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Transcriptome Profiling Reveals Insight into Distinct Immune Responses to Aeromonas salmonicida in Gill of Two Rainbow Trout Strains

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Abstract

The fish gills represent a crucial organ for the communication with the aquatic environment. Transcriptional changes in gills of two hatchery rainbow trout strains in response to injection with the potent pathogen Aeromonas salmonicida were detected by global gene expression profiling using a 4×44K oligonucleotide microarray. Emphasis was placed on “day 3 postinfection” representing a decisive time point for the resolution of inflammation. The comparison of features and pathways differentially regulated in branchial tissues revealed that the local breeding strain BORN and imported American rainbow trout apply common and specific immune strategies. In gills of infected BORN trout, we observed a dynamic regulation of genes controlling NF-κB pathways and the induction of factors promoting the development of myeloid cells, whereas an increased expression of lysozyme and immunoglobulin genes was obvious in gills of infected import trout. In order to prove the relevance of the array-predicted candidates as well as well-known immune genes for gill immunity, a subsequent in vitro experiment was conducted. Altogether, we uncovered dynamic but moderate changes in the expression of a broad range of immune-relevant features implying the gill’s involvement in pathogen defense strategies.

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Abbreviations

aa:

Amino acids

Ct:

Cycle threshold

EST:

Expressed sequence tag

PAMP:

Pathogen-associated molecular pattern

PBS:

Phosphate-buffered saline

PFA:

Perfluoroalkoxy

p.i.:

Post-infection

PRR:

Pattern recognition receptor

qRT-PCR:

Real-time quantitative reverse transcriptase polymerase chain reaction

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Acknowledgments

This work was funded by the European Social Fund and Ministry of Education, Science and Culture of Mecklenburg-Western Pomerania (Project AU11040). DFG-Grant SE 326/16-1 from the German Research Foundation also supported this project. We kindly thank I. Hennings, B. Schöpel, and M. Fuchs for expert technical assistance. The A. salmonicida ssp. salmonicida wild-type strain JF 2267 was kindly provided by Prof. Dr. J. Frey, University Bern, Switzerland.

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  1. Institut für Genombiologie, Leibniz-Institut für Nutztierbiologie (FBN), Wilhelm-Stahl-Allee 2, 18196, Dummerstorf, Germany

    Alexander Rebl, Judith M. Köbis, Marieke Verleih & Tom Goldammer

  2. Institut für Immunologie, Friedrich-Loeffler-Institut (FLI), Greifswald, Insel Riems, Germany

    Tomáš Korytář, Joanna Jaros & Bernd Köllner

  3. Norwegian Institute of Food, Fisheries and Aquaculture Research (Nofima), Postboks 5010, Ås, Norway

    Aleksei Krasnov

  4. Institut für Fischerei, Landesforschungsanstalt für Landwirtschaft und Fischerei Mecklenburg-Vorpommern (LFA-MV), Born, Germany

    Carsten Kühn

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ESM 3

Alignment of cDNA sequences representing putative paralogues of (A) CCL4, (B) CCL19, (C) LYG, (D) PSMB7, and (E) CD200 genes. Dashes denote gaps; asterisks below the alignment denote identical nucleotides. Different variants (a, b, c; as termed in the manuscript) are listed with their respective GenBank accession codes and are indicated by different colors (red, blue, green, respectively). The ORF is printed in boldface type. Arrows indicate the location of paralogue-specific oligonucleotides used for qRT-PCR (DOCX 111 kb)

ESM 4

Quantitative PCR analysis of immune gene expression after bacterial infection of BORN (black bars) and imported trout (grey bars) (n = 4). Expression levels of lysozyme genes (A–C); haptoglobin gene (D); complement gene CFH (E); CD209 gene (F); cytokine genes CXCL14 (G), CXCF1b (H), CC-chemokine (I), CCL4 (J, K), CCL19 (L, M), CCL20 (N), CXCL12 (O); and PSMB7 genes (P–R) were examined at 0, 1, 2, 3, and 7 days after bacterial injection and expressed as means ± SEM. The time point 0 h indicates injection of sterile PBS. Stars above the error bars indicate a significant expression difference compared to PBS 0 h controls: *p ≤ 0.1; *p ≤ 0.05; **p ≤ 0.01 (JPEG 100 kb)

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Rebl, A., Korytář, T., Köbis, J.M. et al. Transcriptome Profiling Reveals Insight into Distinct Immune Responses to Aeromonas salmonicida in Gill of Two Rainbow Trout Strains. Mar Biotechnol 16, 333–348 (2014). https://doi.org/10.1007/s10126-013-9552-x

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