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      Redundancy, resilience, and host specificity of the ruminal microbiota: implications for engineering improved ruminal fermentations

      review-article
      1 , 2
      Frontiers in Microbiology
      Frontiers Media S.A.
      fermentation, host specificity, redundancy, resilience, rumen

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          Abstract

          The ruminal microbial community is remarkably diverse, containing 100s of different bacterial and archaeal species, plus many species of fungi and protozoa. Molecular studies have identified a “core microbiome” dominated by phyla Firmicutes and Bacteroidetes, but also containing many other taxa. The rumen provides an ideal laboratory for studies on microbial ecology and the demonstration of ecological principles. In particular, the microbial community demonstrates both redundancy (overlap of function among multiple species) and resilience (resistance to, and capacity to recover from, perturbation). These twin properties provide remarkable stability that maintains digestive function for the host across a range of feeding and management conditions, but they also provide a challenge to engineering the rumen for improved function (e.g., improved fiber utilization or decreased methane production). Direct ruminal dosing or feeding of probiotic strains often fails to establish the added strains, due to intensive competition and amensalism from the indigenous residents that are well-adapted to the historical conditions within each rumen. Known exceptions include introduced strains that can fill otherwise unoccupied niches, as in the case of specialist bacteria that degrade phytotoxins such as mimosine or fluoroacetate. An additional complicating factor in manipulating the ruminal fermentation is the individuality or host specificity of the microbiota, in which individual animals contain a particular community whose species composition is capable of reconstituting itself, even following a near-total exchange of ruminal contents from another herd mate maintained on the same diet. Elucidation of the interactions between the microbial community and the individual host that establish and maintain this specificity may provide insights into why individual hosts vary in production metrics (e.g., feed efficiency or milk fat synthesis), and how to improve herd performance.

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          The Keystone-Species Concept in Ecology and Conservation

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            Composition and Similarity of Bovine Rumen Microbiota across Individual Animals

            The bovine rumen houses a complex microbiota which is responsible for cattle's remarkable ability to convert indigestible plant mass into food products. Despite this ecosystem's enormous significance for humans, the composition and similarity of bacterial communities across different animals and the possible presence of some bacterial taxa in all animals' rumens have yet to be determined. We characterized the rumen bacterial populations of 16 individual lactating cows using tag amplicon pyrosequencing. Our data showed 51% similarity in bacterial taxa across samples when abundance and occurrence were analyzed using the Bray-Curtis metric. By adding taxon phylogeny to the analysis using a weighted UniFrac metric, the similarity increased to 82%. We also counted 32 genera that are shared by all samples, exhibiting high variability in abundance across samples. Taken together, our results suggest a core microbiome in the bovine rumen. Furthermore, although the bacterial taxa may vary considerably between cow rumens, they appear to be phylogenetically related. This suggests that the functional requirement imposed by the rumen ecological niche selects taxa that potentially share similar genetic features.
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              Methane yield phenotypes linked to differential gene expression in the sheep rumen microbiome

              Ruminant livestock represent the single largest anthropogenic source of the potent greenhouse gas methane, which is generated by methanogenic archaea residing in ruminant digestive tracts. While differences between individual animals of the same breed in the amount of methane produced have been observed, the basis for this variation remains to be elucidated. To explore the mechanistic basis of this methane production, we measured methane yields from 22 sheep, which revealed that methane yields are a reproducible, quantitative trait. Deep metagenomic and metatranscriptomic sequencing demonstrated a similar abundance of methanogens and methanogenesis pathway genes in high and low methane emitters. However, transcription of methanogenesis pathway genes was substantially increased in sheep with high methane yields. These results identify a discrete set of rumen methanogens whose methanogenesis pathway transcription profiles correlate with methane yields and provide new targets for CH4 mitigation at the levels of microbiota composition and transcriptional regulation.
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                Author and article information

                Contributors
                Journal
                Front Microbiol
                Front Microbiol
                Front. Microbiol.
                Frontiers in Microbiology
                Frontiers Media S.A.
                1664-302X
                10 April 2015
                2015
                : 6
                : 296
                Affiliations
                [1] 1US Dairy Forage Research Center, US Department of Agriculture – Agricultural Research Service Madison, WI, USA
                [2] 2Department of Bacteriology, University of Wisconsin Madison, WI, USA
                Author notes

                Edited by: Emilio M. Ungerfeld, Instituto de Investigaciones Agropecuarias-Carillanca, Chile

                Reviewed by: Diego P. Morgavi, Institute National de la Recherche Agronomique, France; Hilary G. Morrison, Marine Biological Laboratory, USA

                *Correspondence: Paul J. Weimer, US Department of Agriculture – Agricultural Research Service, US Dairy Forage Research Center, 1925 Linden Drive West, Madison, WI 53706, USA paul.weimer@ 123456ars.usda.gov

                This article was submitted to Systems Microbiology, a section of the journal Frontiers in Microbiology

                Article
                10.3389/fmicb.2015.00296
                4392294
                25914693
                24a092c9-5c3c-4e55-91f2-022d4ae384df
                Copyright © 2015 Weimer.

                This is an open-access article distributed under the terms of the Creative Commons Attribution License (CC BY). The use, distribution or reproduction in other forums is permitted, provided the original author(s) or licensor are credited and that the original publication in this journal is cited, in accordance with accepted academic practice. No use, distribution or reproduction is permitted which does not comply with these terms.

                History
                : 20 February 2015
                : 11 March 2015
                Page count
                Figures: 0, Tables: 6, Equations: 0, References: 146, Pages: 16, Words: 0
                Categories
                Microbiology
                Review

                Microbiology & Virology
                fermentation,host specificity,redundancy,resilience,rumen
                Microbiology & Virology
                fermentation, host specificity, redundancy, resilience, rumen

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