Dataset Information

Adaptation and evolution of deep-sea scale worms (Annelida: Polynoidae): insights from transcriptome comparison with a shallow-water species.

ABSTRACT: Polynoid scale worms (Polynoidae, Annelida) invaded deep-sea chemosynthesis-based ecosystems approximately 60 million years ago, but little is known about their genetic adaptation to the extreme deep-sea environment. In this study, we reported the first two transcriptomes of deep-sea polynoids (Branchipolynoe pettiboneae, Lepidonotopodium sp.) and compared them with the transcriptome of a shallow-water polynoid (Harmothoe imbricata). We determined codon and amino acid usage, positive selected genes, highly expressed genes and putative duplicated genes. Transcriptome assembly produced 98,806 to 225,709 contigs in the three species. There were more positively charged amino acids (i.e., histidine and arginine) and less negatively charged amino acids (i.e., aspartic acid and glutamic acid) in the deep-sea species. There were 120 genes showing clear evidence of positive selection. Among the 10% most highly expressed genes, there were more hemoglobin genes with high expression levels in both deep-sea species. The duplicated genes related to DNA recombination and metabolism, and gene expression were only enriched in deep-sea species. Deep-sea scale worms adopted two strategies of adaptation to hypoxia in the chemosynthesis-based habitats (i.e., rapid evolution of tetra-domain hemoglobin in Branchipolynoe or high expression of single-domain hemoglobin in Lepidonotopodium sp.).

SUBMITTER: Zhang Y

PROVIDER: S-EPMC5387418 | biostudies-literature | 2017 Apr

REPOSITORIES: biostudies-literature

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Adaptation and evolution of deep-sea scale worms (Annelida: Polynoidae): insights from transcriptome comparison with a shallow-water species.

Zhang Yanjie Y Sun Jin J Chen Chong C Watanabe Hiromi K HK Feng Dong D Zhang Yu Y Chiu Jill M Y JM Qian Pei-Yuan PY Qiu Jian-Wen JW

Scientific reports 20170411

Polynoid scale worms (Polynoidae, Annelida) invaded deep-sea chemosynthesis-based ecosystems approximately 60 million years ago, but little is known about their genetic adaptation to the extreme deep-sea environment. In this study, we reported the first two transcriptomes of deep-sea polynoids (Branchipolynoe pettiboneae, Lepidonotopodium sp.) and compared them with the transcriptome of a shallow-water polynoid (Harmothoe imbricata). We determined codon and amino acid usage, positive selected ge ...[more]

PMID: 28397791

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Project description:Polynoidae Kinberg, 1856 has five branchiate genera: Branchipolynoe Pettibone, 1984, Branchinotogluma Pettibone, 1985, Branchiplicatus Pettibone, 1985, Peinaleopolynoe Desbruyères & Laubier, 1988, and Thermopolynoe Miura, 1994, all native to deep-sea, chemosynthetic-based habitats. Of these, Peinaleopolynoe has two accepted species; Peinaleopolynoe sillardi Desbruyères & Laubier, 1988 (Atlantic Ocean) and Peinaleopolynoe santacatalina Pettibone, 1993 (East Pacific Ocean). The goal of this study was to assess the phylogenetic position of Peinaleopolynoe, utilizing DNA sequences from a broad sampling of deep-sea polynoids. Representatives from all five branchiate genera were included, several species of which were sampled from near the type localities; Branchinotogluma sandersi Pettibone, 1985 from the Galápagos Rift (E/V "Nautilus"); Peinaleopolynoe sillardi from organic remains in the Atlantic Ocean; Peinaleopolynoe santacatalina from a whalefall off southern California (R/V "Western Flyer") and Thermopolynoe branchiata Miura, 1994 from Lau Back-Arc Basin in the western Pacific (R/V "Melville"). Phylogenetic analyses were conducted using mitochondrial (COI, 16S rRNA, and CytB) and nuclear (18S rRNA, 28S rRNA, and H3) genes. The analyses revealed four new Peinaleopolynoe species from the Pacific Ocean that are formally described here: Peinaleopolynoe orphanae Hatch & Rouse, sp. nov., type locality Pescadero Basin in the Gulf of California, Mexico (R/V "Western Flyer"); Peinaleopolynoe elvisi Hatch & Rouse, sp. nov. and Peinaleopolynoe goffrediae Hatch & Rouse, sp. nov., both with a type locality in Monterey Canyon off California (R/V "Western Flyer") and Peinaleopolynoe mineoi Hatch & Rouse, sp. nov. from Costa Rica methane seeps (R/V "Falkor"). In addition to DNA sequence data, the monophyly of Peinaleopolynoe is supported by the presence of ventral papillae on segments 12-15. The results also demonstrated the paraphyly of Branchinotogluma and Lepidonotopodium Pettibone, 1983 and taxonomic revision of these genera is required. We apply the subfamily name Lepidonotopodinae Pettibone 1983, for the clade comprised of Branchipolynoe, Branchinotogluma, Bathykurila, Branchiplicatus, Lepidonotopodium, Levensteiniella Pettibone, 1985, Thermopolynoe, and Peinaleopolynoe.

Project description:Osedax, commonly known as bone-eating worms, are unusual marine annelids belonging to Siboglinidae and represent a remarkable example of evolutionary adaptation to a specialized habitat, namely sunken vertebrate bones. Usually, females of these animals live anchored inside bone owing to a ramified root system from an ovisac, and obtain nutrition via symbiosis with Oceanospirillales gamma-proteobacteria. Since their discovery, 26 Osedax operational taxonomic units (OTUs) have been reported from a wide bathymetric range in the Pacific, the North Atlantic, and the Southern Ocean. Using experimentally deployed and naturally occurring bones we report here the presence of Osedax deceptionensis at very shallow-waters in Deception Island (type locality; Antarctica) and at moderate depths near South Georgia Island (Subantarctic). We present molecular evidence in a new phylogenetic analysis based on five concatenated genes (28S rDNA, Histone H3, 18S rDNA, 16S rDNA, and cytochrome c oxidase I-COI-), using Maximum Likelihood and Bayesian inference, supporting the placement of O. deceptionensis as a separate lineage (Clade VI) although its position still remains uncertain. This phylogenetic analysis includes a new unnamed species (O. 'mediterranea') recently discovered in the shallow-water Mediterranean Sea belonging to Osedax Clade I. A timeframe of the diversification of Osedax inferred using a Bayesian framework further suggests that Osedax diverged from other siboglinids during the Middle Cretaceous (ca. 108 Ma) and also indicates that the most recent common ancestor of Osedax extant lineages dates to the Late Cretaceous (ca. 74.8 Ma) concomitantly with large marine reptiles and teleost fishes. We also provide a phylogenetic framework that assigns newly-sequenced Osedax endosymbionts of O. deceptionensis and O. 'mediterranea' to ribospecies Rs1. Molecular analysis for O. deceptionensis also includes a COI-based haplotype network indicating that individuals from Deception Island and the South Georgia Island (ca. 1,600 km apart) are clearly the same species, confirming the well-developed dispersal capabilities reported in other congeneric taxa. In addition, we include a complete description of living features and morphological characters (including scanning and transmission electron microscopy) of O. deceptionensis, a species originally described from a single mature female, and compare it to information available for other congeneric OTUs.

Project description:BackgroundBarnacles are specialized marine organisms that differ from other crustaceans in possession of a calcareous shell, which is attached to submerged surfaces. Barnacles have a wide distribution, mostly in the intertidal zone and shallow waters, but a few species inhabit the deep-sea floor. It is of interest to investigate how such sessile crustaceans became adapted to extreme deep-sea environments. We sequenced the transcriptomes of a deep-sea barnacle, Glyptelasma gigas collected at a depth of 731 m from the northern area of the Zhongjiannan Basin, and a shallow-water coordinal relative, Octolasmis warwicki. The purpose of this study was to provide genetic resources for investigating adaptation mechanisms of deep-sea barnacles.ResultsTotals of 62,470 and 51,585 unigenes were assembled for G. gigas and O. warwicki, respectively, and functional annotation of these unigenes was made using public databases. Comparison of the protein-coding genes between the deep- and shallow-water barnacles, and with those of four other shallow-water crustaceans, revealed 26 gene families that had experienced significant expansion in G. gigas. Functional annotation showed that these expanded genes were predominately related to DNA repair, signal transduction and carbohydrate metabolism. Base substitution analysis on the 11,611 single-copy orthologs between G. gigas and O. warwicki indicated that 25 of them were distinctly positive selected in the deep-sea barnacle, including genes related to transcription, DNA repair, ligand binding, ion channels and energy metabolism, potentially indicating their importance for survival of G. gigas in the deep-sea environment.ConclusionsThe barnacle G. gigas has adopted strategies of expansion of specific gene families and of positive selection of key genes to counteract the negative effects of high hydrostatic pressure, hypoxia, low temperature and food limitation on the deep-sea floor. These expanded gene families and genes under positive selection would tend to enhance the capacities of G. gigas for signal transduction, genetic information processing and energy metabolism, and facilitate networks for perceiving and responding physiologically to the environmental conditions in deep-sea habitats. In short, our results provide genomic evidence relating to deep-sea adaptation of G. gigas, which provide a basis for further biological studies of sessile crustaceans in the deep sea.

Dataset Information

Adaptation and evolution of deep-sea scale worms (Annelida: Polynoidae): insights from transcriptome comparison with a shallow-water species.

Publications

Adaptation and evolution of deep-sea scale worms (Annelida: Polynoidae): insights from transcriptome comparison with a shallow-water species.

Similar Datasets

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