Rumen Microbiome from Steers Differing in Feed Efficiency

RESEARCH ARTICLE Rumen Microbiome from Steers Differing in Feed Efficiency Phillip R. Myer☯, Timothy P. L. Smith☯, James E. Wells☯, Larry A. Kuehn☯, Harvey C. Freetly*☯ USDA, ARS, U.S. Meat Animal Research Center, Clay Center, Nebraska, United States of America ☯ These authors contributed equally to this work. * a11111 OPEN ACCESS Citation: Myer PR, Smith TPL, Wells JE, Kuehn LA, Freetly HC (2015) Rumen Microbiome from Steers Differing in Feed Efficiency. PLoS ONE 10(6): e0129174. doi:10.1371/journal.pone.0129174 Academic Editor: Robert J Forster, Agriculture and Agri-Food Canada, CANADA Received: October 9, 2014 Accepted: May 5, 2015 Published: June 1, 2015 Copyright: This is an open access article, free of all copyright, and may be freely reproduced, distributed, transmitted, modified, built upon, or otherwise used by anyone for any lawful purpose. The work is made available under the Creative Commons CC0 public domain dedication. Data Availability Statement: Sequence data is available from the NCBI Sequence Read Archive (SRA Accession SRP047292). Additional descriptive information is associated with NCBI BioProject PRJNA261425. Funding: This project was supported by Agriculture and Food Research Initiative Competitive Grant No. 2011-68004-30214 from the USDA National Institute of Food Agriculture as well as the USDA, Agricultural Research Service. Competing Interests: The authors have declared that no competing interests exist. Abstract The cattle rumen has a diverse microbial ecosystem that is essential for the host to digest plant material. Extremes in body weight (BW) gain in mice and humans have been associated with different intestinal microbial populations. The objective of this study was to characterize the microbiome of the cattle rumen among steers differing in feed efficiency. Two contemporary groups of steers (n=148 and n=197) were fed a ration (dry matter basis) of 57.35% dry-rolled corn, 30% wet distillers grain with solubles, 8% alfalfa hay, 4.25% supplement, and 0.4% urea for 63 days. Individual feed intake (FI) and BW gain were determined. Within contemporary group, the four steers within each Cartesian quadrant were sampled (n=16/group) from the bivariate distribution of average daily BW gain and average daily FI. Bacterial 16S rRNA gene amplicons were sequenced from the harvested bovine rumen fluid samples using next-generation sequencing technology. No significant changes in diversity or richness were indicated, and UniFrac principal coordinate analysis did not show any separation of microbial communities within the rumen. However, the abundances of relative microbial populations and operational taxonomic units did reveal significant differences with reference to feed efficiency groups. Bacteroidetes and Firmicutes were the dominant phyla in all ruminal groups, with significant population shifts in relevant ruminal taxa, including phyla Firmicutes and Lentisphaerae, as well as genera Succiniclasticum, Lactobacillus, Ruminococcus, and Prevotella. This study suggests the involvement of the rumen microbiome as a component influencing the efficiency of weight gain at the 16S level, which can be utilized to better understand variations in microbial ecology as well as host factors that will improve feed efficiency. Introduction The bovine gastrointestinal (GI) tract is a complex system that is responsible for animal nutrient uptake and overall health. Rumen function and the microbiology of culturable rumen microorganisms has been well-studied, but it has only been since the advent of next-generation sequencing technology in the last decade that research on total microbial diversity, microbial PLOS ONE | DOI:10.1371/journal.pone.0129174 June 1, 2015 1 / 17 Rumen Microbiome Feed Efficiency community function, and their effects on the host could be quantitatively examined at a higher resolution. These new technologies have enabled a thorough examination of the host microbiota, independent of culture-based methods. The gastrointestinal tract is host to a diverse microbial ecosystem that can vary depending on both host genetic and environmental factors [1]. Studies have shown that even minor shifts in these populations can have a tremendous impact on livestock nutrition and productivity [2–4]. Changes in the composition and diversity of the ruminal microbiota have been linked with diet and age [5]. Extremes in body weight (BW) gain in mice and humans have been associated with different intestinal microbial populations [6–7]. However, the majority of research in cattle has focused on the microbial responses to changes in external parameters, such as diet influences, and management practices [8–9]. Little has been done to examine the effect of differing microbial populations on host phenotypes, specifically related to performance and feed efficiency. Furthermore, many of these studies lack adequate sample size; examining only a few subjects. With advances in sequencing technology, researchers can examine these relationships with greater depth and coverage than has previously been reported. Feed costs remain the largest variable cost in beef production [10]. Optimizing feed efficiency in cattle has long been an effort devoted to host genetics, management, and diet. Yet, data supports possible microbial interactions within the host, influencing a multitude of processes pertaining to digestion and the host GI tract. We hypothesize that variable microbial populations have differential abilities to degrade feedstuffs in the rumen into nutrients available for absorption, as a possible route to impacting feed efficiency. This study aimed to characterize the microbiome, specifically the bacterial community, of the cattle rumen among steers differing in feed intake and growth, in order to assess the association of the ruminal microbial community profile with variation in bovine feed efficiency. Materials and Methods Ethics Statement This experiment was approved by the U.S. Meat Animal Research Center Animal Care and Use Committee. Experimental design and rumen sampling Steers selected for this study came from a populations of cattle being developed to have a high percentage of the following breeds: Angus, Beefmaster, Brahman, Brangus, Braunvieh, Charolais, Chiangus, Gelbvieh, Hereford, Limousin, Maine Anjou, Red Angus, Salers, Santa Gertrudis, Shorthorn, Simmental, South Devon, and Tarentaise. Each year heifers and cows were artificially inseminated with semen from prominent industry bulls of their dominant breed. This program resulted in offspring ranging from 50% to 75% of the same breed as their sire with the exception of Angus and Hereford which ranged from 50% to 100% of the same breed as their sire. Individual feed intake was measured using an Insentec feeding system (Marknesse, The Netherlands). Steers were fed a ration (dry matter basis) of 57.35% dry-rolled corn, 30% wet distillers grain with solubles, 8% alfalfa hay, 4.25% supplement (containing (...truncated)