nucleotide-binding oligomerization domain-like receptors; PMC, Blue circles stand for the genes encoding ribosomal proteins, which are commonly considered as highly expressed proteins. Clean reads were mapped to genome scaffolds by the Burrows-Wheeler Aligner [69]. Of even greater interest is the fact that sea cucumbers display a capacity to regrow body parts and internal organs [3], which is much greater than that of sea stars and sea urchins, making them prime regeneration models. Echinodermata, an ancient phylum of marine invertebrates, comprises 5 extant classes, including Echinoidea (sea urchins), Asteroidea (sea stars), Holothuroidea (sea cucumbers), Ophiuroidea (brittle stars), and Crinoidea (sea lilies). Compared to S. purpuratus and A. planci, A. japonicus has a similar average exon size (193.43 bp) and exon number per gene (6.1), but it has a shorter intron size (1,319 bp on average) than S. purpuratus (S5 Fig and S9 Table). Writing – original draft, Roles Moreover, most of the miRNAs are distributed across the genome in clusters (12 clusters), in which 2 or more miRNAs are located in physically adjacent regions, indicating possible cotranscription and functional cooperation (Fig 1). Image credits: "Introduction to zoology; a guide to the study of animals, for the use of secondary schools" (1900) Macmillan; Freshwater and Marine Image Bank; Encyclopædia Britannica; Jerry Kirkhart; authors' own; public domain; Freshwater and Marine Image Bank; National Oceanic and Atmospheric Administration; Martin Cooper. Reads for 26.01 Gb of clean data were split into k-mers, and k-mer depth was computed to obtain depth distribution. The 137 miRNAs can be clustered into 76 families, including 39 conserved and 37 novel families, among which miR-92 (with 12 copies) was the most abundant. No, PLOS is a nonprofit 501(c)(3) corporation, #C2354500, based in San Francisco, California, US,,,,,,,,, Writing – original draft, Affiliations Visualization, Roles RepeatModeler ( was used for repeat family identification in a de novo approach. CAI, They were held in a laboratory for 1 week in sea water at 15–17°C and fed once a day. The Hox gene cluster, Hox1 to Hox11/13c, spanned approximately 940 Kb, which is similar to reports from acorn worms (S. kowalevskii and Ptychodera flava, approximately 500 Kb) [31], sea urchin (S. purpuratus, 588 Kb) [32], and sea star (A. planci, 1,195Kb) [33]. Mo, J. et al, PNAS, October 5, 2016., Shihao Li, Roles extracellular matrix; FALCON, Main Characteristics. Visualization, Roles Received by JX and XZ. Two conserved gene clusters related to pharyngeal gill slit development (pax1/9~foxA and six6~six4) showed strong synteny within deuterostomes [24], whereas they were incomplete and showed poor synteny within nondeuterostomes (Fig 3C and S10 Fig). For each gene family, protein sequences from all represented sequenced genomes were searched using BLASTP (E-value cutoff 1.00E-10) against unigenes from each species. Relatives of Sea Stars, Sand Dollars, and Urchins. Methods and Resources The transcriptome data revealed that most biomineralization genes were highly expressed in S. purpuratus from the blastula (embryo) through the pluteus (larva) stages, whereas the 7 corresponding biomineralization genes in A. japonicus showed relatively lower expression levels in these developmental stages (Fig 5C). GO enrichment analyses of the A. japonicus-specific genes and significantly expanded gene families suggested that most genes were associated with GO terms in cellular process, metabolic process, and binding and catalytic activity (S6 and S8 Figs). Among them, 43 single-copy genes were used for phylogenetic tree construction. The corresponding expression information for 4 biomineralization genes was obtained from A. japonicus developmental transcriptomes. Track 5: distribution of microRNA (miRNA) in the genome. Moreover, the multiomics data will be of prime value for commercial sea cucumber breeding programs. A total of 3,821 scaffolds were assembled with an N50 length of 486 Kb, and approximately 90% of the total assembled genome consisted of the 1,779 longest scaffolds (Table 1 and S5 Table). Mo, J. et al, PNAS, October 5, 2016. small nucleolar RNA; snRNA, Most genes are enriched in GO terms of cellular process, metabolic process, binding, and catalytic activity. However, Hox4 is lost in S. purpuratus [32] whose Hox6 was highly homologous to A. planci Hox4, suggesting that these 2 genes may have the same ancestral origin. The GO terms with a light green background are associated with immunity, and those with a yellow background are associated with signal recognition. brachury and FGF9 showed high expression levels at the stages of gastrula, doliolaria, and pentactula. e2003790. 95 ($12.48/Fl Oz) Yes The animal material for genome sequencing and assembly was from a male A. japonicus captured off the coast of Laoshan, Qingdao, China. The genes whose identity has been confirmed are in a dark rectangle, whereas those cases not yet confirmed are in a lighter rectangle. The scale covers log expression values. This phylum is divided into five extant classes: Asteroidea (sea stars), Ophiuroidea (brittle stars), Echinoidea (sea urchins and sand dollars), Crinoidea (sea lilies or feather stars), and Holothuroidea (sea cucumbers) (Figure 2). European Synchrotron Radiation Facility - 71, avenue des Martyrs, CS 40220, 38043 Grenoble Cedex 9, France. Using PhyML [95], we performed ML analysis with the substitution model WAG + gamma + Inv, and 1,000 bootstraps were conducted to produce the branch support values. All species of sea cucumber breathe by dilating their anal sphincter to suck water into their rectum, where specialized structures called respiratory trees — butt lungs — extract oxygen molecules from the water. The genome data supported these characteristics. Total RNA was extracted using the TRIzol extraction method (Thermo Fischer Scientific, Germany) according to the manufacturer’s protocol. Data curation, In the A. japonicus genome, we found a single, substantially intact, and well-ordered Hox gene cluster containing 10 Hox genes, as well as a conserved ParaHox gene cluster (Fig 4) and large numbers of other homeobox genes (S17 Table). Sea Cucumber Alcohol-Free Liquid Extract, Sea Cucumber (Cucumaria Frondosa) Glycerite Natural Herbal Supplement, Hawaii Pharm, USA 2 fl.oz 4.1 out of 5 stars 17 $24.95 $ 24 . Of the 248 conserved core eukaryotic genes used for assessing the genome completeness, 242 genes (97.6%) were covered by the genome (S7 Table). in-situ hybridization; iTRAQ, No, Is the Subject Area "Sea cucumbers" applicable to this article? The funders had no role in study design, data collection and analysis, decision to publish, or preparation of the manuscript. Supervision, The amino acid sequence alignment and domain prediction of proteins coded by these PSP94-like genes show highly conserved cysteine residues in the PSP94 domain. Formal analysis, Sea cucumber adults exhibit an elongated shape that belies their pentaradial symmetry, combined with weak calcification in the form of microscopic ossicles that contrasts with the solid calcified test of sea urchins. A neighbor-joining phylogeny was reconstructed using MEGA (v5) [90]. After digestion, peptides were dried by vacuum centrifugation, reconstituted in 0.5 mol/L TEAB, and processed according to the manufacturer’s protocol for 8-plex iTRAQ reagent (Applied Biosystems, Foster City, California, US). These could be useful in flexible scaffolds for tissue engineering, cosmetic treatments against skin ageing, implantable biosensors, and materials for soft robotics.”. gene ontology; iPS, Over 94% of reads from the Illumina short-insert library could be successfully mapped to the genome; moreover, over 97% of transcriptome unigenes were mapped to the assembly, and over 93% of unigenes were covered by a single scaffold at half length (50% in 1 scaffold) (S6 Table), reflecting the high integrity and accuracy of the assembly. Funding acquisition, A homeodomain of Hox2 was found between Hox1 and Hox3 in the A. japonicus Hox cluster, but its gene structure was not intact. Together, the phyla Echinodermata, Hemichordata, and Chordata form the deuterostome clade, based on their closely shared developmental features. These data provided an important resource for sea cucumber genomics, but their incompleteness and fragmentation limit applications for research. Codon usage analysis indicated that these genes had high codon adaptive index (CAI) values like ribosomal protein-coding genes, suggesting they are highly expressed genes performing an important function (S16 Fig). These genes are all present in deuterostomes, but some of them are present in nondeuterostomes. This result confirmed the effectiveness of the approaches and the superiority of PacBio long reads for large genome assembly (S2 Table). Extinction and evolution of gene families were processed by CAFE, using a random birth and death process model to identify gene gain and loss along each lineage of the RAxML tree (Fig 2). The divergence times were estimated and displayed below the phylogenetic tree. However, some crucial genes related to central nervous system development were absent in A. japonicus, S. purpuratus, and A. planci, including hunchback, vax, sax7, pax2, gfap, krox20, L-fng, Gli, and pax3/7 (S2 Data), suggesting that all echinoderms have a similar genomic comparison and an absence of central nervous system genes. Among the 30,350 protein-coding genes of A. japonicus, many-to-many orthologs (15.38%), patchy orthologs (36.44%), and species-specific genes (43.17%) were 3 major gene model groups (Fig 2C). Single Molecule Real Time; SOAPdenovo, Conceptualization, Supervision, Reporting in the journal Proceedings of the National Academy of Sciences, the QMUL team analysed the body wall of sea cucumbers at the ESRF. Furthermore, we found that most marker genes associated with notochord formation and gill slit development (e.g., brachyury, β-catenin, foxA, and otx) were commonly present in echinoderms, whereas some of them were absent in the nondeuterostome species (Fig 3A and 3C). Transcriptome data for the 3 echinoderms were assembled into unigenes using Trinity and cap3 with default parameters [91,92]. Laboratory for Marine Biology and Biotechnology & Marine Ecology and Environmental Science, Qingdao National Laboratory for Marine Science and Technology, Qingdao, China, Roles The orthologs of the 4 key pluripotency factors in A. japonicus were SoxB1 (AJAP16673), Myc (AJAP11986), Oct1/2/11 (AJAP10188), and Klf1/2/4 (AJAP08993). RNA expression analysis was based on the predicted genes of A. japonicus genome. Target indicates the genome of A. japonicus; H0.01–H0.06 indicate the simulated genome with heterozygosity of 1%–6%, respectively. The data underlying Fig 6B and 6C can be found in S3 Data. Five 10-Kb SMRTbell libraries were prepared and sequenced using the C4 sequencing chemistry and P6 polymerase. Raw sequencing data of transcriptomes have been deposited in NCBI under the accession number SRR5083072-SRR5083088. For gene functional prediction, NCBI nr and the SwissProt database were used for gene blasts. small nuclear RNA; TAI, Relieve arthritis and joint pain. Data Availability: The sea cucumber genome project has been deposited at NCBI under the accession number PRJNA354676. (A) Regeneration diagram showing A. japonicus (a) undergoing evisceration, (b) immediately post evisceration, and (c) after complete recovery. Another cluster with 21 tandem-duplicated FREP genes was located on Scaffold75. Corresponding proteomic studies (3, 5, 7, 14, and 21 dpe) of intestinal regeneration were analyzed using isobaric tags for relative and absolute quantitation (iTRAQ) coupled with mass spectrometry (MS). It has relatively intact skeletogenic signal pathways, key transcription factors, and important skeletogenesis-related genes (e.g., otx, soxB, ets1, alx1, dlx, runx2, snail, and twist) (S18 Table). In-situ hybridization (ISH) results showed that brachury specifically expressed around the mouth (S12 Fig), which was similar to reports from other echinoderms [26]; however, it was different from chordates, whose brachury expressed along the notochord [25]. Sea Cucumber Behavior. The LC-ESI-MS/MS analysis was based on Triple TOF 5600 (AB SCIEX, Ontario, Canada). These FREPs were significantly up-regulated during the early and middle stages of visceral regeneration at mRNA and protein levels (S15 Fig and S21 Table). Software, The gene ratios in each GO term are compared between the significantly expanded and full protein-coding genes of the genome. Investigation, In early 2017, a draft genome of A. japonicus was published that represented only about 80.5% of the estimated genome size (0.82 Gb), with scaffolds N50 value of 10.5 Kb [14]. The tensile strain is applied along the vertical direction. In this study, we report an analysis of body wall metabolites of the sea cucumber (A. japonicus) from different geographical origins in Dalian, Pikou, Jinzhou and Rushan using ultra-high performance liquid chromatography–quadrupole time-of-flight mass spectrometry (UPLC–Q-TOF/MS). codon adaptive index; CARD, Fast & Free shipping on many items! Clean sRNA reads were compared with the Rfam database ( to exclude noncoding RNAs other than miRNAs. Department of Ocean Sciences, Memorial University, St. John's, Newfoundland, Canada, Roles induced pluripotent stem; ISH, Investigation, (A) A heatmap showing the expression profile of tandem-duplicated gene clusters during the intestinal regeneration of A. japonicus. Using tubulin expression as the control, the biomineralization genes showed significantly lower expression in A. japonicus than S. purpuratus (Fig 3F). Writing – original draft, Roles Most of these biomineralization genes (Sm30 and Sm50) encode spicule matrix proteins that mediate the deposition of the initial calcite crystal granules [39,40]; the others encode collagens (colp3a), the mesenchyme-specific cell surface protein (Msp130), and the primary mesenchyme cell (PMC) specific carbonic anhydrase (can1) [41]. However, the gene order of Hox clusters in A. japonicus was similar to that of A. planci and different from that of S. purpuratus, whose anterior class genes (Hox1, Hox2, and Hox3) were inverted and translocated to the end of the cluster because of genomic rearrangement (Fig 4) [32]. Data curation, The 5 gene families are fibrinogen-related proteins (FREPs) (F), retrovirus-related Pol polyprotein from transposon (R), nucleotide-binding oligomerization domain-like receptors (NLR) family caspase recruitment domain (CARD) domain-containing protein (N), tyrosine-protein kinase receptor (T), and zinc finger CysCysHisCys (CCHC) domain-containing protein (Z). Showing page 1. Sequencing depth averaged 50-fold for parents and 10-fold for the 130 offspring. Sea cucumbers can rapidly change the stiffness of their body, and scientists from Queen Mary University of London (QMUL) have discovered for the first time how they do it using data collected at ESRF. Investigation, The stomochord was considered as the supporting organ of hemichordates, even though no molecular evidence of homology has been detected between stomochord and notochord [28,29]. Genome size and N50 of assembled contigs were calculated and used for performance evaluation (S1 Fig). To extend the taxonomic sampling, gene families were surveyed in transcriptome datasets in F. serratissima, Patiria miniata, and A. filiformis (NCBI SRA database accession numbers SRR2454338, SRR573710, SRR573709, SRR573708, SRR573706, SRR573707, SRR573705, SRR573675, SRR1523743, SRR1533125, SRR794587, SRR794568, SRR789489, and SRR3097584). The data are expressed as mean ± SD after normalization. The genes of A. japonicus are shown in red, and the genes of other species are shown in different colors: Homo sapiens (green); Anolis carolinensis (purple); Chrysemys picta (khaki); Danio rerio (blue); Xenopus tropicalis (gray); Ciona intestinalis (black); Branchiostoma floridae (royal purple); Saccoglossus kowalevskii (dark green); Strongylocentrotus purpuratus (pink); Crassostrea gigas (cyan); Nematostella vectensis (yellow); Helobdella robusta (buff); Drosophila melanogaster (tan); and Octopus bimaculoides (orange). Johnsons sea cucumber, an echinoderm, has a long, tube-like, almost cylindrical soft body which like its echinoderm relatives, sea stars, sea urchins, and sand dollars, exhibits five-part symmetry. Eleven PSP94-like genes are tandemly arranged on Scaffold889. Variants including SNPs were identified using SAMtools [70]. Cufflinks (version 2.1.1) ( was used to identify spliced transcripts in gene models [83]. Besides, FGF has been found to regulate skeleton morphogenesis in sea urchins, but it lost the regulatory function on brachyury expression [27]. However, FGF gene families contracted significantly in echinoderms, such that only 1 FGF gene (fgf8) exists in A. japonicus, S. purpuratus, and A. planci (Fig 3B). To further test if foxE was absent in echinoderms, we compared S. kowalevskii fox genes against the draft assembly of other echinoderms from NCBI, including sea urchin Lytechinus variegates (AGCV00000000.2), sea cucumber Parastichopus parvimensis (JXUT00000000.1), brittle star Ophiothrix spiculata (JXSR00000000.1), and sea star P. miniata (AKZP00000000.1). In order to get the best assembly results, we tried Short Oligonucleotide Analysis Package de novo assembly tool (SOAPdenovo) [64], de Bruijn graph to Overlap-Layout-Consensus (DBG2OLC) (, FALCON (, and SMARTdenovo ( Here we present the complete genome sequence of an economically important sea cucumber, A. japonicus, generated using Illumina and PacBio platforms, to achieve an assembly of approximately 805 Mb (contig N50 of 190 Kb and scaffold N50 of 486 Kb), with 30,350 protein-coding genes and high continuity. We found a Hox gene cluster containing 10 conserved Hox genes in the A. japonicus genome. Validation, Peptide sequences were clustered by the Markov clustering program orthoMCL [89]. The draft scaffolds of 4 echinoderm genomes were blasted against the Fox gene family, and the homologous regions were extracted to blast against the nr database. They are marine animals with a leathery skin and an elongated body containing a single, branched gonad. $88.00. To obtain an exact heterozygous rate, we used the software gce to analyze k-mer frequency data with parameters of -c unique_depth -H 1 ( Marker genes associated with the notochord and gill slits were also found, providing valuable insight into the origin of chordates. (A) Phylogenetic placement of A. japonicus within the metazoan tree. For reads with multiple mapping positions, only the single best hit was retained. (B) Plot of CAI against the effective number of codons (Nc). Finally, sea cucumbers, like many echinoderms, can be extremely long-lived and somewhat immune to senescence [6,7]. Homologous proteins from 8 known whole genome sequences Homo sapiens, Danio rerio, B. floridae, S. kowalevskii, S. purpuratus, Daphnia pulex, C. gigas, and Hydra vulgaris were used for alignment to the repeat-masked A. japonicus genome using Exonerate (version 2.2.0) [79]. Unlike hemichordates and chordates, adult echinoderms lack the ancestral deuterostome characters of gill slits and notochord. Among them, cytochrome P450 family 2 (CYP2) was a major gene family that was significantly expanded in A. japonicus and S. purpuratus (S7 Fig). Apart from sharing common ancestry with chordates, sea cucumbers exhibit a unique morphology and exceptional regenerative capacity. Methodology, Adults of A. japonicus (100–120 g) were collected from the coast of Qingdao, Shandong Province. Investigation, Fast Alignment and Consensus for Assembly; FGF, Credits: Maxim Gavrilyuk. 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