Thermodynamic Driving Force of Hydrogen on Rumen Microbial Metabolism: A Theoretical Investigation.

Henk J Van Lingen,James G Fadel,Caroline M Plugge,André Bannink,Jan Dijkstra,Ermias Kebreab,John M Senko

doi:10.1371/journal.pone.0161362

Henk J Van Lingen, James G Fadel + Show 5 more

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https://doi.org/10.1371/journal.pone.0161362

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Abstract

Hydrogen is a key product of rumen fermentation and has been suggested to thermodynamically control the production of the various volatile fatty acids (VFA). Previous studies, however, have not accounted for the fact that only thermodynamic near-equilibrium conditions control the magnitude of reaction rate. Furthermore, the role of NAD, which is affected by hydrogen partial pressure (PH2), has often not been considered. The aim of this study was to quantify the control of PH2 on reaction rates of specific fermentation pathways, methanogenesis and NADH oxidation in rumen microbes. The control of PH2 was quantified using the thermodynamic potential factor (FT), which is a dimensionless factor that corrects a predicted kinetic reaction rate for the thermodynamic control exerted. Unity FT was calculated for all glucose fermentation pathways considered, indicating no inhibition of PH2 on the production of a specific type of VFA (e.g., acetate, propionate and butyrate) in the rumen. For NADH oxidation without ferredoxin oxidation, increasing PH2 within the rumen physiological range decreased FT from unity to zero for different NAD+ to NADH ratios and pH of 6.2 and 7.0, which indicates thermodynamic control of PH2. For NADH oxidation with ferredoxin oxidation, increasing PH2 within the rumen physiological range decreased FT from unity at pH of 7.0 only. For the acetate to propionate conversion, FT increased from 0.65 to unity with increasing PH2, which indicates thermodynamic control. For propionate to acetate and butyrate to acetate conversions, FT decreased to zero below the rumen range of PH2, indicating full thermodynamic suppression. For methanogenesis by archaea without cytochromes, FT differed from unity only below the rumen range of PH2, indicating no thermodynamic control. This theoretical investigation shows that thermodynamic control of PH2 on individual VFA produced and associated yield of hydrogen and methane cannot be explained without considering NADH oxidation.

Highlights

Carbohydrates ingested by ruminants are degraded into monomers by action of rumen microbial enzymes and subsequently fermented to products such as volatile fatty acids (VFA) and alcohols
The NADH, a cofactor carrying electrons, needs to be oxidized back to NAD+ to keep the glycolysis possible and to maintain further metabolic steps of the overall microbial metabolism that depend on pyruvate [1, 2]
NADH is oxidized via H2 production, which is thermodynamically inhibited at elevated hydrogen partial pressure (PH2)

Summary

Introduction

Carbohydrates ingested by ruminants are degraded into monomers by action of rumen microbial enzymes and subsequently fermented to products such as volatile fatty acids (VFA) and alcohols. The oxidation of NADH to NAD+ may be directly coupled to the product formation from pyruvate that follows glycolysis. Acetate is quantitatively the main VFA in the rumen, but its production from pyruvate is not directly coupled to the oxidation of NADH. In this case, NADH is oxidized via H2 production, which is thermodynamically inhibited at elevated hydrogen partial pressure (PH2). Many methanogenic archaea utilize H2 to reduce CO2 to CH4 This keeps PH2 at a low level, which enables NADH oxidation in bacteria that are not able to directly couple NADH oxidation to reduction of metabolites [4]

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