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      Dietary Energy Level Promotes Rumen Microbial Protein Synthesis by Improving the Energy Productivity of the Ruminal Microbiome

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          Abstract

          Improving the yield of rumen microbial protein (MCP) has significant importance in the promotion of animal performance and the reduction of protein feed waste. The amount of energy supplied to rumen microorganisms is an important factor affecting the amount of protein nitrogen incorporated into rumen MCP. Substrate-level phosphorylation (SLP) and electron transport phosphorylation (ETP) are two major mechanisms of energy generation within microbial cells. However, the way that energy and protein levels in the diet impact the energy productivity of the ruminal microbiome and, thereafter, rumen MCP yields is not known yet. In present study, we have investigated, by animal experiments and metagenome shotgun sequencing, the effects of energy-rich and protein-rich diets on rumen MCP yields, as well as SLP-coupled and ETP-coupled energy productivity of the ruminal microbiome. We have found that an energy-rich diet induces a significant increase in rumen MCP yield, whereas a protein-rich diet has no significant impacts on it. Based on 10 reconstructed pathways related to the energy metabolism of the ruminal microbiome, we have determined that the energy-rich diet induces significant increases in the total abundance of SLP enzymes coupled to the nicotinamide adenine dinucleotide (NADH) oxidation in the glucose fermentation and F-type ATPase of the electron transporter chain, whereas the protein-rich diet has no significant impact in the abundance of these enzymes. At the species level, the energy-rich diet induces significant increases in the total abundance of 15 ETP-related genera and 40 genera that have SLP-coupled fermentation pathways, whereas the protein-rich diet has no significant impact on the total abundance of these genera. Our results suggest that an increase in dietary energy levels promotes rumen energy productivity and MCP yield by improving levels of ETP and SLP coupled to glucose fermentation in the ruminal microbiome. But, an increase in dietary protein level has no such effects.

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          Fast Identification and Removal of Sequence Contamination from Genomic and Metagenomic Datasets

          High-throughput sequencing technologies have strongly impacted microbiology, providing a rapid and cost-effective way of generating draft genomes and exploring microbial diversity. However, sequences obtained from impure nucleic acid preparations may contain DNA from sources other than the sample. Those sequence contaminations are a serious concern to the quality of the data used for downstream analysis, causing misassembly of sequence contigs and erroneous conclusions. Therefore, the removal of sequence contaminants is a necessary and required step for all sequencing projects. We developed DeconSeq, a robust framework for the rapid, automated identification and removal of sequence contamination in longer-read datasets ( 150 bp mean read length). DeconSeq is publicly available as standalone and web-based versions. The results can be exported for subsequent analysis, and the databases used for the web-based version are automatically updated on a regular basis. DeconSeq categorizes possible contamination sequences, eliminates redundant hits with higher similarity to non-contaminant genomes, and provides graphical visualizations of the alignment results and classifications. Using DeconSeq, we conducted an analysis of possible human DNA contamination in 202 previously published microbial and viral metagenomes and found possible contamination in 145 (72%) metagenomes with as high as 64% contaminating sequences. This new framework allows scientists to automatically detect and efficiently remove unwanted sequence contamination from their datasets while eliminating critical limitations of current methods. DeconSeq's web interface is simple and user-friendly. The standalone version allows offline analysis and integration into existing data processing pipelines. DeconSeq's results reveal whether the sequencing experiment has succeeded, whether the correct sample was sequenced, and whether the sample contains any sequence contamination from DNA preparation or host. In addition, the analysis of 202 metagenomes demonstrated significant contamination of the non-human associated metagenomes, suggesting that this method is appropriate for screening all metagenomes. DeconSeq is available at http://deconseq.sourceforge.net/.
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            Electricity Production by Geobacter sulfurreducens Attached to Electrodes

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              The Genome Sequence of the Rumen Methanogen Methanobrevibacter ruminantium Reveals New Possibilities for Controlling Ruminant Methane Emissions

              Background Methane (CH4) is a potent greenhouse gas (GHG), having a global warming potential 21 times that of carbon dioxide (CO2). Methane emissions from agriculture represent around 40% of the emissions produced by human-related activities, the single largest source being enteric fermentation, mainly in ruminant livestock. Technologies to reduce these emissions are lacking. Ruminant methane is formed by the action of methanogenic archaea typified by Methanobrevibacter ruminantium, which is present in ruminants fed a wide variety of diets worldwide. To gain more insight into the lifestyle of a rumen methanogen, and to identify genes and proteins that can be targeted to reduce methane production, we have sequenced the 2.93 Mb genome of M. ruminantium M1, the first rumen methanogen genome to be completed. Methodology/Principal Findings The M1 genome was sequenced, annotated and subjected to comparative genomic and metabolic pathway analyses. Conserved and methanogen-specific gene sets suitable as targets for vaccine development or chemogenomic-based inhibition of rumen methanogens were identified. The feasibility of using a synthetic peptide-directed vaccinology approach to target epitopes of methanogen surface proteins was demonstrated. A prophage genome was described and its lytic enzyme, endoisopeptidase PeiR, was shown to lyse M1 cells in pure culture. A predicted stimulation of M1 growth by alcohols was demonstrated and microarray analyses indicated up-regulation of methanogenesis genes during co-culture with a hydrogen (H2) producing rumen bacterium. We also report the discovery of non-ribosomal peptide synthetases in M. ruminantium M1, the first reported in archaeal species. Conclusions/Significance The M1 genome sequence provides new insights into the lifestyle and cellular processes of this important rumen methanogen. It also defines vaccine and chemogenomic targets for broad inhibition of rumen methanogens and represents a significant contribution to worldwide efforts to mitigate ruminant methane emissions and reduce production of anthropogenic greenhouse gases.
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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
                17 April 2019
                2019
                : 10
                : 847
                Affiliations
                [1] 1The Key Laboratory of Animal Physiology and Biochemistry, College of Veterinary Medicine, Nanjing Agricultural University , Nanjing, China
                [2] 2College of Life Science, Nanjing Agricultural University , Nanjing, China
                [3] 3Bioinformatics Center, Nanjing Agricultural University , Nanjing, China
                [4] 4College of Agriculture, Nanjing Agricultural University , Nanjing, China
                Author notes

                Edited by: Garret Suen, University of Wisconsin-Madison, United States

                Reviewed by: Shengguo Zhao, Institute of Animal Sciences (CAAS), China; Luciano Takeshi Kishi, São Paulo State University, Brazil; Hilario C. Mantovani, Universidade Federal de Viçosa, Brazil

                *Correspondence: Hong Shen, hongshen@ 123456njau.edu.cn

                These authors have contributed equally to this work

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

                Article
                10.3389/fmicb.2019.00847
                6479175
                31057531
                7cd457e3-ac39-4235-9043-9d6e5e171ed1
                Copyright © 2019 Lu, Xu, Shen, Tian and Shen.

                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) and the copyright owner(s) 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
                : 29 November 2018
                : 02 April 2019
                Page count
                Figures: 3, Tables: 5, Equations: 0, References: 47, Pages: 14, Words: 0
                Funding
                Funded by: National Natural Science Foundation of China 10.13039/501100001809
                Funded by: Natural Science Foundation of Jiangsu Province 10.13039/501100004608
                Categories
                Microbiology
                Original Research

                Microbiology & Virology
                rumen microbiome,energy productivity,substrate-level phosphorylation,electron transport phosphorylation,microbial protein synthesis,dietary modulation

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