Examination of hydrogen cross-feeders using a colonic microbiota model

Abstract Background Hydrogen cross-feeding microbes form a functionally important subset of the human colonic microbiota. The three major hydrogenotrophic functional groups of the colon: sulphate-reducing bacteria (SRB), methanogens and reductive acetogens, have been linked to wide ranging impacts o...

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Main Authors: Nick W. Smith, Paul R. Shorten, Eric Altermann, Nicole C. Roy, Warren C. McNabb
Format: Article
Language:English
Published: BMC 2021-01-01
Series:BMC Bioinformatics
Subjects:
Online Access:https://doi.org/10.1186/s12859-020-03923-6
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spelling doaj-e57c28a0de484487b2417f2c3cc0cb852021-01-10T13:03:16ZengBMCBMC Bioinformatics1471-21052021-01-0122112910.1186/s12859-020-03923-6Examination of hydrogen cross-feeders using a colonic microbiota modelNick W. Smith0Paul R. Shorten1Eric Altermann2Nicole C. Roy3Warren C. McNabb4School of Food and Advanced Technology, Massey UniversityRiddet Institute, Massey UniversityRiddet Institute, Massey UniversityRiddet Institute, Massey UniversityRiddet Institute, Massey UniversityAbstract Background Hydrogen cross-feeding microbes form a functionally important subset of the human colonic microbiota. The three major hydrogenotrophic functional groups of the colon: sulphate-reducing bacteria (SRB), methanogens and reductive acetogens, have been linked to wide ranging impacts on host physiology, health and wellbeing. Results An existing mathematical model for microbial community growth and metabolism was combined with models for each of the three hydrogenotrophic functional groups. The model was further developed for application to the colonic environment via inclusion of responsive pH, host metabolite absorption and the inclusion of host mucins. Predictions of the model, using two existing metabolic parameter sets, were compared to experimental faecal culture datasets. Model accuracy varied between experiments and measured variables and was most successful in predicting the growth of high relative abundance functional groups, such as the Bacteroides, and short chain fatty acid (SCFA) production. Two versions of the colonic model were developed: one representing the colon with sequential compartments and one utilising a continuous spatial representation. When applied to the colonic environment, the model predicted pH dynamics within the ranges measured in vivo and SCFA ratios comparable to those in the literature. The continuous version of the model simulated relative abundances of microbial functional groups comparable to measured values, but predictions were sensitive to the metabolic parameter values used for each functional group. Sulphate availability was found to strongly influence hydrogenotroph activity in the continuous version of the model, correlating positively with SRB and sulphide concentration and negatively with methanogen concentration, but had no effect in the compartmentalised model version. Conclusions Although the model predictions compared well to only some experimental measurements, the important features of the colon environment included make it a novel and useful contribution to modelling the colonic microbiota.https://doi.org/10.1186/s12859-020-03923-6microPopCommunity modellingMethaneHydrogen sulphideMicrobiome
collection DOAJ
language English
format Article
sources DOAJ
author Nick W. Smith
Paul R. Shorten
Eric Altermann
Nicole C. Roy
Warren C. McNabb
spellingShingle Nick W. Smith
Paul R. Shorten
Eric Altermann
Nicole C. Roy
Warren C. McNabb
Examination of hydrogen cross-feeders using a colonic microbiota model
BMC Bioinformatics
microPop
Community modelling
Methane
Hydrogen sulphide
Microbiome
author_facet Nick W. Smith
Paul R. Shorten
Eric Altermann
Nicole C. Roy
Warren C. McNabb
author_sort Nick W. Smith
title Examination of hydrogen cross-feeders using a colonic microbiota model
title_short Examination of hydrogen cross-feeders using a colonic microbiota model
title_full Examination of hydrogen cross-feeders using a colonic microbiota model
title_fullStr Examination of hydrogen cross-feeders using a colonic microbiota model
title_full_unstemmed Examination of hydrogen cross-feeders using a colonic microbiota model
title_sort examination of hydrogen cross-feeders using a colonic microbiota model
publisher BMC
series BMC Bioinformatics
issn 1471-2105
publishDate 2021-01-01
description Abstract Background Hydrogen cross-feeding microbes form a functionally important subset of the human colonic microbiota. The three major hydrogenotrophic functional groups of the colon: sulphate-reducing bacteria (SRB), methanogens and reductive acetogens, have been linked to wide ranging impacts on host physiology, health and wellbeing. Results An existing mathematical model for microbial community growth and metabolism was combined with models for each of the three hydrogenotrophic functional groups. The model was further developed for application to the colonic environment via inclusion of responsive pH, host metabolite absorption and the inclusion of host mucins. Predictions of the model, using two existing metabolic parameter sets, were compared to experimental faecal culture datasets. Model accuracy varied between experiments and measured variables and was most successful in predicting the growth of high relative abundance functional groups, such as the Bacteroides, and short chain fatty acid (SCFA) production. Two versions of the colonic model were developed: one representing the colon with sequential compartments and one utilising a continuous spatial representation. When applied to the colonic environment, the model predicted pH dynamics within the ranges measured in vivo and SCFA ratios comparable to those in the literature. The continuous version of the model simulated relative abundances of microbial functional groups comparable to measured values, but predictions were sensitive to the metabolic parameter values used for each functional group. Sulphate availability was found to strongly influence hydrogenotroph activity in the continuous version of the model, correlating positively with SRB and sulphide concentration and negatively with methanogen concentration, but had no effect in the compartmentalised model version. Conclusions Although the model predictions compared well to only some experimental measurements, the important features of the colon environment included make it a novel and useful contribution to modelling the colonic microbiota.
topic microPop
Community modelling
Methane
Hydrogen sulphide
Microbiome
url https://doi.org/10.1186/s12859-020-03923-6
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