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      Developing specific molecular biomarkers for thermal stress in salmonids

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          Abstract

          Background

          Pacific salmon ( Oncorhynchus spp.) serve as good biological indicators of the breadth of climate warming effects on fish because their anadromous life cycle exposes them to environmental challenges in both marine and freshwater environments. Our study sought to mine the extensive functional genomic studies in fishes to identify robust thermally-responsive biomarkers that could monitor molecular physiological signatures of chronic thermal stress in fish using non-lethal sampling of gill tissue.

          Results

          Candidate thermal stress biomarkers for gill tissue were identified using comparisons among microarray datasets produced in the Molecular Genetics Laboratory, Pacific Biological Station, Nanaimo, BC, six external, published microarray studies on chronic and acute temperature stress in salmon, and a comparison of significant genes across published studies in multiple fishes using deep literature mining. Eighty-two microarray features related to 39 unique gene IDs were selected as candidate chronic thermal stress biomarkers. Most of these genes were identified both in the meta-analysis of salmon microarray data and in the literature mining for thermal stress markers in salmonids and other fishes. Quantitative reverse transcription PCR (qRT-PCR) assays for 32 unique genes with good efficiencies across salmon species were developed, and their activity in response to thermally challenged sockeye salmon ( O. nerka) and Chinook salmon ( O. tshawytscha) (cool, 13–14 °C and warm temperatures 18–19 °C) over 5–7 days was assessed. Eight genes, including two transcripts of each SERPINH1 and HSP90AA1, FKBP10, MAP3K14, SFRS2, and EEF2 showed strong and robust chronic temperature stress response consistently in the discovery analysis and both sockeye and Chinook salmon validation studies.

          Conclusions

          The results of both discovery analysis and gene expression showed that a panel of genes involved in chaperoning and protein rescue, oxidative stress, and protein biosynthesis were differentially activated in gill tissue of Pacific salmon in response to elevated temperatures. While individually, some of these biomarkers may also respond to other stressors or biological processes, when expressed in concert, we argue that a biomarker panel comprised of some or all of these genes could provide a reliable means to specifically detect thermal stress in field-caught salmon.

          Electronic supplementary material

          The online version of this article (10.1186/s12864-018-5108-9) contains supplementary material, which is available to authorized users.

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          Most cited references83

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          Heat-shock proteins, molecular chaperones, and the stress response: evolutionary and ecological physiology.

          Molecular chaperones, including the heat-shock proteins (Hsps), are a ubiquitous feature of cells in which these proteins cope with stress-induced denaturation of other proteins. Hsps have received the most attention in model organisms undergoing experimental stress in the laboratory, and the function of Hsps at the molecular and cellular level is becoming well understood in this context. A complementary focus is now emerging on the Hsps of both model and nonmodel organisms undergoing stress in nature, on the roles of Hsps in the stress physiology of whole multicellular eukaryotes and the tissues and organs they comprise, and on the ecological and evolutionary correlates of variation in Hsps and the genes that encode them. This focus discloses that (a) expression of Hsps can occur in nature, (b) all species have hsp genes but they vary in the patterns of their expression, (c) Hsp expression can be correlated with resistance to stress, and (d) species' thresholds for Hsp expression are correlated with levels of stress that they naturally undergo. These conclusions are now well established and may require little additional confirmation; many significant questions remain unanswered concerning both the mechanisms of Hsp-mediated stress tolerance at the organismal level and the evolutionary mechanisms that have diversified the hsp genes.
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            featureCounts: An efficient general-purpose program for assigning sequence reads to genomic features

            , , (2013)
            Next-generation sequencing technologies generate millions of short sequence reads, which are usually aligned to a reference genome. In many applications, the key information required for downstream analysis is the number of reads mapping to each genomic feature, for example to each exon or each gene. The process of counting reads is called read summarization. Read summarization is required for a great variety of genomic analyses but has so far received relatively little attention in the literature. We present featureCounts, a read summarization program suitable for counting reads generated from either RNA or genomic DNA sequencing experiments. featureCounts implements highly efficient chromosome hashing and feature blocking techniques. It is considerably faster than existing methods (by an order of magnitude for gene-level summarization) and requires far less computer memory. It works with either single or paired-end reads and provides a wide range of options appropriate for different sequencing applications. featureCounts is available under GNU General Public License as part of the Subread (http://subread.sourceforge.net) or Rsubread (http://www.bioconductor.org) software packages.
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              What is principal component analysis?

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                Author and article information

                Contributors
                akbarzadeh@ut.ac.ir
                oliver@guntheranalytics.com
                Aimee.Houde@dfo-mpo.gc.ca
                shaorong.li@dfo-mpo.gc.ca
                Tobi.Ming@dfo-mpo.gc.ca
                Ken.Jeffries@umanitoba.ca
                scott.hinch@ubc.ca
                Kristi.Saunders@dfo-mpo.gc.ca
                Journal
                BMC Genomics
                BMC Genomics
                BMC Genomics
                BioMed Central (London )
                1471-2164
                16 October 2018
                16 October 2018
                2018
                : 19
                : 749
                Affiliations
                [1 ]ISNI 0000 0004 0449 2129, GRID grid.23618.3e, Fisheries and Oceans Canada, Pacific Biological Station, ; 3190 Hammond Bay Road, Nanaimo, BC V9T 6N7 Canada
                [2 ]GRID grid.444744.3, Department of Fisheries, Faculty of Marine Science and technology, , University of Hormozgan, ; P.O. Box: 3995, Bandar Abbas, Iran
                [3 ]Günther Analytics, Vancouver, BC Canada
                [4 ]ISNI 0000 0004 1936 9609, GRID grid.21613.37, Department of Biological Sciences, , University of Manitoba, ; Winnipeg, MB R3T 2N2 Canada
                [5 ]ISNI 0000 0001 2288 9830, GRID grid.17091.3e, Pacific Salmon Ecology and Conservation Laboratory, Department of Forest and Conservation Sciences, , University of British Columbia, ; Vancouver, BC V6T1Z4 Canada
                Author information
                http://orcid.org/0000-0002-2527-4791
                Article
                5108
                10.1186/s12864-018-5108-9
                6192343
                30326831
                b8757827-d500-4c57-acc4-ae5c331ef1ab
                © 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
                : 9 July 2018
                : 21 September 2018
                Funding
                Funded by: FundRef http://dx.doi.org/10.13039/501100002790, Canadian Network for Research and Innovation in Machining Technology, Natural Sciences and Engineering Research Council of Canada;
                Funded by: Genome BC
                Funded by: DFO Genomics Research and Development Initiative
                Categories
                Research Article
                Custom metadata
                © The Author(s) 2018

                Genetics
                gene expression,salmon fit-chips,biomarker,pacific salmon,thermal stress
                Genetics
                gene expression, salmon fit-chips, biomarker, pacific salmon, thermal stress

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