Research Article: Perturbation Dynamics of the Rumen Microbiota in Response to Exogenous Butyrate

Date Published: January 12, 2012

Publisher: Public Library of Science

Author(s): Robert W. Li, Sitao Wu, Ransom L. Baldwin, Weizhong Li, Congjun Li, David M. Ojcius. http://doi.org/10.1371/journal.pone.0029392

Abstract

The capacity of the rumen microbiota to produce volatile fatty acids (VFAs) has important implications in animal well-being and production. We investigated temporal changes of the rumen microbiota in response to butyrate infusion using pyrosequencing of the 16S rRNA gene. Twenty one phyla were identified in the rumen microbiota of dairy cows. The rumen microbiota harbored 54.5±6.1 genera (mean ± SD) and 127.3±4.4 operational taxonomic units (OTUs), respectively. However, the core microbiome comprised of 26 genera and 82 OTUs. Butyrate infusion altered molar percentages of 3 major VFAs. Butyrate perturbation had a profound impact on the rumen microbial composition. A 72 h-infusion led to a significant change in the numbers of sequence reads derived from 4 phyla, including 2 most abundant phyla, Bacteroidetes and Firmicutes. As many as 19 genera and 43 OTUs were significantly impacted by butyrate infusion. Elevated butyrate levels in the rumen seemingly had a stimulating effect on butyrate-producing bacteria populations. The resilience of the rumen microbial ecosystem was evident as the abundance of the microorganisms returned to their pre-disturbed status after infusion withdrawal. Our findings provide insight into perturbation dynamics of the rumen microbial ecosystem and should guide efforts in formulating optimal uses of probiotic bacteria treating human diseases.

Partial Text

Volatile fatty acids (VFAs or short-chain fatty acids), such as acetate, butyrate and propionate, are major fermentation products of microorganisms in the rumen and hindgut. VFAs contribute up to 70% of the total metabolizable energy supply in ruminants [1]. In addition to their energetic or nutritional roles, VFAs are able to regulate animal physiology, including cholesterol synthesis and insulin and glucagon secretion. For example, butyrate is a preferred energy source for ruminal epithelial cells [2]. Most importantly, it has a multitude of cellular regulatory effects, such as modulating cell differentiation and motility, inducing apoptosis, and inhibiting cell proliferation [3], [4]. Intraruminal infusion of VFAs, including butyrate, has been used to study the effect of nutrient supply on milk secretion [5] and nutrient partition, liver physiology, lipid metabolism, and rumen wall development, as well as ruminal pH maintenance [6]–[8]. A decreased ratio of glucogenic (propionate)/lipogenic (acetate and butyrate) in ruminal VFAs could decrease hepatic gluconeogenesis [9], leading to a reduction in milk fat secretion [10]. Steady-state ruminal butyrate concentration reflects a delicate balance between butyrate production by rumen microbes and its clearance, mainly via epithelial absorption. Many attempts have been made to identify butyrate-producing bacteria in the human gut and the rumen [11]–[13]. However, little is known about the ecological and physiological role of predominant butyrate-producing bacteria in the rumen microbial ecosystem. The community level response of rumen microorganisms to exogenous VFAs, such as butyrate, has yet to be understood. While biochemical processes leading to butyrate biosynthesis is well described [14], the rumen microorganisms involved in this process have yet to be fully identified. In this study, we attempted to understand the effect of butyrate perturbation on the rumen microbial community composition and dynamics.

The rumen microbiota plays an essential role in nutrient production and utilization in ruminants [15], [16]. Efficient microbial transformation of plant fibers results in production of VFAs, which are subsequently used to produce meat and milk for human consumption. Rumen fermentation is poorly understood process controlled by the interacting rumen microbiota constituents. Understanding of microbial interactions and dynamics in the rumen microbial ecosystem should provide a scientific basis for successful manipulation of ruminal fermentation for optimal outcomes. In this study, we characterized temporal changes of the rumen microbiota of dairy cows in their mid-lactation in response to an exogenous butyrate disturbance. We identified 21 prokaryotic phyla in the rumen microbial community, which were dominated by 2 phyla, Bacteroidetes and Firmicutes. Together, these 2 phyla accounted for up to 93% of all 16S rRNA gene sequences. Compared to the rumen of 12-month-old steers fed a similar hay-based diet, where 16S rRNA gene sequences can be assigned to 15 bacterial phyla [16], the rumen microbiota of mid-lactating dairy cows displayed some unique features. One of the salient features was prominent establishment of bacteria from a candidate phylum SR1 in the community, which was absent from the rumen of 12-month-old steers. The role of these bacteria in the rumen microbial ecosystem remains unknown.

Source:

http://doi.org/10.1371/journal.pone.0029392