Phenolic amides are potent inhibitors of De Novo nucleotide biosynthesis
Abstract
An outstanding challenge toward efficient production of biofuels and value-added chemicals from plant biomass is the impact that lignocellulose-derived inhibitors have on microbial fermentations. Elucidating the mechanisms that underlie their toxicity is critical for developing strategies to overcome them. Here, using Escherichia coli as a model system, we investigated the metabolic effects and toxicity mechanisms of feruloyl amide and coumaroyl amide, the predominant phenolic compounds in ammonia-pretreated biomass hydrolysates. Using metabolomics, isotope tracers, and biochemical assays, we showed that these two phenolic amides act as potent and fast-acting inhibitors of purine and pyrimidine biosynthetic pathways. Feruloyl or coumaroyl amide exposure leads to (i) a rapid buildup of 5-phosphoribosyl-1-pyrophosphate (PRPP), a key precursor in nucleotide biosynthesis, (ii) a rapid decrease in the levels of pyrimidine biosynthetic intermediates, and (iii) a long-term generalized decrease in nucleotide and deoxynucleotide levels. Tracer experiments using 13C-labeled sugars and [15N]ammonia demonstrated that carbon and nitrogen fluxes into nucleotides and deoxynucleotides are inhibited by these phenolic amides. We found that these effects are mediated via direct inhibition of glutamine amidotransferases that participate in nucleotide biosynthetic pathways. In particular, feruloyl amide is a competitive inhibitor of glutamine PRPP amidotransferase (PurF), which catalyzes the first committed step in demore » purine biosynthesis. Finally, external nucleoside supplementation prevents phenolic amide-mediated growth inhibition by allowing nucleotide biosynthesis via salvage pathways. Furthermore, the results presented here will help in the development of strategies to overcome toxicity of phenolic compounds and facilitate engineering of more efficient microbial producers of biofuels and chemicals.
- Authors:
-
- Univ. of Wisconsin, Madison, WI (United States)
- Publication Date:
- Research Org.:
- Great Lakes Bioenergy Research Center (GLBRC), Madison, WI (United States)
- Sponsoring Org.:
- USDOE Office of Science (SC), Biological and Environmental Research (BER)
- OSTI Identifier:
- 1345181
- Grant/Contract Number:
- FC02-07ER64494
- Resource Type:
- Accepted Manuscript
- Journal Name:
- Applied and Environmental Microbiology
- Additional Journal Information:
- Journal Volume: 81; Journal Issue: 17; Journal ID: ISSN 0099-2240
- Publisher:
- American Society for Microbiology
- Country of Publication:
- United States
- Language:
- English
- Subject:
- 59 BASIC BIOLOGICAL SCIENCES
Citation Formats
Pisithkul, Tippapha, Jacobson, Tyler B., O'Brien, Thomas J., Stevenson, David M., and Amador-Noguez, Daniel. Phenolic amides are potent inhibitors of De Novo nucleotide biosynthesis. United States: N. p., 2015.
Web. doi:10.1128/aem.01324-15.
Pisithkul, Tippapha, Jacobson, Tyler B., O'Brien, Thomas J., Stevenson, David M., & Amador-Noguez, Daniel. Phenolic amides are potent inhibitors of De Novo nucleotide biosynthesis. United States. https://doi.org/10.1128/aem.01324-15
Pisithkul, Tippapha, Jacobson, Tyler B., O'Brien, Thomas J., Stevenson, David M., and Amador-Noguez, Daniel. Fri .
"Phenolic amides are potent inhibitors of De Novo nucleotide biosynthesis". United States. https://doi.org/10.1128/aem.01324-15. https://www.osti.gov/servlets/purl/1345181.
@article{osti_1345181,
title = {Phenolic amides are potent inhibitors of De Novo nucleotide biosynthesis},
author = {Pisithkul, Tippapha and Jacobson, Tyler B. and O'Brien, Thomas J. and Stevenson, David M. and Amador-Noguez, Daniel},
abstractNote = {An outstanding challenge toward efficient production of biofuels and value-added chemicals from plant biomass is the impact that lignocellulose-derived inhibitors have on microbial fermentations. Elucidating the mechanisms that underlie their toxicity is critical for developing strategies to overcome them. Here, using Escherichia coli as a model system, we investigated the metabolic effects and toxicity mechanisms of feruloyl amide and coumaroyl amide, the predominant phenolic compounds in ammonia-pretreated biomass hydrolysates. Using metabolomics, isotope tracers, and biochemical assays, we showed that these two phenolic amides act as potent and fast-acting inhibitors of purine and pyrimidine biosynthetic pathways. Feruloyl or coumaroyl amide exposure leads to (i) a rapid buildup of 5-phosphoribosyl-1-pyrophosphate (PRPP), a key precursor in nucleotide biosynthesis, (ii) a rapid decrease in the levels of pyrimidine biosynthetic intermediates, and (iii) a long-term generalized decrease in nucleotide and deoxynucleotide levels. Tracer experiments using 13C-labeled sugars and [15N]ammonia demonstrated that carbon and nitrogen fluxes into nucleotides and deoxynucleotides are inhibited by these phenolic amides. We found that these effects are mediated via direct inhibition of glutamine amidotransferases that participate in nucleotide biosynthetic pathways. In particular, feruloyl amide is a competitive inhibitor of glutamine PRPP amidotransferase (PurF), which catalyzes the first committed step in de novo purine biosynthesis. Finally, external nucleoside supplementation prevents phenolic amide-mediated growth inhibition by allowing nucleotide biosynthesis via salvage pathways. Furthermore, the results presented here will help in the development of strategies to overcome toxicity of phenolic compounds and facilitate engineering of more efficient microbial producers of biofuels and chemicals.},
doi = {10.1128/aem.01324-15},
journal = {Applied and Environmental Microbiology},
number = 17,
volume = 81,
place = {United States},
year = {Fri Jun 12 00:00:00 EDT 2015},
month = {Fri Jun 12 00:00:00 EDT 2015}
}
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FIG 1: Phenolic amides hinder anaerobic growth and alter intracellular metabolite levels. (A) E. coli cultures were grown anaerobically in M9 minimal medium containing 1% (wt/vol) xylose as the single carbon source. At the time indicated by the arrows (early/mid-exponential phase), lignocellulose-derived phenolic inhibitors (LDPIs) were added at various concentrationsmore »
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