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      De novo transcriptome assembly and positive selection analysis of an individual deep-sea fish

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          Abstract

          Background

          High hydrostatic pressure and low temperatures make the deep sea a harsh environment for life forms. Actin organization and microtubules assembly, which are essential for intracellular transport and cell motility, can be disrupted by high hydrostatic pressure. High hydrostatic pressure can also damage DNA. Nucleic acids exposed to low temperatures can form secondary structures that hinder genetic information processing. To study how deep-sea creatures adapt to such a hostile environment, one of the most straightforward ways is to sequence and compare their genes with those of their shallow-water relatives.

          Results

          We captured an individual of the fish species Aldrovandia affinis, which is a typical deep-sea inhabitant, from the Okinawa Trough at a depth of 1550 m using a remotely operated vehicle (ROV). We sequenced its transcriptome and analyzed its molecular adaptation. We obtained 27,633 protein coding sequences using an Illumina platform and compared them with those of several shallow-water fish species. Analysis of 4918 single-copy orthologs identified 138 positively selected genes in A. affinis, including genes involved in microtubule regulation. Particularly, functional domains related to cold shock as well as DNA repair are exposed to positive selection pressure in both deep-sea fish and hadal amphipod.

          Conclusions

          Overall, we have identified a set of positively selected genes related to cytoskeleton structures, DNA repair and genetic information processing, which shed light on molecular adaptation to the deep sea. These results suggest that amino acid substitutions of these positively selected genes may contribute crucially to the adaptation of deep-sea animals. Additionally, we provide a high-quality transcriptome of a deep-sea fish for future deep-sea studies.

          Electronic supplementary material

          The online version of this article (10.1186/s12864-018-4720-z) contains supplementary material, which is available to authorized users.

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          Most cited references40

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          Life in extreme environments.

          Each recent report of liquid water existing elsewhere in the Solar System has reverberated through the international press and excited the imagination of humankind. Why? Because in the past few decades we have come to realize that where there is liquid water on Earth, virtually no matter what the physical conditions, there is life. What we previously thought of as insurmountable physical and chemical barriers to life, we now see as yet another niche harbouring 'extremophiles'. This realization, coupled with new data on the survival of microbes in the space environment and modelling of the potential for transfer of life between celestial bodies, suggests that life could be more common than previously thought. Here we examine critically what it means to be an extremophile, and the implications of this for evolution, biotechnology and especially the search for life in the Universe.
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            Inparanoid: a comprehensive database of eukaryotic orthologs

            The Inparanoid eukaryotic ortholog database (http://inparanoid.cgb.ki.se/) is a collection of pairwise ortholog groups between 17 whole genomes; Anopheles gambiae, Caenorhabditis briggsae, Caenorhabditis elegans, Drosophila melanogaster, Danio rerio, Takifugu rubripes, Gallus gallus, Homo sapiens, Mus musculus, Pan troglodytes, Rattus norvegicus, Oryza sativa, Plasmodium falciparum, Arabidopsis thaliana, Escherichia coli, Saccharomyces cerevisiae and Schizosaccharomyces pombe. Complete proteomes for these genomes were derived from Ensembl and UniProt and compared pairwise using Blast, followed by a clustering step using the Inparanoid program. An Inparanoid cluster is seeded by a reciprocally best-matching ortholog pair, around which inparalogs (should they exist) are gathered independently, while outparalogs are excluded. The ortholog clusters can be searched on the website using Ensembl gene/protein or UniProt identifiers, annotation text or by Blast alignment against our protein datasets. The entire dataset can be downloaded, as can the Inparanoid program itself.
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              Genome duplication, a trait shared by 22000 species of ray-finned fish.

              Through phylogeny reconstruction we identified 49 genes with a single copy in man, mouse, and chicken, one or two copies in the tetraploid frog Xenopus laevis, and two copies in zebrafish (Danio rerio). For 22 of these genes, both zebrafish duplicates had orthologs in the pufferfish (Takifugu rubripes). For another 20 of these genes, we found only one pufferfish ortholog but in each case it was more closely related to one of the zebrafish duplicates than to the other. Forty-three pairs of duplicated genes map to 24 of the 25 zebrafish linkage groups but they are not randomly distributed; we identified 10 duplicated regions of the zebrafish genome that each contain between two and five sets of paralogous genes. These phylogeny and synteny data suggest that the common ancestor of zebrafish and pufferfish, a fish that gave rise to approximately 22000 species, experienced a large-scale gene or complete genome duplication event and that the pufferfish has lost many duplicates that the zebrafish has retained.
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                Author and article information

                Contributors
                ylan@connect.ust.hk
                sunjinsd@gmail.com
                xuting0708@gmail.com
                cchen@jamstec.go.jp
                rtian@connect.ust.hk
                qiujw@hkbu.edu.hk
                +852-2358-7331 , boqianpy@ust.hk
                Journal
                BMC Genomics
                BMC Genomics
                BMC Genomics
                BioMed Central (London )
                1471-2164
                24 May 2018
                24 May 2018
                2018
                : 19
                : 394
                Affiliations
                [1 ]ISNI 0000 0004 1937 1450, GRID grid.24515.37, Department of Ocean Science and Division of Life Science, , Hong Kong University of Science and Technology, ; Clear Water Bay, Kowloon, Hong Kong, China
                [2 ]ISNI 0000 0004 1764 5980, GRID grid.221309.b, Department of Biology, , Hong Kong Baptist University, ; Hong Kong, China
                [3 ]ISNI 0000 0001 2191 0132, GRID grid.410588.0, Japan Agency for Marine-Earth Science and Technology (JAMSTEC), ; 2-15 Natsushima-cho, Yokosuka, Kanagawa 237-0061 Japan
                Article
                4720
                10.1186/s12864-018-4720-z
                5968573
                29793428
                e5ef47b8-f648-47f7-b587-69e96aaae4d8
                © The Author(s). 2018

                Open AccessThis article is distributed under the terms of the Creative Commons Attribution 4.0 International License ( http://creativecommons.org/licenses/by/4.0/), which permits unrestricted use, distribution, and reproduction in any medium, provided you give appropriate credit to the original author(s) and the source, provide a link to the Creative Commons license, and indicate if changes were made. The Creative Commons Public Domain Dedication waiver ( http://creativecommons.org/publicdomain/zero/1.0/) applies to the data made available in this article, unless otherwise stated.

                History
                : 15 November 2017
                : 23 April 2018
                Funding
                Funded by: the Strategic Priority Research Program of the Chinese Academy of Sciences
                Award ID: XDB06010102
                Award Recipient :
                Categories
                Research Article
                Custom metadata
                © The Author(s) 2018

                Genetics
                positive selection,high hydrostatic pressure,cold shock,cytoskeleton,microtubule
                Genetics
                positive selection, high hydrostatic pressure, cold shock, cytoskeleton, microtubule

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