Abstract

The gut microbiota is a complex ecological community that plays multiple critical roles within a host. Known intrinsic and extrinsic factors affect gut microbiota structure, but the influence of host genetics is understudied. To investigate the role of host genetics upon the gut microbiota structure, we performed a longitudinal study in which we evaluated the hindgut microbiota and its association with animal growth and immunity across life. We evaluated three different growth stages in an Angus-Brahman multibreed population with a graduated spectrum of genetic variation, raised under variable environmental conditions and diets. We found the gut microbiota structure was changed significantly during growth when preweaning, and fattening calves experienced large variations in diet and environmental changes. However, regardless of the growth stage, we found gut microbiota is significantly influenced by breed composition throughout life. Host genetics explained the relative abundances of 52.2%, 40.0%, and 37.3% of core bacterial taxa at the genus level in preweaning, postweaning, and fattening calves, respectively. Sutterella, Oscillospira, and Roseburia were consistently associated with breed composition at these three growth stages. Especially, butyrate-producing bacteria, Roseburia and Oscillospira, were associated with nine single-nucleotide polymorphisms (SNPs) located in genes involved in the regulation of host immunity and metabolism in the hindgut. Furthermore, minor allele frequency analysis found breed-associated SNPs in the short-chain fatty acids (SCFAs) receptor genes that promote anti-inflammation and enhance intestinal epithelial barrier functions. Our findings provide evidence of dynamic and lifelong host genetic effects upon gut microbiota, regardless of growth stages. We propose that diet, environmental changes, and genetic components may explain observed variation in critical hindgut microbiota throughout life.

Highlights

  • The gut microbial community is dynamic and complex

  • These findings indicate that genetic variations in short-chain fatty acids (SCFAs) receptors, especially in GPR109A and GPR43, may contribute to the observed differences in immune response and energy harvest among the multibreed Angus-Brahman (MAB) population (Fig. 7B)

  • We show that gut microbiota structure is influenced by host genetics throughout life

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Summary

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The gut microbial community is dynamic and complex. It is populated by trillions of microorganisms that consist. Recent findings challenge the statistical significance of associations between host SNPs and bacterial taxa in a chicken model, and show that influences of the environment and diet dominate host genetics in shaping the gut microbiota [8, 12, 17] This uncertainty is due in part to the difficulty of controlling extrinsic factors that influence the microbial community among individuals, such as variations in diet, age, and environmental conditions. We hypothesized that repeated measures of the gut microbiota in a cohort of animals with different genetic backgrounds raised under variable diet and environmental conditions would reveal readily apparent host genetic effects on gut microbiota development To test this hypothesis, we deepened the understanding of host genetic effects in shaping the hindgut microbiota using the MAB population throughout the production lifecycle. We investigated how host genetic effects upon gut microbiota may affect animal growth rates and immune responses by identifying specific host genes at different growth stages that are known to be associated with bacteria related to weight gain and immunity

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