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Genetic architecture and correlations between the gut microbiome and gut gene transcription in Chinook salmon (Oncorhynchus tshawytscha)

Abstract

Population divergence through selection can drive local adaptation in natural populations which has implications for the effective restoration of declining and extirpated populations. However, adaptation to local environmental conditions is complicated when both the host and its associated microbiomes must respond via co-evolutionary change. Nevertheless, for adaptation to occur through selection, variation in both host and microbiome traits should include additive genetic effects. Here we focus on host immune function and quantify factors affecting variation in gut immune gene transcription and gut bacterial community composition in early life-stage Chinook salmon (Oncorhynchus tshawytscha). Specifically, we utilized a replicated factorial breeding design to determine the genetic architecture (sire, dam and sire-by-dam interaction) of gut immune gene transcription and microbiome composition. Furthermore, we explored correlations between host gut gene transcription and microbiota composition. Gene transcription was quantified using nanofluidic qPCR arrays (22 target genes) and microbiota composition using 16 S rRNA gene (V5-V6) amplicon sequencing. We discovered limited but significant genetic architecture in gut microbiota composition and transcriptional profiles. We also identified significant correlations between gut gene transcription and microbiota composition, highlighting potential mechanisms for functional interactions between the two. Overall, this study provides support for the co-evolution of host immune function and their gut microbiota in Chinook salmon, a species recognized as locally adapted. Thus, the inclusion of immune gene transcription profile and gut microbiome composition as factors in the development of conservation and commercial rearing practices may provide new and more effective approaches to captive rearing.

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Fig. 1: Stacked bar plots showing relative abundance of gut bacterial community composition presented at the genus level for all 260 offspring Chinook salmon from 15 dams (each panel is one dam).
Fig. 2: Results of the LMM analysis of dam, sire and dam-by-sire interaction effects on the abundance for Chinook salmon gut bacteria at the individual ASV level (X-axis, 152 ASVs).
Fig. 3: Heat diagram showing the pattern of correlation between the relative abundance of the gut bacteria at the ASV level with gut gene transcription at 19 selected host genes.

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Data availability

Raw data are available at the Sequence Read Archive of NCBI with PRJNA925893 BioProject accession number.

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Acknowledgements

We thank Drs. John Heath and Ann Heath for providing resources to rear fish at Yellow Island Aquaculture Ltd. (YIAL). We would like to thank Alex Kajtar, Dr. Clare Venney, and Jane Drown for their assistance with sampling. Lastly, we want to thank Shelby Mackie for her aid with lab work. We are also grateful to three anonymous reviewers for their constructive comments that significantly improved the manuscript. Funding for this project was provided by The Natural Sciences and Engineering Research Council of Canada (NSERC), Ontario Trillium Scholarship (OTS), and Ontario Graduate Scholarship (OGS).

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J.S, F.Z, D.D.H. conceived and planned the experiments. F.Z carried out field work, wet laboratory sample preparations and experiments. J.S. and D.D.H. contributed to the interpretation of the results. J.S. took the lead in analyzing and interpreting the data and writing the manuscript. D.D.H., provided critical feedback and helped shape the research, analysis, and manuscript.

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Correspondence to Daniel D. Heath.

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This study was reviewed and approved by the University of Windsor Animal Care Committee (ACC) for adherence to the Canadian Counsel on Animal Care (CCAC). The University of Windsor permit number for this work was: AUPP-17-08. All guidelines and protocols required by the Canadian Counsel for Animal Care were followed.

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Genetic architecture and correlations between the gut microbiome and gut gene transcription in Chinook salmon (Oncorhynchus tshawytscha)

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Sadeghi, J., Zaib, F. & Heath, D.D. Genetic architecture and correlations between the gut microbiome and gut gene transcription in Chinook salmon (Oncorhynchus tshawytscha). Heredity 133, 54–66 (2024). https://doi.org/10.1038/s41437-024-00692-3

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