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Title: Metatranscriptomic and Thermodynamic Insights into Medium-Chain Fatty Acid Production Using an Anaerobic Microbiome

Abstract

Biomanufacturing from renewable feedstocks can offset fossil fuel-based chemical production. One potential biomanufacturing strategy is production of medium-chain fatty acids (MCFA) from organic feedstocks using either pure cultures or microbiomes. While the set of microbes in a microbiome can often metabolize organic materials of greater diversity than a single species can and while the role of specific species may be known, knowledge of the carbon and energy flow within and between organisms in MCFA-producing microbiomes is only now starting to emerge. Here, we integrated metagenomic, metatranscriptomic, and thermodynamic analyses to predict and characterize the metabolic network of an anaerobic microbiome producing MCFA from organic matter derived from lignocellulosic ethanol fermentation conversion residue. A total of 37 high-quality (>80% complete, <10% contamination) metagenome-assembled genomes (MAGs) were recovered from the microbiome, and metabolic reconstruction of the 10 most abundant MAGs was performed. Metabolic reconstruction combined with metatranscriptomic analysis predicted that organisms affiliated with Lactobacillus and Coriobacteriaceae would degrade carbohydrates and ferment sugars to lactate and acetate. Lachnospiraceae- and Eubacteriaceae-affiliated organisms were predicted to transform these fermentation products to MCFA. Thermodynamic analyses identified conditions under which H 2is expected to be either produced or consumed, suggesting a potential role of H 2partial pressuremore » in MCFA production. From an integrated systems analysis perspective, we propose that MCFA production could be improved if microbiomes were engineered to use homofermentative instead of heterofermentative Lactobacillus and if MCFA-producing organisms were engineered to preferentially use a thioesterase instead of a coenzyme A (CoA) transferase as the terminal enzyme in reverse β-oxidation. IMPORTANCE: Mixed communities of microbes play important roles in health, the environment, agriculture, and biotechnology. While tapping the combined activities of organisms within microbiomes may allow the utilization of a wider range of substrates in preference to the use of pure cultures for biomanufacturing, harnessing the metabolism of these mixed cultures remains a major challenge. Here, we predicted metabolic functions of bacteria in a microbiome that produces medium-chain fatty acids from a renewable feedstock. Our findings lay the foundation for efforts to begin addressing how to engineer and control microbiomes for improved biomanufacturing, how to build synthetic mixtures of microbes that produce valuable chemicals from renewable resources, and how to better understand the microbial communities that contribute to health, agriculture, and the environment.« less

Authors:
 [1];  [1];  [1]; ORCiD logo [1]; ORCiD logo [1];  [2]
  1. Univ. of Wisconsin, Madison, WI (United States)
  2. Ghent Univ., Ghent (Belgium)
Publication Date:
Research Org.:
Univ. of Wisconsin, Madison, WI (United States)
Sponsoring Org.:
USDOE Office of Science (SC), Biological and Environmental Research (BER) (SC-23)
OSTI Identifier:
1506659
Grant/Contract Number:  
SC0018409
Resource Type:
Journal Article: Accepted Manuscript
Journal Name:
mSystems
Additional Journal Information:
Journal Volume: 3; Journal Issue: 6; Journal ID: ISSN 2379-5077
Publisher:
American Society for Microbiology
Country of Publication:
United States
Language:
English
Subject:
59 BASIC BIOLOGICAL SCIENCES; medium-chain fatty acids; hexanoic acid; octanoic acid; carboxylate platform; anaerobic digestion; biorefining; metagenomics; metatranscriptomics

Citation Formats

Scarborough, Matthew J., Lawson, Christopher E., Hamilton, Joshua J., Donohue, Timothy J., Noguera, Daniel R., and Rabaey, Korneel. Metatranscriptomic and Thermodynamic Insights into Medium-Chain Fatty Acid Production Using an Anaerobic Microbiome. United States: N. p., 2018. Web. doi:10.1128/mSystems.00221-18.
Scarborough, Matthew J., Lawson, Christopher E., Hamilton, Joshua J., Donohue, Timothy J., Noguera, Daniel R., & Rabaey, Korneel. Metatranscriptomic and Thermodynamic Insights into Medium-Chain Fatty Acid Production Using an Anaerobic Microbiome. United States. doi:10.1128/mSystems.00221-18.
Scarborough, Matthew J., Lawson, Christopher E., Hamilton, Joshua J., Donohue, Timothy J., Noguera, Daniel R., and Rabaey, Korneel. Tue . "Metatranscriptomic and Thermodynamic Insights into Medium-Chain Fatty Acid Production Using an Anaerobic Microbiome". United States. doi:10.1128/mSystems.00221-18. https://www.osti.gov/servlets/purl/1506659.
@article{osti_1506659,
title = {Metatranscriptomic and Thermodynamic Insights into Medium-Chain Fatty Acid Production Using an Anaerobic Microbiome},
author = {Scarborough, Matthew J. and Lawson, Christopher E. and Hamilton, Joshua J. and Donohue, Timothy J. and Noguera, Daniel R. and Rabaey, Korneel},
abstractNote = {Biomanufacturing from renewable feedstocks can offset fossil fuel-based chemical production. One potential biomanufacturing strategy is production of medium-chain fatty acids (MCFA) from organic feedstocks using either pure cultures or microbiomes. While the set of microbes in a microbiome can often metabolize organic materials of greater diversity than a single species can and while the role of specific species may be known, knowledge of the carbon and energy flow within and between organisms in MCFA-producing microbiomes is only now starting to emerge. Here, we integrated metagenomic, metatranscriptomic, and thermodynamic analyses to predict and characterize the metabolic network of an anaerobic microbiome producing MCFA from organic matter derived from lignocellulosic ethanol fermentation conversion residue. A total of 37 high-quality (>80% complete, <10% contamination) metagenome-assembled genomes (MAGs) were recovered from the microbiome, and metabolic reconstruction of the 10 most abundant MAGs was performed. Metabolic reconstruction combined with metatranscriptomic analysis predicted that organisms affiliated with Lactobacillus and Coriobacteriaceae would degrade carbohydrates and ferment sugars to lactate and acetate.Lachnospiraceae- and Eubacteriaceae-affiliated organisms were predicted to transform these fermentation products to MCFA. Thermodynamic analyses identified conditions under which H2is expected to be either produced or consumed, suggesting a potential role of H2partial pressure in MCFA production. From an integrated systems analysis perspective, we propose that MCFA production could be improved if microbiomes were engineered to use homofermentative instead of heterofermentative Lactobacillus and if MCFA-producing organisms were engineered to preferentially use a thioesterase instead of a coenzyme A (CoA) transferase as the terminal enzyme in reverse β-oxidation. IMPORTANCE: Mixed communities of microbes play important roles in health, the environment, agriculture, and biotechnology. While tapping the combined activities of organisms within microbiomes may allow the utilization of a wider range of substrates in preference to the use of pure cultures for biomanufacturing, harnessing the metabolism of these mixed cultures remains a major challenge. Here, we predicted metabolic functions of bacteria in a microbiome that produces medium-chain fatty acids from a renewable feedstock. Our findings lay the foundation for efforts to begin addressing how to engineer and control microbiomes for improved biomanufacturing, how to build synthetic mixtures of microbes that produce valuable chemicals from renewable resources, and how to better understand the microbial communities that contribute to health, agriculture, and the environment.},
doi = {10.1128/mSystems.00221-18},
journal = {mSystems},
issn = {2379-5077},
number = 6,
volume = 3,
place = {United States},
year = {2018},
month = {11}
}

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Works referenced in this record:

Lignocellulosic Biomass Pretreatment Using AFEX
book, January 2009