Metabolic Synergy between Human Symbionts Bacteroides and Methanobrevibacter
Abstract
Trophic interactions between microbes are postulated to determine whether a host microbiome is healthy or causes predisposition to disease. Two abundant taxa, the Gram-negative heterotrophic bacterium Bacteroides thetaiotaomicron and the methanogenic archaeon Methanobrevibacter smithii, are proposed to have a synergistic metabolic relationship. Both organisms play vital roles in human gut health; B. thetaiotaomicron assists the host by fermenting dietary polysaccharides, whereas M. smithii consumes end-stage fermentation products and is hypothesized to relieve feedback inhibition of upstream microbes such as B. thetaiotaomicron. To study their metabolic interactions, we defined and optimized a coculture system and used software testing techniques to analyze growth under a range of conditions representing the nutrient environment of the host. Here we verify that B. thetaiotaomicron fermentation products are sufficient for M. smithii growth and that accumulation of fermentation products alters secretion of metabolites by B. thetaiotaomicron to benefit M. smithii. Studies suggest that B. thetaiotaomicron metabolic efficiency is greater in the absence of fermentation products or in the presence of M. smithii. Under certain conditions, B. thetaiotaomicron and M. smithii form interspecies granules consistent with behavior observed for syntrophic partnerships between microbes in soil or sediment enrichments and anaerobic digesters. Furthermore, when vitamin B12, hematin, andmore »
- Authors:
-
[1]
- Univ. of Nebraska, Lincoln, NE (United States)
- Oak Ridge National Lab. (ORNL), Oak Ridge, TN (United States)
- Univ. of Nebraska, Lincoln, NE (United States); Iowa State Univ., Ames, IA (United States)
- Publication Date:
- Research Org.:
- Oak Ridge National Lab. (ORNL), Oak Ridge, TN (United States)
- Sponsoring Org.:
- USDOE; National Science Foundation (NSF); National Institutes of Heath (NIH)
- OSTI Identifier:
- 1872867
- Grant/Contract Number:
- AC05-00OR22725; 1901543; IOS-1938948; CCF-1816969; MCB-1449014; P20-GM113126
- Resource Type:
- Accepted Manuscript
- Journal Name:
- Microbiology Spectrum
- Additional Journal Information:
- Journal Volume: 10; Journal Issue: 3; Journal ID: ISSN 2165-0497
- Publisher:
- American Society for Microbiology
- Country of Publication:
- United States
- Language:
- English
- Subject:
- 59 BASIC BIOLOGICAL SCIENCES; microbiome; bacteroides; methanobrevibacter; cross-feeding; synergy; metabolism; syntrophy
Citation Formats
Catlett, Jennie L., Carr, Sean, Cashman McDevitt, Mikaela, Smith, Megan D., Walter, Mary, Sakkaff, Zahmeeth, Kelley, Christine, Pierobon, Massimiliano, Cohen, Myra B., and Buan, Nicole R. Metabolic Synergy between Human Symbionts Bacteroides and Methanobrevibacter. United States: N. p., 2022.
Web. doi:10.1128/spectrum.01067-22.
Catlett, Jennie L., Carr, Sean, Cashman McDevitt, Mikaela, Smith, Megan D., Walter, Mary, Sakkaff, Zahmeeth, Kelley, Christine, Pierobon, Massimiliano, Cohen, Myra B., & Buan, Nicole R. Metabolic Synergy between Human Symbionts Bacteroides and Methanobrevibacter. United States. https://doi.org/10.1128/spectrum.01067-22
Catlett, Jennie L., Carr, Sean, Cashman McDevitt, Mikaela, Smith, Megan D., Walter, Mary, Sakkaff, Zahmeeth, Kelley, Christine, Pierobon, Massimiliano, Cohen, Myra B., and Buan, Nicole R. Tue .
"Metabolic Synergy between Human Symbionts Bacteroides and Methanobrevibacter". United States. https://doi.org/10.1128/spectrum.01067-22. https://www.osti.gov/servlets/purl/1872867.
@article{osti_1872867,
title = {Metabolic Synergy between Human Symbionts Bacteroides and Methanobrevibacter},
author = {Catlett, Jennie L. and Carr, Sean and Cashman McDevitt, Mikaela and Smith, Megan D. and Walter, Mary and Sakkaff, Zahmeeth and Kelley, Christine and Pierobon, Massimiliano and Cohen, Myra B. and Buan, Nicole R.},
abstractNote = {Trophic interactions between microbes are postulated to determine whether a host microbiome is healthy or causes predisposition to disease. Two abundant taxa, the Gram-negative heterotrophic bacterium Bacteroides thetaiotaomicron and the methanogenic archaeon Methanobrevibacter smithii, are proposed to have a synergistic metabolic relationship. Both organisms play vital roles in human gut health; B. thetaiotaomicron assists the host by fermenting dietary polysaccharides, whereas M. smithii consumes end-stage fermentation products and is hypothesized to relieve feedback inhibition of upstream microbes such as B. thetaiotaomicron. To study their metabolic interactions, we defined and optimized a coculture system and used software testing techniques to analyze growth under a range of conditions representing the nutrient environment of the host. Here we verify that B. thetaiotaomicron fermentation products are sufficient for M. smithii growth and that accumulation of fermentation products alters secretion of metabolites by B. thetaiotaomicron to benefit M. smithii. Studies suggest that B. thetaiotaomicron metabolic efficiency is greater in the absence of fermentation products or in the presence of M. smithii. Under certain conditions, B. thetaiotaomicron and M. smithii form interspecies granules consistent with behavior observed for syntrophic partnerships between microbes in soil or sediment enrichments and anaerobic digesters. Furthermore, when vitamin B12, hematin, and hydrogen gas are abundant, coculture growth is greater than the sum of growth observed for monocultures, suggesting that both organisms benefit from a synergistic mutual metabolic relationship.},
doi = {10.1128/spectrum.01067-22},
journal = {Microbiology Spectrum},
number = 3,
volume = 10,
place = {United States},
year = {Tue May 10 00:00:00 EDT 2022},
month = {Tue May 10 00:00:00 EDT 2022}
}
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