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Polyinosinic:polycytidylic acid in vivo enhances Chinook salmon (Oncorhynchus tshawytscha) immunity and alters the fish metabolome

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Abstract

Poly (I:C) is a viral pathogen-associated molecular pattern (PAMP) and a synthetic dsRNA analogue, which orchestrates antiviral responses through well conserved toll-like receptor 3 (tlr3), retinoic acid inducible gene I (RIG-1) like receptors (RLRs) and class A scavenger receptors (SR-As). This study investigated the effect of poly (I:C) in vivo on Chinook salmon (Oncorhynchus tshawytscha) haematology, innate immunity, serum and liver metabolite profiles, and lymphoid tissue cytokine transcript expression, over a 5-day period post-exposure. Poly (I:C) significantly enhanced differential monocyte and neutrophil counts, and reactive oxygen species (ROS) production in peripheral blood mononuclear cells (PBMCs). GC-MS-based metabolomics revealed that poly (I:C) significantly altered 23 liver and 13 serum metabolic features. Liver and serum metabolites involved in branched chain amino acid (BCAA) metabolism significantly increased at day 1 and returned to baseline by day 5; the citric acid cycle and ROS regulation were altered. Also, liver and serum metabolites involved in glycolysis were persistently depleted from day 1 to day 5. Liver metabolites involved in phospholipid metabolism increased at day 4 to 5 and decreased from day 2 to 4 in serum. At the molecular level, poly (I:C) upregulated antiviral ifnγ and Mx1, and anti-inflammatory il-10 in fish lymphoid tissues, which normalised to baseline by day 5. Overall, poly (I:C) induced innate and adaptive immune responses through multiple mechanisms and different levels in teleost O. tshawytscha. Findings may aid design and development of amelioration strategies against viral pathogens via metabolome reprograming. Targeted studies are recommended into identified pathways and survival biomarkers.

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Acknowledgement

The authors are grateful for the kind support received from the team at the Aquaculture Biotechnology Research Group, Auckland University of Technology (Auckland), Nelson Marlborough Institute of Technology (NMIT) Glenduan Aquaculture facility, and the NMIT nursing laboratory. We also thank the technicians and the logistical team at AUT’s School of Science, and Dr. Erica Zarate and Saras Green from the University of Auckland GC-MS facility. Kind thanks also goes to Dr. Seumas Walker at Cawthron Institute for technical support.

Funding

This work was supported by a New Zealand AID doctoral scholarship to Ronald Lulijwa under the supervision of Andrea C. Alfaro and Fabrice Merien and co-funded by Auckland University of Technology (AUT)’s Aquaculture Biotechnology Research Group (ABRG).

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Authors and Affiliations

  1. Aquaculture Biotechnology Research Group, School of Science, Faculty of Health and Environmental Sciences, Auckland University of Technology, Private Bag 92006, Auckland, 1142, New Zealand

    Ronald Lulijwa, Andrea C. Alfaro, Fabrice Merien, Jill Meyer, Leonie Venter & Tim Young

  2. National Agricultural Research Organisation (NARO), Rwebitaba Zonal Agricultural Research and Development Institute (Rwebitaba-ZARDI), P. O. Box 96, Fort Portal, Uganda

    Ronald Lulijwa

  3. AUT-Roche Diagnostics Laboratory, School of Science, Faculty of Health and Environmental Sciences, Auckland University of Technology, Private Bag 92006, Auckland, 1142, New Zealand

    Fabrice Merien & Jill Meyer

  4. Nelson Marlborough Institute of Technology (NMIT), H-Block, 322 Hardy Street, Private Bag 19, Nelson, 7042, New Zealand

    Mark Burdass

  5. The Centre for Biomedical and Chemical Sciences, School of Science, Auckland University of Technology, Auckland, New Zealand

    Tim Young

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  1. Ronald Lulijwa
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  2. Andrea C. Alfaro
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  3. Fabrice Merien
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  5. Jill Meyer
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  6. Leonie Venter
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  7. Tim Young
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Correspondence to Andrea C. Alfaro.

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Ethical approval was obtained from the NMIT Animal Ethics Committee (NMIT-AEC-2018-NMIT-03).

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Lulijwa, R., Alfaro, A.C., Merien, F. et al. Polyinosinic:polycytidylic acid in vivo enhances Chinook salmon (Oncorhynchus tshawytscha) immunity and alters the fish metabolome. Aquacult Int 28, 2437–2463 (2020). https://doi.org/10.1007/s10499-020-00599-w

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