Biological funneling of phenolics from transgenic plants engineered to express the bacterial 3-dehydroshikimate dehydratase (qsuB) gene

The economic and environmental sustainability of lignocellulosic biomass biorefineries is predicated on generating biofuels and bioproducts from cell-wall polysaccharide and lignin polymers. Historical efforts in plant genetic engineering have focused on the development of strategies that facilitate...

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Main Authors: German E. Umana, Jose M. Perez, Faride Unda, Chien-Yuan Lin, Canan Sener, Steven D. Karlen, Shawn D. Mansfield, Aymerick Eudes, John Ralph, Timothy J. Donohue, Daniel R. Noguera
Format: Article
Language:English
Published: Frontiers Media S.A. 2022-10-01
Series:Frontiers in Chemical Engineering
Subjects:
Online Access:https://www.frontiersin.org/articles/10.3389/fceng.2022.1036084/full
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author German E. Umana
German E. Umana
German E. Umana
Jose M. Perez
Jose M. Perez
Jose M. Perez
Faride Unda
Faride Unda
Chien-Yuan Lin
Chien-Yuan Lin
Canan Sener
Canan Sener
Steven D. Karlen
Steven D. Karlen
Shawn D. Mansfield
Shawn D. Mansfield
Aymerick Eudes
Aymerick Eudes
John Ralph
John Ralph
John Ralph
Timothy J. Donohue
Timothy J. Donohue
Timothy J. Donohue
Daniel R. Noguera
Daniel R. Noguera
Daniel R. Noguera
author_facet German E. Umana
German E. Umana
German E. Umana
Jose M. Perez
Jose M. Perez
Jose M. Perez
Faride Unda
Faride Unda
Chien-Yuan Lin
Chien-Yuan Lin
Canan Sener
Canan Sener
Steven D. Karlen
Steven D. Karlen
Shawn D. Mansfield
Shawn D. Mansfield
Aymerick Eudes
Aymerick Eudes
John Ralph
John Ralph
John Ralph
Timothy J. Donohue
Timothy J. Donohue
Timothy J. Donohue
Daniel R. Noguera
Daniel R. Noguera
Daniel R. Noguera
author_sort German E. Umana
collection DOAJ
description The economic and environmental sustainability of lignocellulosic biomass biorefineries is predicated on generating biofuels and bioproducts from cell-wall polysaccharide and lignin polymers. Historical efforts in plant genetic engineering have focused on the development of strategies that facilitate biomass deconstruction, with more recently efforts including the synthesis of high-value chemicals in planta. One such genetic modification is the expression of the bacterial quinate and shikimate utilization B (qsuB) gene that increases the accumulation of protocatechuic acid in lignocellulosic biomass. Herein, we evaluated the effectiveness of an alkaline pretreatment process to extract phenolics directly from wild-type and QsuB-transgenic lines of Arabidopsis, poplar, and sorghum, and then upgrade them to the polyester precursor 2-pyrone-4,6-dicarboxylic acid (PDC) with an engineered strain of Novosphingobium aromaticivorans. Protocatechuic acid extracted from all QsuB transgenic lines was found to be mostly in the glycosylated form. Glycosylated protocatechuic acid and other plant-derived phenolics were effectively metabolized by N. aromaticivorans, and PDC production was greatest using extracts from an Arabidopsis QsuB transgenic line (∼5% w/w), followed by QsuB sorghum (∼1.1% w/w), and QsuB poplar (∼0.4% w/w) lines. The comparison of PDC production from wild-type and QsuB transgenic lines of Arabidopsis, poplar, and sorghum demonstrates the utility of a mild alkaline pretreatment to liberate phenolics from plant biomass that are either naturally present or that accumulate as a consequence of genetic engineering strategies. All QsuB transgenic lines outperformed their wild-type counterparts with respect to observed PDC yields. In addition, microbial funneling to PDC was effective even when most of the protocatechuic acid extracted was in glycosylated form, clearly demonstrating that this bacterium can metabolize these aromatic conjugates. These findings illustrate the benefits of combining plant and microbial engineering for bioproduct formation from phenolics in lignocellulosic biorefineries.
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spelling doaj.art-d433cd9b8ae748be94934d7c674a63732022-12-22T02:34:19ZengFrontiers Media S.A.Frontiers in Chemical Engineering2673-27182022-10-01410.3389/fceng.2022.10360841036084Biological funneling of phenolics from transgenic plants engineered to express the bacterial 3-dehydroshikimate dehydratase (qsuB) geneGerman E. Umana0German E. Umana1German E. Umana2Jose M. Perez3Jose M. Perez4Jose M. Perez5Faride Unda6Faride Unda7Chien-Yuan Lin8Chien-Yuan Lin9Canan Sener10Canan Sener11Steven D. Karlen12Steven D. Karlen13Shawn D. Mansfield14Shawn D. Mansfield15Aymerick Eudes16Aymerick Eudes17John Ralph18John Ralph19John Ralph20Timothy J. Donohue21Timothy J. Donohue22Timothy J. Donohue23Daniel R. Noguera24Daniel R. Noguera25Daniel R. Noguera26Department of Civil and Environmental Engineering, University of Wisconsin-Madison, Madison, WI, United StatesGreat Lakes Bioenergy Research Center, Madison, WI, United StatesWisconsin Energy Institute, University of Wisconsin-Madison, Madison, WI, United StatesDepartment of Civil and Environmental Engineering, University of Wisconsin-Madison, Madison, WI, United StatesGreat Lakes Bioenergy Research Center, Madison, WI, United StatesWisconsin Energy Institute, University of Wisconsin-Madison, Madison, WI, United StatesGreat Lakes Bioenergy Research Center, Madison, WI, United StatesDepartment of Wood Science, University of British Columbia, Vancouver, BC, CanadaJoint BioEnergy Institute, Emeryville, CA, United StatesEnvironmental Genomics and Systems Biology Division, Lawrence Berkeley National Laboratory, Berkeley, CA, United StatesGreat Lakes Bioenergy Research Center, Madison, WI, United StatesWisconsin Energy Institute, University of Wisconsin-Madison, Madison, WI, United StatesGreat Lakes Bioenergy Research Center, Madison, WI, United StatesWisconsin Energy Institute, University of Wisconsin-Madison, Madison, WI, United StatesGreat Lakes Bioenergy Research Center, Madison, WI, United StatesDepartment of Wood Science, University of British Columbia, Vancouver, BC, CanadaJoint BioEnergy Institute, Emeryville, CA, United StatesEnvironmental Genomics and Systems Biology Division, Lawrence Berkeley National Laboratory, Berkeley, CA, United StatesGreat Lakes Bioenergy Research Center, Madison, WI, United StatesWisconsin Energy Institute, University of Wisconsin-Madison, Madison, WI, United StatesDepartment of Biochemistry, University of Wisconsin-Madison, Madison, WI, United StatesGreat Lakes Bioenergy Research Center, Madison, WI, United StatesWisconsin Energy Institute, University of Wisconsin-Madison, Madison, WI, United StatesDepartment of Bacteriology, University of Wisconsin-Madison, Madison, WI, United StatesDepartment of Civil and Environmental Engineering, University of Wisconsin-Madison, Madison, WI, United StatesGreat Lakes Bioenergy Research Center, Madison, WI, United StatesWisconsin Energy Institute, University of Wisconsin-Madison, Madison, WI, United StatesThe economic and environmental sustainability of lignocellulosic biomass biorefineries is predicated on generating biofuels and bioproducts from cell-wall polysaccharide and lignin polymers. Historical efforts in plant genetic engineering have focused on the development of strategies that facilitate biomass deconstruction, with more recently efforts including the synthesis of high-value chemicals in planta. One such genetic modification is the expression of the bacterial quinate and shikimate utilization B (qsuB) gene that increases the accumulation of protocatechuic acid in lignocellulosic biomass. Herein, we evaluated the effectiveness of an alkaline pretreatment process to extract phenolics directly from wild-type and QsuB-transgenic lines of Arabidopsis, poplar, and sorghum, and then upgrade them to the polyester precursor 2-pyrone-4,6-dicarboxylic acid (PDC) with an engineered strain of Novosphingobium aromaticivorans. Protocatechuic acid extracted from all QsuB transgenic lines was found to be mostly in the glycosylated form. Glycosylated protocatechuic acid and other plant-derived phenolics were effectively metabolized by N. aromaticivorans, and PDC production was greatest using extracts from an Arabidopsis QsuB transgenic line (∼5% w/w), followed by QsuB sorghum (∼1.1% w/w), and QsuB poplar (∼0.4% w/w) lines. The comparison of PDC production from wild-type and QsuB transgenic lines of Arabidopsis, poplar, and sorghum demonstrates the utility of a mild alkaline pretreatment to liberate phenolics from plant biomass that are either naturally present or that accumulate as a consequence of genetic engineering strategies. All QsuB transgenic lines outperformed their wild-type counterparts with respect to observed PDC yields. In addition, microbial funneling to PDC was effective even when most of the protocatechuic acid extracted was in glycosylated form, clearly demonstrating that this bacterium can metabolize these aromatic conjugates. These findings illustrate the benefits of combining plant and microbial engineering for bioproduct formation from phenolics in lignocellulosic biorefineries.https://www.frontiersin.org/articles/10.3389/fceng.2022.1036084/fullQsuBligninlignin valorizationvalue-added products2-pyrone-4,6-dicarboxylic acid (PDC)QsuB transgenics
spellingShingle German E. Umana
German E. Umana
German E. Umana
Jose M. Perez
Jose M. Perez
Jose M. Perez
Faride Unda
Faride Unda
Chien-Yuan Lin
Chien-Yuan Lin
Canan Sener
Canan Sener
Steven D. Karlen
Steven D. Karlen
Shawn D. Mansfield
Shawn D. Mansfield
Aymerick Eudes
Aymerick Eudes
John Ralph
John Ralph
John Ralph
Timothy J. Donohue
Timothy J. Donohue
Timothy J. Donohue
Daniel R. Noguera
Daniel R. Noguera
Daniel R. Noguera
Biological funneling of phenolics from transgenic plants engineered to express the bacterial 3-dehydroshikimate dehydratase (qsuB) gene
Frontiers in Chemical Engineering
QsuB
lignin
lignin valorization
value-added products
2-pyrone-4,6-dicarboxylic acid (PDC)
QsuB transgenics
title Biological funneling of phenolics from transgenic plants engineered to express the bacterial 3-dehydroshikimate dehydratase (qsuB) gene
title_full Biological funneling of phenolics from transgenic plants engineered to express the bacterial 3-dehydroshikimate dehydratase (qsuB) gene
title_fullStr Biological funneling of phenolics from transgenic plants engineered to express the bacterial 3-dehydroshikimate dehydratase (qsuB) gene
title_full_unstemmed Biological funneling of phenolics from transgenic plants engineered to express the bacterial 3-dehydroshikimate dehydratase (qsuB) gene
title_short Biological funneling of phenolics from transgenic plants engineered to express the bacterial 3-dehydroshikimate dehydratase (qsuB) gene
title_sort biological funneling of phenolics from transgenic plants engineered to express the bacterial 3 dehydroshikimate dehydratase qsub gene
topic QsuB
lignin
lignin valorization
value-added products
2-pyrone-4,6-dicarboxylic acid (PDC)
QsuB transgenics
url https://www.frontiersin.org/articles/10.3389/fceng.2022.1036084/full
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