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Examination of hydrogen cross-feeders using a colonic microbiota model

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 p...

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Autores principales: Smith, Nick W., Shorten, Paul R., Altermann, Eric, Roy, Nicole C., McNabb, Warren C.
Formato: Online Artículo Texto
Lenguaje:English
Publicado: BioMed Central 2021
Materias:
Acceso en línea:https://www.ncbi.nlm.nih.gov/pmc/articles/PMC7789523/
https://www.ncbi.nlm.nih.gov/pubmed/33407079
http://dx.doi.org/10.1186/s12859-020-03923-6
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author Smith, Nick W.
Shorten, Paul R.
Altermann, Eric
Roy, Nicole C.
McNabb, Warren C.
author_facet Smith, Nick W.
Shorten, Paul R.
Altermann, Eric
Roy, Nicole C.
McNabb, Warren C.
author_sort Smith, Nick W.
collection PubMed
description 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.
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spelling pubmed-77895232021-01-07 Examination of hydrogen cross-feeders using a colonic microbiota model Smith, Nick W. Shorten, Paul R. Altermann, Eric Roy, Nicole C. McNabb, Warren C. BMC Bioinformatics Research Article 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. BioMed Central 2021-01-06 /pmc/articles/PMC7789523/ /pubmed/33407079 http://dx.doi.org/10.1186/s12859-020-03923-6 Text en © The Author(s) 2021 Open AccessThis article is licensed under a Creative Commons Attribution 4.0 International License, which permits use, sharing, adaptation, distribution and reproduction in any medium or format, as long as you give appropriate credit to the original author(s) and the source, provide a link to the Creative Commons licence, and indicate if changes were made. The images or other third party material in this article are included in the article's Creative Commons licence, unless indicated otherwise in a credit line to the material. If material is not included in the article's Creative Commons licence and your intended use is not permitted by statutory regulation or exceeds the permitted use, you will need to obtain permission directly from the copyright holder. To view a copy of this licence, visit http://creativecommons.org/licenses/by/4.0/. The Creative Commons Public Domain Dedication waiver (http://creativecommons.org/publicdomain/zero/1.0/) applies to the data made available in this article, unless otherwise stated in a credit line to the data.
spellingShingle Research Article
Smith, Nick W.
Shorten, Paul R.
Altermann, Eric
Roy, Nicole C.
McNabb, Warren C.
Examination of hydrogen cross-feeders using a colonic microbiota model
title 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_short Examination of hydrogen cross-feeders using a colonic microbiota model
title_sort examination of hydrogen cross-feeders using a colonic microbiota model
topic Research Article
url https://www.ncbi.nlm.nih.gov/pmc/articles/PMC7789523/
https://www.ncbi.nlm.nih.gov/pubmed/33407079
http://dx.doi.org/10.1186/s12859-020-03923-6
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