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

Zhongyan Lu; Zhihui Xu; Zanming Shen; Yuanchun Tian; Hong Shen

doi:10.3389/fmicb.2019.00847

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

Front Microbiol. 2019 Apr 17:10:847. doi: 10.3389/fmicb.2019.00847. eCollection 2019.

Authors

Zhongyan Lu¹, Zhihui Xu^{2

3}, Zanming Shen¹, Yuanchun Tian⁴, Hong Shen^{2

3}

Affiliations

¹ The Key Laboratory of Animal Physiology and Biochemistry, College of Veterinary Medicine, Nanjing Agricultural University, Nanjing, China.
² College of Life Science, Nanjing Agricultural University, Nanjing, China.
³ Bioinformatics Center, Nanjing Agricultural University, Nanjing, China.
⁴ College of Agriculture, Nanjing Agricultural University, Nanjing, China.

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.

Keywords: dietary modulation; electron transport phosphorylation; energy productivity; microbial protein synthesis; rumen microbiome; substrate-level phosphorylation.