Regulation of Host Gene Expression by Gastrointestinal Tract Microbiota in Chinook Salmon (Oncorhynchus tshawytscha)

Abstract

Differences in gut microbiome composition are linked with health, disease and ultimately host fitness; however, the molecular mechanisms underlying that relationship are not well characterized. Here, we modified the fish gut microbiota using antibiotic and probiotic feed treatments to address the effect of host microbiome on gene expression patterns. Chinook salmon (Oncorhynchus tshawytscha) gut gene expression was evaluated using whole transcriptome sequencing (RNA-Seq) on hindgut mucosa samples from individuals treated with antibiotic, probiotic and control diets to determine differentially expressed (DE) host genes. Fifty DE host genes were selected for further characterization using nanofluidic qPCR chips. We used 16S rRNA gene metabarcoding to characterize the rearing water and host gut microbiome bacterial communities. Daily administration of antibiotics and probiotics resulted in significant changes in fish gut and aquatic microbiota as well as more than 100 DE genes in the antibiotic and probiotic treatment fish, relative to healthy controls. Normal microbiota depletion by antibiotics mostly led to downregulation of different aspects of immunity and upregulation of apoptotic process. In the probiotic treatment, genes related to post-translation modification and inflammatory responses were up-regulated relative to controls. Our qPCR results revealed significant effects of treatment (antibiotic and probiotic) on rabep2, aifm3, manf, prmt3 gene transcription. Moreover, we found significant associations between members of Lactobacillaceae and Aeromonadaceae with host gene expression patterns. Overall, our analysis showed that the microbiota had significant impacts on many host signaling pathways, specifically targeting immune, developmental, and metabolic processes. Our characterization of some of the molecular mechanisms involved in microbiome-host interactions will help develop new strategies for preventing/ treating microbiome disruption-related diseases.

Investigating the role of genetic variation in vgll3 and six6 in the domestication of gilthead seabream (Sparus aurata Linnaeus) and European seabass (Dicentrarchus labrax Linnaeus)

“…Interestingly, the mboat2 gene, along with six6 and vgll3 , has been linked to sea age at maturity in Atlantic salmon (Sinclair‐Waters et al., 2022). The expression of the kidins220 gene in Chinook salmon was influenced by the modification of gastrointestinal tract microbiota with the use of antibiotics and probiotics (Sadeghi et al., 2022). The id2 gene, together with the id1 in teleosts, plays a role in the control the early myogenesis and the phenotype of the muscle fibres (Rallière et al., 2004).…”

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

“…36 Probiotics are live microorganisms which confer a health benefit to the host. 37,38 Probiotics can serve as food additives designed to create a healthy gut environment, 39 and can aid in modulating brain activity, 40 gene expression [41][42][43][44] and subsequent behavioral responses. 45 Probiotics have been widely used in aquaculture, 11 including the commercial probiotic mix used in our study, 46 and can possibly overcome some of the drawbacks of triploidy.…”

“…These effects include increased growth‐related gene transcription (i.e., GH and insulin‐like growth factor 1 receptor) (e.g., Senegalese sole larvae ( Solea senegalensis ) 42 and rainbow trout ( Oncorhynchus mykiss ) 43 ); and expression of heat shock proteins (i.e., HSP70 and HSP90AA) related to stress response and possibly indicative of increased resistance to stressful situations 42 . Downregulation of genes involved in meiosis, intracellular protein transport, cell adhesion, and so on, as well as upregulation of genes related to post translation modifications (e.g., Chinook salmon 44 ) have also been observed, possibly indicative of microbial alterations to host signaling pathways.…”