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Article

Cross-Feeding of a Toxic Metabolite in a Synthetic Lignocellulose-Degrading Microbial Community

1
NASA Ames Research Center, Moffett Field, CA 94035, USA
2
Department of Biological Sciences, University of Idaho, Moscow, ID 83844, USA
3
Institute for Bioinformatics and Evolutionary Studies, University of Idaho, Moscow, ID 83844, USA
4
Institute for Modeling Collaboration and Innovation, University of Idaho, Moscow, ID 83844, USA
5
Department of Microbiology, University of Georgia, Athens, GA 30602, USA
*
Authors to whom correspondence should be addressed.
Present address: Incyte Diagnostics, Spokane, WA 99216, USA.
Present address: M Health Fairview Masonic Children’s Hospital, University of Minnesota, Minneapolis, MN 55454, USA.
Academic Editor: Christopher B. Blackwood
Microorganisms 2021, 9(2), 321; https://doi.org/10.3390/microorganisms9020321
Received: 31 December 2020 / Revised: 27 January 2021 / Accepted: 1 February 2021 / Published: 4 February 2021
(This article belongs to the Special Issue Microbial One-Carbon Metabolism of Natural and Engineered Systems)
The recalcitrance of complex organic polymers such as lignocellulose is one of the major obstacles to sustainable energy production from plant biomass, and the generation of toxic intermediates can negatively impact the efficiency of microbial lignocellulose degradation. Here, we describe the development of a model microbial consortium for studying lignocellulose degradation, with the specific goal of mitigating the production of the toxin formaldehyde during the breakdown of methoxylated aromatic compounds. Included are Pseudomonas putida, a lignin degrader; Cellulomonas fimi, a cellulose degrader; and sometimes Yarrowia lipolytica, an oleaginous yeast. Unique to our system is the inclusion of Methylorubrum extorquens, a methylotroph capable of using formaldehyde for growth. We developed a defined minimal “Model Lignocellulose” growth medium for reproducible coculture experiments. We demonstrated that the formaldehyde produced by P. putida growing on vanillic acid can exceed the minimum inhibitory concentration for C. fimi, and, furthermore, that the presence of M. extorquens lowers those concentrations. We also uncovered unexpected ecological dynamics, including resource competition, and interspecies differences in growth requirements and toxin sensitivities. Finally, we introduced the possibility for a mutualistic interaction between C. fimi and M. extorquens through metabolite exchange. This study lays the foundation to enable future work incorporating metabolomic analysis and modeling, genetic engineering, and laboratory evolution, on a model system that is appropriate both for fundamental eco-evolutionary studies and for the optimization of efficiency and yield in microbially-mediated biomass transformation. View Full-Text
Keywords: synthetic ecology; lignocellulose; formaldehyde; microbial communities; methylotrophy; Methylorubrum extorquens; Pseudomonas putida; Cellulomonas fimi; Yarrowia lipolytica synthetic ecology; lignocellulose; formaldehyde; microbial communities; methylotrophy; Methylorubrum extorquens; Pseudomonas putida; Cellulomonas fimi; Yarrowia lipolytica
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MDPI and ACS Style

Lee, J.A.; Baugh, A.C.; Shevalier, N.J.; Strand, B.; Stolyar, S.; Marx, C.J. Cross-Feeding of a Toxic Metabolite in a Synthetic Lignocellulose-Degrading Microbial Community. Microorganisms 2021, 9, 321. https://doi.org/10.3390/microorganisms9020321

AMA Style

Lee JA, Baugh AC, Shevalier NJ, Strand B, Stolyar S, Marx CJ. Cross-Feeding of a Toxic Metabolite in a Synthetic Lignocellulose-Degrading Microbial Community. Microorganisms. 2021; 9(2):321. https://doi.org/10.3390/microorganisms9020321

Chicago/Turabian Style

Lee, Jessica A.; Baugh, Alyssa C.; Shevalier, Nicholas J.; Strand, Brandi; Stolyar, Sergey; Marx, Christopher J. 2021. "Cross-Feeding of a Toxic Metabolite in a Synthetic Lignocellulose-Degrading Microbial Community" Microorganisms 9, no. 2: 321. https://doi.org/10.3390/microorganisms9020321

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