Abstract

BackgroundRumen microbes play a greater role in host energy acquisition than that of gut-associated microbes in monogastric animals. Although genome-enabled advancements are providing access to the vast diversity of uncultivated microbes, our understanding of variables shaping rumen microbial communities is in its infancy. Viruses have been shown to impact microbial populations through a myriad of processes, including cell lysis and reprogramming of host metabolism. However, little is known about the processes shaping the distribution of rumen viruses or how viruses may modulate microbial-driven processes in the rumen. To this end, we investigated how rumen bacterial and viral community structure and function responded in five steers fed four randomized dietary treatments in a crossover design.ResultsTotal digestible nutrients (TDN), a measure of dietary energy, best explained the variation in bacterial and viral communities. Additional ecological drivers of viral communities included dietary zinc content and microbial functional diversity. Using partial least squares regression, we demonstrate significant associations between the abundances of 267 viral populations and variables driving the variation in rumen viral communities. While rumen viruses were dynamic, 14 near ubiquitous viral populations were identified, suggesting the presence of a core rumen virome largely comprised of novel viruses. Moreover, analysis of virally encoded auxiliary metabolic genes (AMGs) indicates rumen viruses have glycosidic hydrolases to potentially augment the breakdown of complex carbohydrates to increase energy production. Other AMGs identified have a role in redirecting carbon to the pentose phosphate pathway and one carbon pools by folate to boost viral replication.ConclusionsWe demonstrate that rumen bacteria and viruses have differing responses and ecological drivers to dietary perturbation. Our results show that rumen viruses have implications for understanding the structuring of the previously identified core rumen microbiota and impacting microbial metabolism through a vast array of AMGs. AMGs in the rumen appear to have consequences for microbial metabolism that are largely in congruence with the current paradigm established in marine systems. This study provides a foundation for future hypotheses regarding the dynamics of viral-mediated processes in the rumen.

Highlights

  • Rumen microbes play a greater role in host energy acquisition than that of gut-associated microbes in monogastric animals

  • Rumen pH differed by diet (P = 0.002, F = 11.540, three-way ANOVA considering effects of diet, period, and host animal; Additional file 1), while total Volatile fatty acid (VFA) altered by host animal (P = 0.016, F = 5.496) and period (P = 0.021, F = 5.431), but not diet (P = 0.110, F = 2.686)

  • Diet and host animal influence the population and functional response of rumen microbial and viral communities Using the abundances of viral populations and bacterial Operational taxonomic unit (OTU) across samples, we explored the global effects of diet on viral and bacterial diversity in the rumen

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Summary

Introduction

Rumen microbes play a greater role in host energy acquisition than that of gut-associated microbes in monogastric animals. Central to grazing ruminants are the nutrient and energy transformations in the rumen that are driven by a complex community of largely uncharacterized microbes [3] This microbial consortia can utilize a broad range of substrates including cellulose-rich substrates of mainly indigestible plant material and convert it into energy sources such as volatile fatty acids (VFAs) and microbial cell protein for host absorption and metabolism [4, 5]. The synergistic actions of rumen microbes and assimilation of fermentation end products account for ~ 70% of the ruminant animal’s energy needs [6] This is far greater than the contribution of hindgut fermentation to energy acquisition in monogastric mammals (~ 10–30%) [6]. While there is a growing understanding of the importance of rumen microbes in regard to ruminant health and productivity, the roles of viruses in shaping rumen microbial communities and in turn ecosystem function are not well established

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