DNA lesions, XPC or RNA Pol II loads TFIIH onto DNA, which is promoted by XPA. Upon detection of a bulky lesion, XPF-ERCC1 and XPG make dual incisions.42(I) Multiple sequence alignment of XPC. XPC underwent convergent positive selection in the hadal YHSC and P. swirei. Amino acids unique to the YHSC or P. swirei are indicated by arrows.

References [+] :

Aertsen, Mrr instigates the SOS response after high pressure stress in Escherichia coli. 2005, Pubmed