Engineering isoprenoids production in metabolically versatile microbial host Pseudomonas putida

Wang, Xi; Baidoo, Edward E. K.; Kakumanu, Ramu; Xie, Silvia; Mukhopadhyay, Aindrila; Lee, Taek Soon

doi:10.1186/s13068-022-02235-6

Title: Engineering isoprenoids production in metabolically versatile microbial host Pseudomonas putida

Abstract

Abstract With the increasing need for microbial bioproduction to replace petrochemicals, it is critical to develop a new industrial microbial workhorse that improves the conversion of lignocellulosic carbon to biofuels and bioproducts in an economically feasible manner. Pseudomonas putida KT2440 is a promising microbial host due to its capability to grow on a broad range of carbon sources and its high tolerance to xenobiotics. In this study, we engineered P. putida KT2440 to produce isoprenoids, a vast category of compounds that provide routes to many petrochemical replacements. A heterologous mevalonate (MVA) pathway was engineered to produce potential biofuels isoprenol (C ₅ ) and epi-isozizaene (C ₁₅ ) for the first time in P. putida . We compared the difference between three different isoprenoid pathways in P. putida on isoprenol production and achieved 104 mg/L of isoprenol production in a batch flask experiment through optimization of the strain. As P. putida can natively consume isoprenol, we investigated how to prevent this self-consumption. We discovered that supplementing l -glutamate in the medium can effectively prevent isoprenol consumption in P. putida and metabolomics analysis showed an insufficient energy availability and an imbalanced redox status during isoprenol degradation. We also showed that the engineered P.more »« less

Authors:: Wang, Xi; Baidoo, Edward E. K.; Kakumanu, Ramu; Xie, Silvia; Mukhopadhyay, Aindrila; Lee, Taek Soon

Publication Date:: Mon Dec 12 00:00:00 EST 2022

Research Org.:: Lawrence Berkeley National Laboratory (LBNL), Berkeley, CA (United States)

Sponsoring Org.:: USDOE Office of Science (SC), Biological and Environmental Research (BER)

OSTI Identifier:: 1903079

Alternate Identifier(s):: OSTI ID: 1985248

Grant/Contract Number:: AC0205CH11231; AC02-05CH11231

Resource Type:: Published Article

Journal Name:: Biotechnology for Biofuels and Bioproducts

Additional Journal Information:: Journal Name: Biotechnology for Biofuels and Bioproducts Journal Volume: 15 Journal Issue: 1; Journal ID: ISSN 2731-3654

Publisher:: Springer Science + Business Media

Country of Publication:: United Kingdom

Language:: English

Subject:: 09 BIOMASS FUELS; P. putida KT2440; isoprenol; mevalonate; IPP-bypass pathway; L-glutamate; p-Coumarate; isoprenoid

Citation Formats


                    Wang, Xi, Baidoo, Edward E. K., Kakumanu, Ramu, Xie, Silvia, Mukhopadhyay, Aindrila, and Lee, Taek Soon. Engineering isoprenoids production in metabolically versatile microbial host Pseudomonas putida.  United Kingdom: N. p., 2022. 
Web.  doi:10.1186/s13068-022-02235-6.

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                    Wang, Xi, Baidoo, Edward E. K., Kakumanu, Ramu, Xie, Silvia, Mukhopadhyay, Aindrila, & Lee, Taek Soon. Engineering isoprenoids production in metabolically versatile microbial host Pseudomonas putida.  United Kingdom.  https://doi.org/10.1186/s13068-022-02235-6

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                    Wang, Xi, Baidoo, Edward E. K., Kakumanu, Ramu, Xie, Silvia, Mukhopadhyay, Aindrila, and Lee, Taek Soon. Mon .  
"Engineering isoprenoids production in metabolically versatile microbial host Pseudomonas putida".  United Kingdom.  https://doi.org/10.1186/s13068-022-02235-6.

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@article{osti_1903079,

  title        = {Engineering isoprenoids production in metabolically versatile microbial host Pseudomonas putida},

  author       = {Wang, Xi and Baidoo, Edward E. K. and Kakumanu, Ramu and Xie, Silvia and Mukhopadhyay, Aindrila and Lee, Taek Soon},

  abstractNote = {Abstract With the increasing need for microbial bioproduction to replace petrochemicals, it is critical to develop a new industrial microbial workhorse that improves the conversion of lignocellulosic carbon to biofuels and bioproducts in an economically feasible manner. Pseudomonas putida KT2440 is a promising microbial host due to its capability to grow on a broad range of carbon sources and its high tolerance to xenobiotics. In this study, we engineered P. putida KT2440 to produce isoprenoids, a vast category of compounds that provide routes to many petrochemical replacements. A heterologous mevalonate (MVA) pathway was engineered to produce potential biofuels isoprenol (C 5 ) and epi-isozizaene (C 15 ) for the first time in P. putida . We compared the difference between three different isoprenoid pathways in P. putida on isoprenol production and achieved 104 mg/L of isoprenol production in a batch flask experiment through optimization of the strain. As P. putida can natively consume isoprenol, we investigated how to prevent this self-consumption. We discovered that supplementing l -glutamate in the medium can effectively prevent isoprenol consumption in P. putida and metabolomics analysis showed an insufficient energy availability and an imbalanced redox status during isoprenol degradation. We also showed that the engineered P. putida strain can produce isoprenol using aromatic substrates such as p -coumarate as the sole carbon source, and this result demonstrates that P. putida is a valuable microbial chassis for isoprenoids to achieve sustainable biofuel production from lignocellulosic biomass. Graphical Abstract},

  doi          = {10.1186/s13068-022-02235-6},

  journal      = {Biotechnology for Biofuels and Bioproducts},

  number       = 1,

  volume       = 15,

  place        = {United Kingdom},

  year         = {Mon Dec 12 00:00:00 EST 2022},

  month        = {Mon Dec 12 00:00:00 EST 2022}

}

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Title: Engineering isoprenoids production in metabolically versatile microbial host Pseudomonas putida

Abstract

Citation Formats

Engineering E. coli for simultaneous glucose–xylose utilization during methyl ketone production journal, January 2018

De novo production of the monoterpenoid geranic acid by metabolically engineered Pseudomonas putida journal, December 2014

Metabolic engineering for isoprenoid-based biofuel production journal, July 2015

Engineering Pseudomonas putida for isoprenoid production by manipulating endogenous and shunt pathways supplying precursors journal, September 2019

Efficient production of oxidized terpenoids via engineering fusion proteins of terpene synthase and cytochrome P450 journal, March 2021

The pyrroloquinoline quinone biosynthesis pathway revisited: A structural approach journal, January 2008

Pseudomonas putida KT2440 Strain Metabolizes Glucose through a Cycle Formed by Enzymes of the Entner-Doudoroff, Embden-Meyerhof-Parnas, and Pentose Phosphate Pathways journal, September 2015

Monitoring differences in gene expression levels and polyhydroxyalkanoate (PHA) production in Pseudomonas putida KT2440 grown on different carbon sources journal, December 2010

Principal component analysis of proteomics (PCAP) as a tool to direct metabolic engineering journal, March 2015

Carbon catabolite repression in Pseudomonas : optimizing metabolic versatility and interactions with the environment journal, September 2010

Metabolic engineering for the high-yield production of isoprenoid-based C5 alcohols in E. coli journal, June 2015

Overexpression of the rice BAHD acyltransferase AT10 increases xylan-bound p-coumarate and reduces lignin in Sorghum bicolor journal, November 2021

Genomics of cellulosic biofuels journal, August 2008

Recent advances in lignin valorization with bacterial cultures: microorganisms, metabolic pathways, and bio-products journal, February 2019

Identification and microbial production of a terpene-based advanced biofuel journal, September 2011

Renewable production of high density jet fuel precursor sesquiterpenes from Escherichia coli journal, October 2018

Optimization of the IPP-bypass mevalonate pathway and fed-batch fermentation for the production of isoprenol in Escherichia coli journal, December 2019

Industrial biotechnology of Pseudomonas putida: advances and prospects journal, August 2020

High-throughput enzyme screening platform for the IPP-bypass mevalonate pathway for isopentenol production journal, May 2017

Metabolic engineering of Escherichia coli for limonene and perillyl alcohol production journal, September 2013

Microbial production of advanced biofuels journal, June 2021

BglBrick vectors and datasheets: A synthetic biology platform for gene expression journal, January 2011

Identification of glyA (Encoding Serine Hydroxymethyltransferase) and Its Use Together with the Exporter ThrE To Increase l -Threonine Accumulation by Corynebacterium glutamicum journal, July 2002

Comprehensive analysis of glucose and xylose metabolism in Escherichia coli under aerobic and anaerobic conditions by 13C metabolic flux analysis journal, January 2017

Production of jet fuel precursor monoterpenoids from engineered Escherichia coli : Production of Jet Fuel Precursor Monoterpenoids journal, May 2017

Mevalonate production from ethanol by direct conversion through acetyl-CoA using recombinant Pseudomonas putida, a novel biocatalyst for terpenoid production journal, October 2019

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From dirt to industrial applications: Pseudomonas putida as a Synthetic Biology chassis for hosting harsh biochemical reactions journal, October 2016

Microbial engineering for the production of advanced biofuels journal, August 2012

Genome-scale metabolic rewiring improves titers rates and yields of the non-native product indigoidine at scale journal, October 2020

Two-step pathway for isoprenoid synthesis journal, December 2018

The isoprenoid alcohol pathway, a synthetic route for isoprenoid biosynthesis journal, June 2019

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Biofuels for a sustainable future journal, March 2021

Bacterial catabolism of lignin-derived aromatics: New findings in a recent decade: Update on bacterial lignin catabolism: Bacterial catabolism of lignin-derived aromatics journal, November 2017

Relative potential of biosynthetic pathways for biofuels and bio-based products journal, December 2011

A field of dreams: Lignin valorization into chemicals, materials, fuels, and health-care products journal, November 2019

Engineering Saccharomyces cerevisiae for isoprenol production journal, March 2021

[4 + 4]-cycloaddition of isoprene for the production of high-performance bio-based jet fuel journal, January 2019

Generation of Pseudomonas putida KT2440 Strains with Efficient Utilization of Xylose and Galactose via Adaptive Laboratory Evolution journal, August 2021

Isopentenyl diphosphate (IPP)-bypass mevalonate pathways for isopentenol production journal, March 2016

Pseudomonas putida KT2440 metabolism undergoes sequential modifications during exponential growth in a complete medium as compounds are gradually consumed journal, April 2019

Global features of the Pseudomonas putida KT2440 genome sequence journal, December 2002

Integrated analysis of isopentenyl pyrophosphate (IPP) toxicity in isoprenoid-producing Escherichia coli journal, May 2018

The PedS2/PedR2 Two-Component System Is Crucial for the Rare Earth Element Switch in Pseudomonas putida KT2440 journal, August 2018

Engineering E. coli for simultaneous glucose–xylose utilization during methyl ketone production
journal, January 2018

De novo production of the monoterpenoid geranic acid by metabolically engineered Pseudomonas putida
journal, December 2014

Metabolic engineering for isoprenoid-based biofuel production
journal, July 2015

Engineering Pseudomonas putida for isoprenoid production by manipulating endogenous and shunt pathways supplying precursors
journal, September 2019

Efficient production of oxidized terpenoids via engineering fusion proteins of terpene synthase and cytochrome P450
journal, March 2021

The pyrroloquinoline quinone biosynthesis pathway revisited: A structural approach
journal, January 2008

Pseudomonas putida KT2440 Strain Metabolizes Glucose through a Cycle Formed by Enzymes of the Entner-Doudoroff, Embden-Meyerhof-Parnas, and Pentose Phosphate Pathways
journal, September 2015

Monitoring differences in gene expression levels and polyhydroxyalkanoate (PHA) production in Pseudomonas putida KT2440 grown on different carbon sources
journal, December 2010

Principal component analysis of proteomics (PCAP) as a tool to direct metabolic engineering
journal, March 2015

Carbon catabolite repression in Pseudomonas : optimizing metabolic versatility and interactions with the environment
journal, September 2010

Metabolic engineering for the high-yield production of isoprenoid-based C5 alcohols in E. coli
journal, June 2015

Overexpression of the rice BAHD acyltransferase AT10 increases xylan-bound p-coumarate and reduces lignin in Sorghum bicolor
journal, November 2021

Genomics of cellulosic biofuels
journal, August 2008

Recent advances in lignin valorization with bacterial cultures: microorganisms, metabolic pathways, and bio-products
journal, February 2019

Identification and microbial production of a terpene-based advanced biofuel
journal, September 2011

Renewable production of high density jet fuel precursor sesquiterpenes from Escherichia coli
journal, October 2018

Optimization of the IPP-bypass mevalonate pathway and fed-batch fermentation for the production of isoprenol in Escherichia coli
journal, December 2019

Industrial biotechnology of Pseudomonas putida: advances and prospects
journal, August 2020

High-throughput enzyme screening platform for the IPP-bypass mevalonate pathway for isopentenol production
journal, May 2017

Metabolic engineering of Escherichia coli for limonene and perillyl alcohol production
journal, September 2013

Microbial production of advanced biofuels
journal, June 2021

BglBrick vectors and datasheets: A synthetic biology platform for gene expression
journal, January 2011

Identification of glyA (Encoding Serine Hydroxymethyltransferase) and Its Use Together with the Exporter ThrE To Increase l -Threonine Accumulation by Corynebacterium glutamicum
journal, July 2002

Comprehensive analysis of glucose and xylose metabolism in Escherichia coli under aerobic and anaerobic conditions by 13C metabolic flux analysis
journal, January 2017

Production of jet fuel precursor monoterpenoids from engineered Escherichia coli : Production of Jet Fuel Precursor Monoterpenoids
journal, May 2017

Mevalonate production from ethanol by direct conversion through acetyl-CoA using recombinant Pseudomonas putida, a novel biocatalyst for terpenoid production
journal, October 2019

Genetic tools for reliable gene expression and recombineering in Pseudomonas putida
journal, January 2018

From dirt to industrial applications: Pseudomonas putida as a Synthetic Biology chassis for hosting harsh biochemical reactions
journal, October 2016

Microbial engineering for the production of advanced biofuels
journal, August 2012

Genome-scale metabolic rewiring improves titers rates and yields of the non-native product indigoidine at scale
journal, October 2020

Two-step pathway for isoprenoid synthesis
journal, December 2018

The isoprenoid alcohol pathway, a synthetic route for isoprenoid biosynthesis
journal, June 2019

An automated Design-Build-Test-Learn pipeline for enhanced microbial production of fine chemicals
journal, June 2018

Biofuels for a sustainable future
journal, March 2021

Bacterial catabolism of lignin-derived aromatics: New findings in a recent decade: Update on bacterial lignin catabolism: Bacterial catabolism of lignin-derived aromatics
journal, November 2017

Relative potential of biosynthetic pathways for biofuels and bio-based products
journal, December 2011

A field of dreams: Lignin valorization into chemicals, materials, fuels, and health-care products
journal, November 2019

Engineering Saccharomyces cerevisiae for isoprenol production
journal, March 2021

[4 + 4]-cycloaddition of isoprene for the production of high-performance bio-based jet fuel
journal, January 2019

Generation of Pseudomonas putida KT2440 Strains with Efficient Utilization of Xylose and Galactose via Adaptive Laboratory Evolution
journal, August 2021

Isopentenyl diphosphate (IPP)-bypass mevalonate pathways for isopentenol production
journal, March 2016

Pseudomonas putida KT2440 metabolism undergoes sequential modifications during exponential growth in a complete medium as compounds are gradually consumed
journal, April 2019

Global features of the Pseudomonas putida KT2440 genome sequence
journal, December 2002

Integrated analysis of isopentenyl pyrophosphate (IPP) toxicity in isoprenoid-producing Escherichia coli
journal, May 2018

The PedS2/PedR2 Two-Component System Is Crucial for the Rare Earth Element Switch in Pseudomonas putida KT2440
journal, August 2018