Bayesian mechanistic modeling of thermodynamically controlled volatile fatty acid, hydrogen and methane production in the bovine rumen

Henk J. van Lingen*, James G. Fadel, Luis E. Moraes, André Bannink, Jan Dijkstra

*Corresponding author for this work

Research output: Contribution to journalArticleAcademicpeer-review

Abstract

Dynamic modeling of mechanisms driving volatile fatty acid and hydrogen production in the rumen microbial ecosystem contributes to the heuristic prediction of CH4 emissions from dairy cattle into the environment. Existing mathematical rumen models, however, lack the representation of these mechanisms. A dynamic mechanistic model was developed that simulates the thermodynamic control of hydrogen partial pressure (pH2 ) on volatile fatty acid (VFA) fermentation pathways via the NAD+ to NADH ratio in fermentative microbes, and methanogenesis in the bovine rumen. This model is unique and closely aligns with principles of reaction kinetics and thermodynamics. Model state variables represent ruminal carbohydrate substrates, bacteria and protozoa, methanogens, and gaseous and dissolved fermentation end products. The model was extended with static equations to model the hindgut metabolism. Feed composition and twice daily feeding were used as model inputs. Model parameters were estimated to experimental data using a Bayesian calibration procedure, after which the uncertainty of the parameter distribution on the model output was assessed. The model predicted a marked peak in pH2 after feeding that rapidly declined in time. This peak in pH2 caused a decrease in NAD+ to NADH ratio followed by an increased propionate molar proportion at the expense of acetate molar proportion, and an increase in CH4 production that steadily decreased in time, although the magnitude of increase for CH4 emission was less than for pH2 . A global sensitivity analysis indicated that parameters that determine the fractional passage rate and NADH oxidation rate altogether explained 86% of the variation in predicted daily CH4 emission. Model evaluation indicated over-prediction of in vivo CH4 emissions shortly after feeding, whereas under-prediction was indicated at later times. The present rumen fermentation modeling effort uniquely provides the integration of the pH2 controlled NAD+ to NADH ratio for dynamically predicting metabolic pathways that yield VFA, H2 and CH4.

Original languageEnglish
Pages (from-to)150-165
Number of pages16
JournalJournal of Theoretical Biology
Volume480
DOIs
Publication statusPublished - 7 Nov 2019

Fingerprint

Volatile fatty acids
Bayesian Modeling
hydrogen production
Volatile Fatty Acids
Rumen
Volatiles
Methane
Fatty Acids
methane production
volatile fatty acids
NAD
Hydrogen
rumen
cattle
Fermentation
Thermodynamics
Model
Prediction
Pathway
Proportion

Keywords

  • Cattle
  • Dairy cow
  • Diurnal dynamics
  • Enteric fermentation
  • Global sensitivity analysis
  • Methanogenesis

Cite this

@article{5e224a2b43e24d80a5be265115522042,
title = "Bayesian mechanistic modeling of thermodynamically controlled volatile fatty acid, hydrogen and methane production in the bovine rumen",
abstract = "Dynamic modeling of mechanisms driving volatile fatty acid and hydrogen production in the rumen microbial ecosystem contributes to the heuristic prediction of CH4 emissions from dairy cattle into the environment. Existing mathematical rumen models, however, lack the representation of these mechanisms. A dynamic mechanistic model was developed that simulates the thermodynamic control of hydrogen partial pressure (pH2 ) on volatile fatty acid (VFA) fermentation pathways via the NAD+ to NADH ratio in fermentative microbes, and methanogenesis in the bovine rumen. This model is unique and closely aligns with principles of reaction kinetics and thermodynamics. Model state variables represent ruminal carbohydrate substrates, bacteria and protozoa, methanogens, and gaseous and dissolved fermentation end products. The model was extended with static equations to model the hindgut metabolism. Feed composition and twice daily feeding were used as model inputs. Model parameters were estimated to experimental data using a Bayesian calibration procedure, after which the uncertainty of the parameter distribution on the model output was assessed. The model predicted a marked peak in pH2 after feeding that rapidly declined in time. This peak in pH2 caused a decrease in NAD+ to NADH ratio followed by an increased propionate molar proportion at the expense of acetate molar proportion, and an increase in CH4 production that steadily decreased in time, although the magnitude of increase for CH4 emission was less than for pH2 . A global sensitivity analysis indicated that parameters that determine the fractional passage rate and NADH oxidation rate altogether explained 86{\%} of the variation in predicted daily CH4 emission. Model evaluation indicated over-prediction of in vivo CH4 emissions shortly after feeding, whereas under-prediction was indicated at later times. The present rumen fermentation modeling effort uniquely provides the integration of the pH2 controlled NAD+ to NADH ratio for dynamically predicting metabolic pathways that yield VFA, H2 and CH4.",
keywords = "Cattle, Dairy cow, Diurnal dynamics, Enteric fermentation, Global sensitivity analysis, Methanogenesis",
author = "{van Lingen}, {Henk J.} and Fadel, {James G.} and Moraes, {Luis E.} and Andr{\'e} Bannink and Jan Dijkstra",
year = "2019",
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language = "English",
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journal = "Journal of Theoretical Biology",
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}

Bayesian mechanistic modeling of thermodynamically controlled volatile fatty acid, hydrogen and methane production in the bovine rumen. / van Lingen, Henk J.; Fadel, James G.; Moraes, Luis E.; Bannink, André; Dijkstra, Jan.

In: Journal of Theoretical Biology, Vol. 480, 07.11.2019, p. 150-165.

Research output: Contribution to journalArticleAcademicpeer-review

TY - JOUR

T1 - Bayesian mechanistic modeling of thermodynamically controlled volatile fatty acid, hydrogen and methane production in the bovine rumen

AU - van Lingen, Henk J.

AU - Fadel, James G.

AU - Moraes, Luis E.

AU - Bannink, André

AU - Dijkstra, Jan

PY - 2019/11/7

Y1 - 2019/11/7

N2 - Dynamic modeling of mechanisms driving volatile fatty acid and hydrogen production in the rumen microbial ecosystem contributes to the heuristic prediction of CH4 emissions from dairy cattle into the environment. Existing mathematical rumen models, however, lack the representation of these mechanisms. A dynamic mechanistic model was developed that simulates the thermodynamic control of hydrogen partial pressure (pH2 ) on volatile fatty acid (VFA) fermentation pathways via the NAD+ to NADH ratio in fermentative microbes, and methanogenesis in the bovine rumen. This model is unique and closely aligns with principles of reaction kinetics and thermodynamics. Model state variables represent ruminal carbohydrate substrates, bacteria and protozoa, methanogens, and gaseous and dissolved fermentation end products. The model was extended with static equations to model the hindgut metabolism. Feed composition and twice daily feeding were used as model inputs. Model parameters were estimated to experimental data using a Bayesian calibration procedure, after which the uncertainty of the parameter distribution on the model output was assessed. The model predicted a marked peak in pH2 after feeding that rapidly declined in time. This peak in pH2 caused a decrease in NAD+ to NADH ratio followed by an increased propionate molar proportion at the expense of acetate molar proportion, and an increase in CH4 production that steadily decreased in time, although the magnitude of increase for CH4 emission was less than for pH2 . A global sensitivity analysis indicated that parameters that determine the fractional passage rate and NADH oxidation rate altogether explained 86% of the variation in predicted daily CH4 emission. Model evaluation indicated over-prediction of in vivo CH4 emissions shortly after feeding, whereas under-prediction was indicated at later times. The present rumen fermentation modeling effort uniquely provides the integration of the pH2 controlled NAD+ to NADH ratio for dynamically predicting metabolic pathways that yield VFA, H2 and CH4.

AB - Dynamic modeling of mechanisms driving volatile fatty acid and hydrogen production in the rumen microbial ecosystem contributes to the heuristic prediction of CH4 emissions from dairy cattle into the environment. Existing mathematical rumen models, however, lack the representation of these mechanisms. A dynamic mechanistic model was developed that simulates the thermodynamic control of hydrogen partial pressure (pH2 ) on volatile fatty acid (VFA) fermentation pathways via the NAD+ to NADH ratio in fermentative microbes, and methanogenesis in the bovine rumen. This model is unique and closely aligns with principles of reaction kinetics and thermodynamics. Model state variables represent ruminal carbohydrate substrates, bacteria and protozoa, methanogens, and gaseous and dissolved fermentation end products. The model was extended with static equations to model the hindgut metabolism. Feed composition and twice daily feeding were used as model inputs. Model parameters were estimated to experimental data using a Bayesian calibration procedure, after which the uncertainty of the parameter distribution on the model output was assessed. The model predicted a marked peak in pH2 after feeding that rapidly declined in time. This peak in pH2 caused a decrease in NAD+ to NADH ratio followed by an increased propionate molar proportion at the expense of acetate molar proportion, and an increase in CH4 production that steadily decreased in time, although the magnitude of increase for CH4 emission was less than for pH2 . A global sensitivity analysis indicated that parameters that determine the fractional passage rate and NADH oxidation rate altogether explained 86% of the variation in predicted daily CH4 emission. Model evaluation indicated over-prediction of in vivo CH4 emissions shortly after feeding, whereas under-prediction was indicated at later times. The present rumen fermentation modeling effort uniquely provides the integration of the pH2 controlled NAD+ to NADH ratio for dynamically predicting metabolic pathways that yield VFA, H2 and CH4.

KW - Cattle

KW - Dairy cow

KW - Diurnal dynamics

KW - Enteric fermentation

KW - Global sensitivity analysis

KW - Methanogenesis

U2 - 10.1016/j.jtbi.2019.08.008

DO - 10.1016/j.jtbi.2019.08.008

M3 - Article

VL - 480

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EP - 165

JO - Journal of Theoretical Biology

JF - Journal of Theoretical Biology

SN - 0022-5193

ER -