Comprehensive molecular characterization of Methylobacterium extorquens AM1 adapted for 1-butanol tolerance

Hu, Bo; Yang, Yi -Ming; Beck, David A. C.; Wang, Qian -Wen; Chen, Wen -Jing; Yang, Jing; Lidstrom, Mary E.; Yang, Song

doi:10.1186/s13068-016-0497-y

Title: Comprehensive molecular characterization of Methylobacterium extorquens AM1 adapted for 1-butanol tolerance

Abstract

In this study, the toxicity of alcohols is one of the major roadblocks of biological fermentation for biofuels production. Methylobacterium extorquens AM1, a facultative methylotrophic α-proteobacterium, has been engineered to generate 1-butanol from cheap carbon feedstocks through a synthetic metabolic pathway. However, M. extorquens AM1 is vulnerable to solvent stress, which impedes further development for 1-butanol production. Only a few studies have reported the general stress response of M. extorquens AM1 to solvent stress. Therefore, it is highly desirable to obtain a strain with ameliorated 1-butanol tolerance and elucidate the molecular mechanism of 1-butnaol tolerance in M. extorquens AM1 for future strain improvement. In this work, adaptive laboratory evolution was used as a tool to isolate mutants with 1-butanol tolerance up to 0.5 %. The evolved strains, BHBT3 and BHBT5, demonstrated increased growth rates and higher survival rates with the existence of 1-butanol. Whole genome sequencing revealed a SNP mutation at kefB in BHBT5, which was confirmed to be responsible for increasing 1-butanol tolerance through an allelic exchange experiment. Global metabolomic analysis further discovered that the pools of multiple key metabolites, including fatty acids, amino acids, and disaccharides, were increased in BHBT5 in response to 1-butanol stress. Additionally, the carotenoidmore »« less

Authors:

Hu, Bo ^[1]; Yang, Yi -Ming ^[2]; Beck, David A. C. ^[3]; Wang, Qian -Wen ^[2]; Chen, Wen -Jing ^[2]; Yang, Jing ^[2]; Lidstrom, Mary E. ^[3]; Yang, Song ^[4]

Univ. of Washington, Seattle, WA (United States); Intrexon Corp., South San Francisco, CA (United States)
Qingdao Agricultural Univ., Qingdao (China)
Univ. of Washington, Seattle, WA (United States)
Qingdao Agricultural Univ., Qingdao (China); Tianjin Univ., Tianjin (China)

Publication Date:: Mon Apr 11 00:00:00 EDT 2016

Research Org.:: Univ. of Washington, Seattle, WA (United States)

Sponsoring Org.:: USDOE

OSTI Identifier:: 1253902

Grant/Contract Number:: SC0006871

Resource Type:: Accepted Manuscript

Journal Name:: Biotechnology for Biofuels

Additional Journal Information:: Journal Volume: 9; Journal Issue: 1; Journal ID: ISSN 1754-6834

Publisher:: BioMed Central

Country of Publication:: United States

Language:: English

Subject:: 59 BASIC BIOLOGICAL SCIENCES; 09 BIOMASS FUELS; Methylobacterium extorquens AM1; 1-butanol tolerance; adaptive evolution; whole genome sequencing; global metabolome analysis; carotenoid

Citation Formats


                    Hu, Bo, Yang, Yi -Ming, Beck, David A. C., Wang, Qian -Wen, Chen, Wen -Jing, Yang, Jing, Lidstrom, Mary E., and Yang, Song. Comprehensive molecular characterization of Methylobacterium extorquens AM1 adapted for 1-butanol tolerance.  United States: N. p., 2016. 
Web.  doi:10.1186/s13068-016-0497-y.

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                    Hu, Bo, Yang, Yi -Ming, Beck, David A. C., Wang, Qian -Wen, Chen, Wen -Jing, Yang, Jing, Lidstrom, Mary E., & Yang, Song. Comprehensive molecular characterization of Methylobacterium extorquens AM1 adapted for 1-butanol tolerance.  United States.  https://doi.org/10.1186/s13068-016-0497-y

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                    Hu, Bo, Yang, Yi -Ming, Beck, David A. C., Wang, Qian -Wen, Chen, Wen -Jing, Yang, Jing, Lidstrom, Mary E., and Yang, Song. Mon .  
"Comprehensive molecular characterization of Methylobacterium extorquens AM1 adapted for 1-butanol tolerance".  United States.  https://doi.org/10.1186/s13068-016-0497-y.  https://www.osti.gov/servlets/purl/1253902.

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@article{osti_1253902,

  title        = {Comprehensive molecular characterization of Methylobacterium extorquens AM1 adapted for 1-butanol tolerance},

  author       = {Hu, Bo and Yang, Yi -Ming and Beck, David A. C. and Wang, Qian -Wen and Chen, Wen -Jing and Yang, Jing and Lidstrom, Mary E. and Yang, Song},

  abstractNote = {In this study, the toxicity of alcohols is one of the major roadblocks of biological fermentation for biofuels production. Methylobacterium extorquens AM1, a facultative methylotrophic α-proteobacterium, has been engineered to generate 1-butanol from cheap carbon feedstocks through a synthetic metabolic pathway. However, M. extorquens AM1 is vulnerable to solvent stress, which impedes further development for 1-butanol production. Only a few studies have reported the general stress response of M. extorquens AM1 to solvent stress. Therefore, it is highly desirable to obtain a strain with ameliorated 1-butanol tolerance and elucidate the molecular mechanism of 1-butnaol tolerance in M. extorquens AM1 for future strain improvement. In this work, adaptive laboratory evolution was used as a tool to isolate mutants with 1-butanol tolerance up to 0.5 %. The evolved strains, BHBT3 and BHBT5, demonstrated increased growth rates and higher survival rates with the existence of 1-butanol. Whole genome sequencing revealed a SNP mutation at kefB in BHBT5, which was confirmed to be responsible for increasing 1-butanol tolerance through an allelic exchange experiment. Global metabolomic analysis further discovered that the pools of multiple key metabolites, including fatty acids, amino acids, and disaccharides, were increased in BHBT5 in response to 1-butanol stress. Additionally, the carotenoid synthesis pathway was significantly down-regulated in BHBT5. In conclusion, we successfully screened mutants resistant to 1-butanol and provided insights into the molecular mechanism of 1-butanol tolerance in M. extorquens AM1. This research will be useful for uncovering the mechanism of cellular response of M. extorquens AM1 to solvent stress, and will provide the genetic blueprint for the rational design of a strain of M. extorquens AM1 with increased 1-butanol tolerance in the future.},

  doi          = {10.1186/s13068-016-0497-y},

  journal      = {Biotechnology for Biofuels},

  number       = 1,

  volume       = 9,

  place        = {United States},

  year         = {Mon Apr 11 00:00:00 EDT 2016},

  month        = {Mon Apr 11 00:00:00 EDT 2016}

}

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https://doi.org/10.1186/s13068-016-0497-y

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Cited by: 29 works

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Figures / Tables:

Fig. 1: Experimental evolution of 1‑butanol tolerance in M. extorquens AM1

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Metabolic engineering of Methylobacterium extorquens AM1 for 1-butanol production
journal, October 2014

Hu, Bo; Lidstrom, Mary E.
Biotechnology for Biofuels, Vol. 7, Issue 1
DOI: 10.1186/s13068-014-0156-0

MS/MS networking guided analysis of molecule and gene cluster families
text, January 2013

M., Gutierrez,; S., Moore, B.; C., Dorrestein, P.
The University of North Carolina at Chapel Hill University Libraries
DOI: 10.17615/bd99-qk88

Global Molecular Analyses of Methane Metabolism in Methanotrophic Alphaproteobacterium, Methylosinus trichosporium OB3b. Part II. Metabolomics and 13C-Labeling Study
journal, January 2013

Yang, Song; Matsen, Janet B.; Konopka, Michael
Frontiers in Microbiology, Vol. 4
DOI: 10.3389/fmicb.2013.00070

Parallel and Divergent Evolutionary Solutions for the Optimization of an Engineered Central Metabolism in Methylobacterium extorquens AM1
journal, April 2015

Carroll, Sean; Chubiz, Lon; Agashe, Deepa
Microorganisms, Vol. 3, Issue 2
DOI: 10.3390/microorganisms3020152

Works referencing / citing this record:

Breeding of Methanol-Tolerant Methylobacterium extorquens AM1 by Atmospheric and Room Temperature Plasma Mutagenesis Combined With Adaptive Laboratory Evolution
journal, May 2018

Cui, Lan-Yu; Wang, Shan-Shan; Guan, Chang-Ge
Biotechnology Journal
DOI: 10.1002/biot.201700679

Guidance for engineering of synthetic methylotrophy based on methanol metabolism in methylotrophy
journal, January 2017

Zhang, Wenming; Zhang, Ting; Wu, Sihua
RSC Advances, Vol. 7, Issue 7
DOI: 10.1039/c6ra27038g

Production of 3-hydroxypropionic acid in engineered Methylobacterium extorquens AM1 and its reassimilation through a reductive route
journal, October 2017

Yang, Yi-Ming; Chen, Wen-Jing; Yang, Jing
Microbial Cell Factories, Vol. 16, Issue 1
DOI: 10.1186/s12934-017-0798-2

Metabolic engineering of Methylobacterium extorquens AM1 for the production of butadiene precursor
journal, December 2018

Yang, Jing; Zhang, Chang-Tai; Yuan, Xiao-Jie
Microbial Cell Factories, Vol. 17, Issue 1
DOI: 10.1186/s12934-018-1042-4

Adaptive Laboratory Evolution of Antibiotic Resistance Using Different Selection Regimes Lead to Similar Phenotypes and Genotypes
journal, May 2017

Jahn, Leonie J.; Munck, Christian; Ellabaan, Mostafa M. H.
Frontiers in Microbiology, Vol. 8
DOI: 10.3389/fmicb.2017.00816

Production of 3-hydroxypropionic acid in engineered Methylobacterium extorquens AM1 and its reassimilation through a reductive route
journal, October 2017

Yang, Yi-Ming; Chen, Wen-Jing; Yang, Jing
Microbial Cell Factories, Vol. 16, Issue 1
DOI: 10.1186/s12934-017-0798-2

Metabolic engineering of Methylobacterium extorquens AM1 for the production of butadiene precursor
journal, December 2018

Yang, Jing; Zhang, Chang-Tai; Yuan, Xiao-Jie
Microbial Cell Factories, Vol. 17, Issue 1
DOI: 10.1186/s12934-018-1042-4

Adaptive Laboratory Evolution of Antibiotic Resistance Using Different Selection Regimes Lead to Similar Phenotypes and Genotypes
journal, May 2017

Jahn, Leonie J.; Munck, Christian; Ellabaan, Mostafa M. H.
Frontiers in Microbiology, Vol. 8
DOI: 10.3389/fmicb.2017.00816

Metabolomics Investigation of an Association of Induced Features and Corresponding Fungus during the Co-culture of Trametes versicolor and Ganoderma applanatum
journal, January 2018

Xu, Xiao-Yan; Shen, Xiao-Ting; Yuan, Xiao-Jie
Frontiers in Microbiology, Vol. 8
DOI: 10.3389/fmicb.2017.02647

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Metabolomics Revealed an Association of Metabolite Changes and Defective Growth in Methylobacterium extorquens AM1 Overexpressing ecm during Growth on Methanol

Journal Article Cui, Jinyu ; Good, Nathan M. ; Hu, Bo ; ... - PLoS ONE

Methylobacterium extorquens AM1 is a facultative methylotroph capable of growth on both single-carbon and multi-carbon compounds. The ethylmalonyl-CoA (EMC) pathway is one of the central assimilatory pathways in M. extorquens during growth on C1 and C2 substrates. Previous studies had shown that ethylmalonyl-CoA mutase functioned as a control point during the transition from growth on succinate to growth on ethylamine. In this study we overexpressed ecm, phaA, mcmAB and found that upregulating ecm by expressing it from the strong constitutive mxaF promoter caused a 27% decrease in growth rate on methanol compared to the strain with an empty vector. Targetedmore »« less
Cited by 14
https://doi.org/10.1371/journal.pone.0154043
Difference in C3–C4 metabolism underlies tradeoff between growth rate and biomass yield in Methylobacterium extorquens AM1

Journal Article Fu, Yanfen ; Beck, David A. C. ; Lidstrom, Mary E. - BMC Microbiology

In this study, two variants of Methylobacterium extorquens AM1 demonstrated a trade-off between growth rate and biomass yield. In addition, growth rate and biomass yield were also affected by supplementation of growth medium with different amounts of cobalt. The metabolism changes relating to these growth phenomena as well as the trade-off were investigated in this study. ¹³C metabolic flux analysis was used to generate a detailed central carbon metabolic flux map with both absolute and normalized flux values. As a result, the major differences between the two variants occurred at the formate node as well as within C3-C4 inter-conversion pathways.more »« less
Cited by 10
https://doi.org/10.1186/s12866-016-0778-4
Engineering Terpene Production Pathways in Methylobacterium extorquens AM1

Journal Article Hurt, Allison ; Bibik, Jacob D. ; Martinez-Gomez, Norma Cecilia ; ... - Microorganisms

Terpenes are diverse specialized metabolites naturally found within plants and have important roles in inter-species communication, adaptation and interaction with the environment. Their industrial applications span a broad range, including fragrances, flavors, cosmetics, natural colorants to agrochemicals and therapeutics, yet formal chemical synthesis is economically challenging due to structural complexities. Engineering terpene biosynthesis could represent an alternative in microbial biotechnological workhorses, such as Saccharomyces cerevisiae or Escherichi coli, utilizing sugars or complex media as feedstocks. Host species that metabolize renewable and affordable carbon sources may offer unique sustainable biotechnological alternatives. Methylotrophs are bacteria with the capacity to utilize one-carbon feedstocks,more »« less
https://doi.org/10.3390/microorganisms12030500
Phenotypic characterization of 10 methanol oxidation mutant classes in Methylobacterium sp. strain AM1

Journal Article Nunn, D N ; Lidstrom, M E - J. Bacteriol.; (United States)

Twenty-five methanol oxidation mutants of the facultative methylotroph Methylobacterium sp. strain AM1 have been characterized by complementation analysis and assigned to 10 complementation groups, Mox A1, A2, A3, and B through H. In this study we have characterized each of the mutants belonging to the 10 Mox complementation groups for the following criteria: (i) phenazine methosulfate-dichlorophenolindophenol dye-linked methanol dehydrogenase activity; (ii) methanol-dependent whole-cell oxygen consumption; (iii) the presence or absence of methanol dehydrogenase protein by sodium dodecyl sulfate-polyacrylamide gel electrophoresis and Western blotting; (iv) the absorption spectra of purified mutant methanol dehydrogenase proteins; and (v) the presence or absence ofmore »« less
Phenotypic characterization of ten methanol oxidation (Mox) mutant classes in methylobacterium AM1

Technical Report Nunn, D N ; Lidstrom, M E

Twenty-five methanol oxidation mutants of the facultative methylotroph Methylobacterium strain AM1 have been characterized by complementation analysis and assigned to ten complementation groups, Mox A1,A2,A3 and B-H. We have characterized each of the mutants belonging to the ten Mox complementation groups by PMS-DCPIP dye linked methanol dehydrogenase activity, by methanol-dependent whole cell oxygen consumption, by the presence or absence of methanol dehydrogenase protein by SDS-polyacrylamide gels and Western blotting, by the absorption spectra of purified mutant methanol dehydrogenase proteins and by the presence or absence of the soluble cytochrome c proteins of Methylobacterium AM1. We propose functions for each ofmore »« less

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