Comparison of Channel Catfish and Blue Catfish Gut Microbiota Assemblages Shows Minimal Effects of Host Genetics on Microbial Structure and Inferred Function.

Jacob W Bledsoe,Geoffrey C Waldbieser,Kelly S Swanson,Brian C Small,Brian C Peterson

doi:10.3389/fmicb.2018.01073

Abstract

The microbiota of teleost fish has gained a great deal of research attention within the past decade, with experiments suggesting that both host-genetics and environment are strong ecological forces shaping the bacterial assemblages of fish microbiomes. Despite representing great commercial and scientific importance, the catfish within the family Ictaluridae, specifically the blue and channel catfish, have received very little research attention directed toward their gut-associated microbiota using 16S rRNA gene sequencing. Within this study we utilize multiple genetically distinct strains of blue and channel catfish, verified via microsatellite genotyping, to further quantify the role of host-genetics in shaping the bacterial communities in the fish gut, while maintaining environmental and husbandry parameters constant. Comparisons of the gut microbiota among the two catfish species showed no differences in bacterial species richness (observed and Chao1) or overall composition (weighted and unweighted UniFrac) and UniFrac distances showed no correlation with host genetic distances (Rst) according to Mantel tests. The microbiota of environmental samples (diet and water) were found to be significantly more diverse than that of the catfish gut associated samples, suggesting that factors within the host were further regulating the bacterial communities, despite the lack of a clear connection between microbiota composition and host genotype. The catfish gut communities were dominated by the phyla Fusobacteria, Proteobacteria, and Firmicutes; however, differential abundance analysis between the two catfish species using analysis of composition of microbiomes detected two differential genera, Cetobacterium and Clostridium XI. The metagenomic pathway features inferred from our dataset suggests the catfish gut bacterial communities possess pathways beneficial to their host such as those involved in nutrient metabolism and antimicrobial biosynthesis, while also containing pathways involved in virulence factors of pathogens. Testing of the inferred KEGG (Kyoto Encyclopedia of Genes and Genomes) pathways by DESeq2 revealed minor difference in microbiota function, with only two metagenomic pathways detected as differentially abundant between the two catfish species. As the first study to characterize the gut microbiota of blue catfish, our study results have direct implications on future ictalurid catfish research. Additionally, our insight into the intrinsic factors driving microbiota structure has basic implications for the future study of fish gut microbiota.

Highlights

The aquaculture industry has seen a great deal of interest in pre, pro, and synbiotic supplementation to modulate the gut microbiota of fish, primarily due to their anticipated efficacy in improving growth rates, feed conversion ratios, and replacing the use of antibiotics to maintain fish health
While this body of research has indicated that the microbiota of fish certainly merits research attention due to their known function, the challenge lies in controlling the variability of the teleost microbiota and better understanding the factors affecting microbial community assemblages in cultured fish species to allow for more effective manipulation of their composition and function
After applying the filtering steps outlined in the section “Materials and Methods,” a total of 2,735,946 high-quality 16S rRNA V4 gene amplicon sequences were obtained from the 42 gut-associated microbiota samples, yet a high level of variation in library size was still present after filtering (66,993 ± 43,547; mean ± SD)

Summary

Introduction

The aquaculture industry has seen a great deal of interest in pre-, pro-, and synbiotic supplementation to modulate the gut microbiota of fish, primarily due to their anticipated efficacy in improving growth rates, feed conversion ratios, and replacing the use of antibiotics to maintain fish health. The physiological utility of the gut-associated microbiota of teleosts has been proven, with many studies implicating the microbiota in host functions such as lipid metabolism and absorption (Semova et al, 2012), vitamin and mineral metabolism (Tsuchiya et al, 2008), digestion of complex feedstuffs (Wu et al, 2012; Di Maiuta et al, 2013; Ni et al, 2014), disease resistance and immune function (Pérez et al, 2010; Galindo-Villegas et al, 2012; Ran et al, 2012; Gomez et al, 2013), and development of the gastrointestinal tract and other tissues (Rawls et al, 2004; Hill et al, 2016) While this body of research has indicated that the microbiota of fish certainly merits research attention due to their known function, the challenge lies in controlling the variability of the teleost microbiota and better understanding the factors affecting microbial community assemblages in cultured fish species to allow for more effective manipulation of their composition and function. In a study using gel-electrophoresis techniques to compare the gut microbiota of four families of rainbow trout Oncorhynchus mykiss fed three different diets, Navarrete et al (2012) observed that host family, not dietary treatment, best explained differences in the gut microbiota composition

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