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. 2024 Jun;23(3):e12898.
doi: 10.1111/gbb.12898.

Behavioral transcriptomic effects of triploidy and probiotic therapy (Bifidobacterium, Lactobacillus, and Lactococcus mixture) on juvenile Chinook salmon (Oncorhynchus tshawytscha)

Chelsea E Frank  1 , Javad Sadeghi  2 , Daniel D Heath  1   2 , Christina A D Semeniuk  1   2
Affiliations

Behavioral transcriptomic effects of triploidy and probiotic therapy (Bifidobacterium, Lactobacillus, and Lactococcus mixture) on juvenile Chinook salmon (Oncorhynchus tshawytscha)

Chelsea E Frank et al. Genes Brain Behav. 2024 Jun.

Abstract

Aquaculturists use polyploid fish to maximize production albeit with some unintended consequences including compromised behaviors and physiological function. Given benefits of probiotic therapies (e.g., improved immune response, growth, and metabolism), we explored probiotic supplementation (mixture of Bifidobacterium, Lactobacillus, and Lactococcus), to overcome drawbacks. We first examined fish gut bacterial community composition using 16S metabarcoding (via principal coordinate analyses and PERMANOVA) and determined probiotics significantly impacted gut bacteria composition (p = 0.001). Secondly, we examined how a genomic disruptor (triploidy) and diet supplements (probiotics) impact gene transcription and behavioral profiles of hatchery-reared Chinook salmon (Oncorhynchus tshawytscha). Juveniles from four treatment groups (diploid-regular feed, diploid-probiotic feed, triploid-regular feed, and triploid-probiotic feed; n = 360) underwent behavioral assays to test activity, exploration, neophobia, predator evasion, aggression/sociality, behavioral sensitivity, and flexibility. In these fish, transcriptional profiles for genes associated with neural functions (neurogenesis/synaptic plasticity) and biomarkers for stress response and development (growth/appetite) were (i) examined across treatments and (ii) used to describe behavioral phenotypes via principal component analyses and general linear mixed models. Triploids exhibited a more active behavioral profile (p = 0.002), and those on a regular diet had greater Neuropeptide Y transcription (p = 0.02). A growth gene (early growth response protein 1, p = 0.02) and long-term neural development genes (neurogenic differentiation factor, p = 0.003 and synaptysomal-associated protein 25-a, p = 0.005) impacted activity and reactionary profiles, respectively. Overall, our probiotic treatment did not compensate for triploidy. Our research highlights novel applications of behavioral transcriptomics for identifying candidate genes and dynamic, mechanistic associations with complex behavioral repertoires.

Keywords: Chinook salmon; behavioral transcriptomics; gut microbiota; gut‐brain axis; probiotic; triploidy.

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Conflict of interest statement

The authors declare no conflicts of interest.

Figures

FIGURE 1
FIGURE 1
Experimental flowchart for the probiotic conformation and behavioral transcriptomic portion of the study. Different individuals were used for these experiments.
FIGURE 2
FIGURE 2
Schematic diagram of the behavioral arena set up. A total of 30 trials were run, four‐tank numbers tested (individuals assigned A‐D based on tank number), with three individuals from a given tank tested at a given time (assigned a number of 01‐03). Each behavioral trial consisted of four assays: an open field test (acclimation period), novel object test, predator response test, and a mirror test. Predator silhouettes were moved across arenas at a steady pace, and mirrors were placed on the opposite side of where predator movement was initiated.
FIGURE 3
FIGURE 3
PCoA of the fish gut microbiome colored based on treatments using the Bray–Curtis dissimilarity matrix (A) and the Unweighted UniFrac matrix (B).
FIGURE 4
FIGURE 4
Summary diagram of findings (significant interactions), incorporating treatments, mass, gene transcriptional profiles, and behavioral profiles. Time of day and rearing tank density not included in this summary. Significant interactions of direct effects indicated with directionality indicated. Where genes are directly involved, gene is indicated in black text, while gene groups included in the behavioral models, but not directly driving the impact, are indicated in gray.
FIGURE 5
FIGURE 5
Significant model‐predicted results of regression analysis of food treatment effects on gene transcription. Probiotic therapies had a significant effect on gene expression for the NPY (n = 135) gene, where those on probiotic diets had decreased gene expression compared with regularly fed counterparts. Model‐predicted relationships are plotted; data points show predicted‐model data.
FIGURE 6
FIGURE 6
Significant model‐predicted results of regression analysis of ploidy treatment effects on active behavioral profile. Triploidization had a significant effect on the activity levels of individuals, with triploids more active than diploid counter parts when the stress response gene functional group (n = 106) was incorporated into the behavioral profile models. Triploidization did not have a significant effect on reactionary, boldness/aggression or the laterality/extremes of locomotor behaviors. Model‐predicted relationships are plotted, data points show the model‐predicted data.
FIGURE 7
FIGURE 7
Significant model‐predicted results of regression analysis of gene transcription effects on behavioral profiles. Significant gene effects on behavioral profiles. Reactionary profiles showed gene effects, particularly for NeuroD1(A) and SNAP‐25a (B) transcription (n = 174). Individuals exhibiting greater NeuroD1 expression also showed an increased level of reactionary behaviors, while those with an increased level of SNAP‐25a expression had a decrease in level of reactionary behaviors. Active profiles showed a significant gene effect of EGR‐1 (C) transcription (n = 16), where individuals with higher EGR‐1 transcription also had increased activity levels. Model‐predicted relationships are plotted, data points show the predicted‐model data.
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References

    1. Asche F, Roll KH, Tveterås S. Future trends in aquaculture: productivity growth and increased production. In: Holmer M, Black K, Duarte CM, Marbà N, Karakassis I, eds. Aquaculture in the Ecosystem. Springer; 2008. doi:10.1007/978-1-4020-6810-2_9 - DOI
    1. FAO . The State of World Fisheries and Aquaculture 2018—Meeting the Sustainable Development Goals. Rome. 2018.
    1. Hardy RW. Collaborative opportunities between fish nutrition and other disciplines in aquaculture: an overview. Aquaculture. 1999;177(1–4):217‐230. doi:10.1016/S0044-8486(99)00086-1 - DOI
    1. Hixson SM. Fish nutrition and current issues in aquaculture: the balance in providing safe and nutritious seafood, in an environmentally sustainable manner. J Aquacult Res Dev. 2014;5(3):1‐10. doi:10.4172/2155-9546.1000234 - DOI
    1. FAO . The State of World Fisheries and Aquaculture 2020 Sustainability in Action. Rome. 2020.

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