The draft genome of the tropical sea cucumber Stichopus monotuberculatus (Echinodermata, Stichopodidae) reveals critical genes in fucosylated chondroitin sulfates biosynthetic pathway.
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ABSTRACT:
SUBMITTER: Zhong S
PROVIDER: S-EPMC10213396 | biostudies-literature | 2023
REPOSITORIES: biostudies-literature
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The draft genome of the tropical sea cucumber <i>Stichopus monotuberculatus</i> (Echinodermata, Stichopodidae) reveals critical genes in fucosylated chondroitin sulfates biosynthetic pathway.
Zhong Shengping S Ma Xiaowan X Jiang Yan Y Liu Xujia X Zeng Mengqing M Zhao Longyan L Huang Lianghua L Huang Guoqiang G Zhao Yongzhen Y Qiao Ying Y Chen Xiuli X
Frontiers in genetics 20230512
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Project description:Fucosylated chondroitin sulfates are complex polysaccharides extracted from sea cucumber. They have been extensively studied for their anticoagulant properties and have been implicated in other biological activities. While nuclear magnetic resonance spectroscopy has been used to extensively characterize fucosylated chondroitin sulfate oligomers, we herein report the first detailed mass characterization of fucosylated chondroitin sulfate using high-resolution Fourier transform ion cyclotron resonance mass spectrometry. The two species of fucosylated chondroitin sulfates considered for this work include Pearsonothuria graeffei (FCS-Pg) and Isostichopus badionotus (FCS-Ib). Fucosylated chondroitin sulfate oligosaccharides were prepared by N-deacetylation-deaminative cleavage of the two fucosylated chondroitin sulfates and purified by repeated gel filtration. Accurate mass measurements obtained from electrospray ionization Fourier transform ion cyclotron resonance mass spectrometry measurements confirmed the oligomeric nature of these two fucosylated chondroitin sulfate oligosaccharides with each trisaccharide repeating unit averaging four sulfates per trisaccharide. Collision-induced dissociation of efficiently deprotonated molecular ions through Na/H+ exchange proved useful in providing structurally relevant glycosidic and cross-ring product ions, capable of assigning the sulfate modifications on the fucosylated chondroitin sulfate oligomers. Careful examination of the tandem mass spectrometry of both species deferring in the positions of sulfate groups on the fucose residue (FCS-Pg-3,4- OS) and (FCS-Ib-2,4- OS) revealed cross-ring products 0,2Aαf and 2,4X2αf which were diagnostic for (FCS-Pg-3,4- OS) and 0,2X2αf diagnostic for (FCS-Ib-2,4- OS). Mass spectrometry and tandem mass spectrometry data acquired for both species varying in oligomer length (dp3-dp15) are presented.
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Project description:Morphologically cryptic and pseudo-cryptic species pose a challenge to taxonomic identification and assessments of species diversity and distributions. Such is the case for the sea cucumber Stichopus horrens, commonly confused with Stichopus monotuberculatus. Here, we used mitochondrial cytochrome oxidase subunit I (COI) and microsatellite markers to examine genetic diversity in Stichopus cf. horrens throughout the Philippine archipelago, to aid species identification and clarify species boundaries. Phylogenetic analysis reveals two recently diverged COI lineages (Clade A and Clade B; c. 1.35-2.54 Mya) corresponding to sequence records for specimens identified as S. monotuberculatus and S. horrens, respectively. Microsatellite markers reveal two significantly differentiated genotype clusters broadly concordant with COI lineages (Cluster 1, Cluster 2). A small proportion of individuals were identified as later-generation hybrids indicating limited contemporary gene flow between genotype clusters, thus confirming species boundaries. Morphological differences in papillae distribution and form are observed for the two species, however tack-like spicules from the dorsal papillae are not a reliable diagnostic character. An additional putative cryptic species was detected within Clade B-Cluster 2 specimens warranting further examination. We propose that these lineages revealed by COI and genotype data be referred to as Stichopus cf. horrens species complex.
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Project description:The sea cucumber, Stichopus monotuberculatus, is an economically important holothuroid in China due to its larger body size and valuable nutrition. However, the taxonomic revision studies of Stichopodidae have been one of the most controversial issues in recent years. Moreover, there remain considerable doubts about a complex of cryptic species within S. monotuberculatus. In this study, we report the complete mitochondrial genome of S. monotuberculatus. The mitogenome has 16,274 base pairs (60.4% A + T content) and made up of total of 37 genes (13 protein-coding, 22 transfer RNAs and 2 ribosomal RNAs), and a putative control region. This study adds one more available complete mitogenomes of Stichopus and will provide useful genetic information for future evolutionary and taxonomic classification of Stichopodidae.
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Project description:Fucosylated chondroitin sulfate (fCS) extracted from the sea cucumber Holothuria forskali is composed of the following repeating trisaccharide unit: → 3)GalNAcβ4,6S(1 → 4) [FucαX(1 → 3)]GlcAβ(1 →, where X stands for different sulfation patterns of fucose (X = 3,4S (46%), 2,4S (39%), and 4S (15%)). As revealed by NMR and molecular dynamics simulations, the fCS repeating unit adopts a conformation similar to that of the Le(x) blood group determinant, bringing several sulfate groups into close proximity and creating large negative patches distributed along the helical skeleton of the CS backbone. This may explain the high affinity of fCS oligosaccharides for L- and P-selectins as determined by microarray binding of fCS oligosaccharides prepared by Cu(2+)-catalyzed Fenton-type and photochemical depolymerization. No binding to E-selectin was observed. fCS poly- and oligosaccharides display low cytotoxicity in vitro, inhibit human neutrophil elastase activity, and inhibit the migration of neutrophils through an endothelial cell layer in vitro. Although the polysaccharide showed some anti-coagulant activity, small oligosaccharide fCS fragments had much reduced anticoagulant properties, with activity mainly via heparin cofactor II. The fCS polysaccharides showed prekallikrein activation comparable with dextran sulfate, whereas the fCS oligosaccharides caused almost no effect. The H. forskali fCS oligosaccharides were also tested in a mouse peritoneal inflammation model, where they caused a reduction in neutrophil infiltration. Overall, the data presented support the action of fCS as an inhibitor of selectin interactions, which play vital roles in inflammation and metastasis progression. Future studies of fCS-selectin interaction using fCS fragments or their mimetics may open new avenues for therapeutic intervention.
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Project description:The mitochondrial genome is widely used to study the molecular evolution of and perform phylogenetic analyses on animals. In this study, the complete mitochondrial genome (mitogenome) of Stichopus naso was sequenced. The mitogenome was 16,239 bp in length and contained 13 protein-coding genes (PCGs), 22 transfer RNA genes (tRNAs), and 2 ribosomal RNA genes (rRNAs). The genome composition showed positive AT-skew (0.023) and negative GC-skew (-0.158). The order of the mitochondrial genes was consistent with those from the Stichopus and Isostichopus species, whereas it was different from those of other species of Aspidochirotida. The phylogenetic analysis, based on the nucleotide sequences of 13 PCGs through the methods of Bayesian inference (BI) and maximum likelihood (ML), indicated that S. naso has close relationships with S. horrens and S. monotuberculatus, and belongs to a member of Stichopodidae. Our study provides a reference mitogenome for further molecular evolution studies and phylogenetic research on sea cucumbers.
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Project description:In this study, we report the complete mitochondrial genome of Stichopus chloronotus. The mitogenome was 16,247 base pairs (58.55% A + T content) in length, comprising a total of 37 genes, including 13 protein-coding genes, 22 transfer RNA genes and 2 ribosomal RNA genes. To resolve the phylogenetic position of S. chloronotus, we analyzed all mitochondrial protein-coding genes from 27 species within the Echinodermata. The results showed that S. chloronotus belonged to the family Stichopodidae and was more closely related to tropical Stichopus species (S. horrens and S. monotuberculatus) than to other species. Our results will be useful for evolutionary analysis of sea cucumber species.
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Project description:Fucosylated chondroitin sulfates (FCSs) PC and HH were isolated from the sea cucumbers Paracaudina chilensis and Holothuria hilla, respectively. The purification of the polysaccharides was carried out by anion-exchange chromatography on a DEAE-Sephacel column. The structural characterization of the polysaccharides was performed in terms of monosaccharide and sulfate content, as well as using a series of nondestructive NMR spectroscopic methods. Both polysaccharides were shown to contain a chondroitin core [→3)-β-d-GalNAc (N-acethyl galactosamine)-(1→4)-β-d-GlcA (glucuronic acid)-(1→]n, bearing sulfated fucosyl branches at O-3 of every GlcA residue in the chain. These fucosyl residues were different in their pattern of sulfation: PC contained Fuc2S4S and Fuc4S in a ratio of 2:1, whereas HH included Fuc2S4S, Fuc3S4S, and Fuc4S in a ratio of 1.5:1:1. Moreover, some GalNAc residues in HH were found to contain an unusual disaccharide branch Fuc4S-(1→2)-Fuc3S4S-(1→ at O-6. Sulfated GalNAc4S6S and GalNAc4S units were found in a ratio of 3:2 in PC and 2:1 in HH. Both polysaccharides demonstrated significant anticoagulant activity in a clotting time assay, which is connected with the ability of these FCSs to potentiate the inhibition of thrombin and factor Xa in the presence of anti-thrombin III (ATIII) and with the direct inhibition of thrombin in the absence of any cofactors.
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Project description:Stichopus ocellatus, known as eye-spotted sea cucumber, is a commercially important Stichopodidae holothuroid in Indo-Pacific region for its valuable nutrition and medicinal ingredients. However, because the taxonomic analyses based on morphological characters and molecular data within Aspidochirotida are limited, the deep-level evolutionary relationships of Aspidochirotida are still poorly understood. Here, for providing better insight of future evolutionary and taxonomic classification of Stichopodidae, we report the first complete mitogenome of S. ocellatus along with 37 annotated and characterized mitochondrial genes, and the phylogenetic analysis based on mitogenome data reveals sister relationship between S. ocellatus and S. monotuberculatus.
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Project description:At present, there exist some confusing issues on the species classification and phylogeny in Echinodermata. In this study, we first determined and described the complete mitochondrial genome of Stichopus variegatus. The complete mitogenome sequence had a circular mapping molecular with the total length of 16,315 bp and contained 13 protein-coding genes, 2 rRNA genes, 22 tRNA genes, and a putative control region. To further validate the newly determined sequences, phylogenetic trees involving all the Holothuroidea and other Echinodermata species available in GenBank Database were constructed. These results would be used for the species identification and further phylogenetic studies of Echinodermata.
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