Evaluating the Hypoxia Response of Ruffe and Flounder Gills by a Combined Proteome and Transcriptome Approach

Tiedke, Jessica; Borner, Janus; Beeck, Hendrik; Kwiatkowski, Marcel; Schmidt, Hanno; Thiel, Ralf; Fabrizius, Andrej; Burmester, Thorsten

doi:10.1371/journal.pone.0135911

Cited by 23 publications

(10 citation statements)

References 56 publications

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“…High uniformity in GO profiles was observed across the four transcriptomes. These findings agree with previous research that reported high consistency of GO terms across multiple species, as well as across multiple phyla [ 62 , 64 , 66 – 68 ]. Consistency across the assemblies further indicates accuracy of the assemblies and the assigned annotations.…”

Section: Resultssupporting

confidence: 93%

De novo transcriptome assembly, annotation and comparison of four ecological and evolutionary model salmonid fish species

et al. 2018

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BackgroundSalmonid fishes exhibit high levels of phenotypic and ecological variation and are thus ideal model systems for studying evolutionary processes of adaptive divergence and speciation. Furthermore, salmonids are of major interest in fisheries, aquaculture, and conservation research. Improving understanding of the genetic mechanisms underlying traits in these species would significantly progress research in these fields. Here we generate high quality de novo transcriptomes for four salmonid species: Atlantic salmon (Salmo salar), brown trout (Salmo trutta), Arctic charr (Salvelinus alpinus), and European whitefish (Coregonus lavaretus). All species except Atlantic salmon have no reference genome publicly available and few if any genomic studies to date.ResultsWe used paired-end RNA-seq on Illumina to generate high coverage sequencing of multiple individuals, yielding between 180 and 210 M reads per species. After initial assembly, strict filtering was used to remove duplicated, redundant, and low confidence transcripts. The final assemblies consisted of 36,505 protein-coding transcripts for Atlantic salmon, 35,736 for brown trout, 33,126 for Arctic charr, and 33,697 for European whitefish and are made publicly available. Assembly completeness was assessed using three approaches, all of which supported high quality of the assemblies: 1) ~78% of Actinopterygian single-copy orthologs were successfully captured in our assemblies, 2) orthogroup inference identified high overlap in the protein sequences present across all four species (40% shared across all four and 84% shared by at least two), and 3) comparison with the published Atlantic salmon genome suggests that our assemblies represent well covered (~98%) protein-coding transcriptomes. Thorough comparison of the generated assemblies found that 84-90% of transcripts in each assembly were orthologous with at least one of the other three species. We also identified 34-37% of transcripts in each assembly as paralogs. We further compare completeness and annotation statistics of our new assemblies to available related species.ConclusionNew, high-confidence protein-coding transcriptomes were generated for four ecologically and economically important species of salmonids. This offers a high quality pipeline for such complex genomes, represents a valuable contribution to the existing genomic resources for these species and provides robust tools for future investigation of gene expression and sequence evolution in these and other salmonid species.Electronic supplementary materialThe online version of this article (10.1186/s12864-017-4379-x) contains supplementary material, which is available to authorized users.

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Section: Resultssupporting

confidence: 93%

De novo transcriptome assembly, annotation and comparison of four ecological and evolutionary model salmonid fish species

et al. 2018

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“…Protocols for body fluids such as plasma and mucus are also being optimised due to its easy retrievable way and show to be a promisor approach to collect important and representative protein content of the fish immune state without the need of animal sacrifice (Morzel et al 2006;Provan et al 2006;Jiang et al 2009;Cordeiro et al 2012;Silva et al 2012;Patel & Brinchmann 2017). Most of the welfare-related proteomic studies concern environmental sources of stress related to common aquaculture production systems, such as diseases and parasites (Chongsatja et al 2007;Yeh et al 2008;Chen et al 2010Chen et al , 2011Ni et al 2010;Somboonwiwat et al 2010;Xiong et al 2011;Ji et al 2013;L€ u et al 2014;Buj an et al 2015;Xu et al 2015;Zhang et al 2017), hypoxia (Bosworth et al 2005;Jiang et al 2009;Cordeiro et al 2012;Douxfils et al 2012;Tiedke et al 2015;P edron et al 2017;Zhang et al 2017), anoxia (Wulff et al 2008;Mendelsohn et al 2009;Smith et al 2009), temperature (Addis et al 2010;Ibarz et al 2010;Chang et al 2016;Richard et al 2016;Schrama et al 2017;Nuez-Ort ın et al 2018), high stocking densities (Iguchi et al 2003;Barton et al 2005;…”

Section: Proteomics As a Tool To Assess Fish Welfarementioning

confidence: 99%

A Proteomics and other Omics approach in the context of farmed fish welfare and biomarker discovery

Magalhães

Cerqueira

Schrama

et al. 2018

Reviews in Aquaculture

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The rapid and intensive growth of aquaculture over the last decade, poses a tremendous challenge to this industry in order to comply with the latest guidelines, established to minimise its negative effects on the environment, animal welfare and public health. Farmed fish welfare has become one of the main priorities towards sustainable aquaculture production with several initiatives launched by the European Union within the framework of the 2030 agenda. It is clear that an unbiased and reliable way to access farmed fish welfare needs to be implemented due to the lack of reliable indicators and standardised methods that are used at present. In this review, we start by addressing the status quo of animal and fish welfare definition in particular, describing the methods and assays currently used to measure it. We then explain why we believe these methods are unreliable and why there is a need to establish new ones that will promote productivity and consumer's acceptance of farmed fish. The establishment of a new type of welfare biomarkers using cutting‐edge technologies like proteomics and other omics technologies is proposed as a solution to this issue. Therefore, we provide a brief description of these new methodologies, describing for each one how they can improve our scientific knowledge and the role they can play in farmed fish welfare biomarker discovery.

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“…Physiological and molecular adaptations include enhanced production of respiratory proteins ( e.g. , hemoglobin, myoglobin, and neuroglobin) to increase oxygen carrying capacity, upregulation of genes encoding enzymes within the glycolytic pathway, and downregulation of genes involved in aerobic energy production and other energy-consuming processes ( Tiedke et al 2015 ). Differential regulation of genes involved in general metabolism, catabolism, and the ubiquitin-proteasome pathway have also been demonstrated in fish as responses to low DO ( Ju et al 2007 ; Zhang et al 2012 ; Olsvik et al 2013 ).…”

mentioning

confidence: 99%

Identification of Hypoxia-Specific Biomarkers in Salmonids Using RNA-Sequencing and Validation Using High-Throughput qPCR

Akbarzadeh

Houde

Sutherland

et al. 2020

G3 Genes|Genomes|Genetics

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Identifying early gene expression responses to hypoxia (i.e., low dissolved oxygen) as a tool to assess the degree of exposure to this stressor is crucial for salmonids, because they are increasingly exposed to hypoxic stress due to anthropogenic habitat change, e.g., global warming, excessive nutrient loading, and persistent algal blooms. Our goal was to discover and validate gill gene expression biomarkers specific to the hypoxia response in salmonids across multi-stressor conditions. Gill tissue was collected from 24 freshwater juvenile Chinook salmon (Oncorhynchus tshawytscha), held in normoxia [dissolved oxygen (DO) > 8 mg L-1] and hypoxia (DO = 4‒5 mg L-1) in 10 and 18°C temperatures for up to six days. RNA-sequencing (RNA-seq) was then used to discover 240 differentially expressed genes between hypoxic and normoxic conditions, but not affected by temperature. The most significantly differentially expressed genes had functional roles in the cell cycle and suppression of cell proliferation associated with hypoxic conditions. The most significant genes (n = 30) were selected for real-time qPCR assay development. These assays demonstrated a strong correlation (r = 0.88; p < 0.001) between the expression values from RNA-seq and the fold changes from qPCR. Further, qPCR of the 30 candidate hypoxia biomarkers was applied to an additional 322 Chinook salmon exposed to hypoxic and normoxic conditions to reveal the top biomarkers to define hypoxic stress. Multivariate analyses revealed that smolt stage, water salinity, and morbidity status were relevant factors to consider with the expression of these genes in relation to hypoxic stress. These hypoxia candidate genes will be put into application screening Chinook salmon to determine the identity of stressors impacting the fish.

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Evaluating the Hypoxia Response of Ruffe and Flounder Gills by a Combined Proteome and Transcriptome Approach

Cited by 23 publications

References 56 publications

De novo transcriptome assembly, annotation and comparison of four ecological and evolutionary model salmonid fish species

De novo transcriptome assembly, annotation and comparison of four ecological and evolutionary model salmonid fish species

A Proteomics and other Omics approach in the context of farmed fish welfare and biomarker discovery

Identification of Hypoxia-Specific Biomarkers in Salmonids Using RNA-Sequencing and Validation Using High-Throughput qPCR

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