Advances and prospects in metabolic engineering of Zymomonas mobilis

Wang, Xia; He, Qiaoning; Yang, Yongfu; Wang, Jingwen; Haning, Katie; Hu, Yun; Wu, Bo; He, Mingxiong; Zhang, Yaoping; Bao, Jie; Contreras, Lydia M.; Yang, Shihui

doi:10.1016/j.ymben.2018.04.001

Advances and prospects in metabolic engineering of Zymomonas mobilis

Journal Article · Thu Apr 05 00:00:00 EDT 2018 · Metabolic Engineering

DOI:https://doi.org/10.1016/j.ymben.2018.04.001· OSTI ID:1459643

Wang, Xia ^[1]; He, Qiaoning ^[2]; Yang, Yongfu ^[2]; Wang, Jingwen ^[2]; Haning, Katie ^[3]; Hu, Yun ^[2]; Wu, Bo ^[4]; He, Mingxiong ^[4]; Zhang, Yaoping ^[5]; Bao, Jie ^[6]; Contreras, Lydia M. ^[3]; Yang, Shihui ^[2]

Hubei Univ., Wuhan (China). College of Life Sciences, Hubei Collaborative Innovation Center for Green Transformation of Bioresources, Environmental Microbial Technology Center and Hubei Key Lab. of Industrial Biotechnology; Hubei Key Laboratory of Industrial Biotechnology, College of Life Sciences, Hubei University
Hubei Univ., Wuhan (China). College of Life Sciences, Hubei Collaborative Innovation Center for Green Transformation of Bioresources, Environmental Microbial Technology Center and Hubei Key Lab. of Industrial Biotechnology
Univ. of Texas, Austin, TX (United States). Cockrell School of Engineering, Dept. of Chemical Engineering and Inst. for Cellular and Molecular Biology
Biogas Inst. of the Ministry of Agriculture (BIOMA), Chengdu (China). Biomass Energy Technology Research Centre and Key Lab. of Development and Application of Rural Renewable Energy
Univ. of Wisconsin, Madison, WI (United States). Great Lakes Bioenergy Research Center (GLBRC)
East China Univ. of Science and Technology, Shanghai (China). State Key Lab. of Bioreactor Engineering

Biorefinery of biomass-based biofuels and biochemicals by microorganisms is a competitive alternative of traditional petroleum refineries. Zymomonas mobilis is a natural ethanologen with many desirable characteristics, which makes it an ideal industrial microbial biocatalyst for commercial production of desirable bioproducts through metabolic engineering. In this paper, we summarize the metabolic engineering progress achieved in Z. mobilis to expand its substrate and product ranges as well as to enhance its robustness against stressful conditions such as inhibitory compounds within the lignocellulosic hydrolysates and slurries. We also discuss a few metabolic engineering strategies that can be applied in Z. mobilis to further develop it as a robust workhorse for economic lignocellulosic bioproducts. In addition, we briefly review the progress of metabolic engineering in Z. mobilis related to the classical synthetic biology cycle of “Design-Build-Test-Learn”, as well as the progress and potential to develop Z. mobilis as a model chassis for biorefinery practices in the synthetic biology era.

View Accepted Manuscript (DOE)

Research Organization:: Univ. of Wisconsin, Madison, WI (United States). Great Lakes Bioenergy Research Center (GLBRC)

Sponsoring Organization:: USDOE Office of Science (SC), Biological and Environmental Research (BER) (SC-23); National Science Foundation (NSF); Welch Foundation

Grant/Contract Number:: SC0018409; FC02-07ER64494

OSTI ID:: 1459643

Alternate ID(s):: OSTI ID: 1819008

Journal Information:: Metabolic Engineering, Journal Name: Metabolic Engineering Vol. 50; ISSN 1096-7176

Publisher:: ElsevierCopyright Statement

Country of Publication:: United States

Language:: English

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Genetic improvement of Escherichia coli for ethanol production: chromosomal integration of Zymomonas mobilis genes encoding pyruvate decarboxylase and alcohol dehydrogenase II. Ohta, K.; Beall, D. S.; Mejia, J. P. Applied and Environmental Microbiology, Vol. 57, Issue 4 https://doi.org/10.1128/AEM.57.4.893-900.1991	journal	January 1991
Expression of an L-alanine dehydrogenase gene in Zymomonas mobilis and excretion of L-alanine Uhlenbusch, I.; Sahm, H.; Sprenger, G. A. Applied and Environmental Microbiology, Vol. 57, Issue 5 https://doi.org/10.1128/AEM.57.5.1360-1366.1991	journal	May 1991
Production of beta-carotene in Zymomonas mobilis and Agrobacterium tumefaciens by introduction of the biosynthesis genes from Erwinia uredovora. Misawa, N.; Yamano, S.; Ikenaga, H. Applied and Environmental Microbiology, Vol. 57, Issue 6 https://doi.org/10.1128/AEM.57.6.1847-1849.1991	journal	January 1991
The Ice Nucleation Gene from Pseudomonas syringae as a Sensitive Gene Reporter for Promoter Analysis in Zymomonas mobilis. Drainas, C.; Vartholomatos, G.; Panopoulos, N. J. Applied and environmental microbiology, Vol. 61, Issue 1 https://doi.org/10.1128/AEM.61.1.273-277.1995	journal	January 1995
Expression of the Escherichia coli pmi gene, encoding phosphomannose-isomerase in Zymomonas mobilis, leads to utilization of mannose as a novel growth substrate, which can be used as a selective marker Weisser, P.; Krämer, R.; Sprenger, G. A. Applied and Environmental Microbiology, Vol. 62, Issue 11 https://doi.org/10.1128/AEM.62.11.4155-4161.1996	journal	November 1996
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Glyceraldehyde-3-phosphate dehydrogenase gene from Zymomonas mobilis: cloning, sequencing, and identification of promoter region. Conway, T.; Sewell, G. W.; Ingram, L. O. Journal of Bacteriology, Vol. 169, Issue 12 https://doi.org/10.1128/JB.169.12.5653-5662.1987	journal	December 1987
Promoter and nucleotide sequences of the Zymomonas mobilis pyruvate decarboxylase. Conway, T.; Osman, Y. A.; Konnan, J. I. Journal of Bacteriology, Vol. 169, Issue 3 https://doi.org/10.1128/JB.169.3.949-954.1987	journal	January 1987
Gene expression in Zymomonas mobilis: promoter structure and identification of membrane anchor sequences forming functional lacZ' fusion proteins. Conway, T.; Osman, Y. A.; Ingram, L. O. Journal of Bacteriology, Vol. 169, Issue 6 https://doi.org/10.1128/JB.169.6.2327-2335.1987	journal	June 1987
Phosphoglycerate kinase gene from Zymomonas mobilis: cloning, sequencing, and localization within the gap operon. Conway, T.; Ingram, L. O. Journal of Bacteriology, Vol. 170, Issue 4 https://doi.org/10.1128/JB.170.4.1926-1933.1988	journal	April 1988
Cloning, sequencing, and characterization of the principal acid phosphatase, the phoC+ product, from Zymomonas mobilis. Pond, J. L.; Eddy, C. K.; Mackenzie, K. F. Journal of Bacteriology, Vol. 171, Issue 2 https://doi.org/10.1128/JB.171.2.767-774.1989	journal	February 1989
Expression of Zymomonas mobilis adhB (encoding alcohol dehydrogenase II) and adhB-lacZ operon fusions in recombinant Z. mobilis. Mackenzie, K. F.; Conway, T.; Aldrich, H. C. Journal of Bacteriology, Vol. 171, Issue 9 https://doi.org/10.1128/JB.171.9.4577-4582.1989	journal	September 1989
Sequence and genetic organization of a Zymomonas mobilis gene cluster that encodes several enzymes of glucose metabolism Barnell, W. O.; Yi, K. C.; Conway, T. Journal of Bacteriology, Vol. 172, Issue 12 https://doi.org/10.1128/JB.172.12.7227-7240.1990	journal	December 1990
Use of the tac promoter and lacIq for the controlled expression of Zymomonas mobilis fermentative genes in Escherichia coli and Zymomonas mobilis. Arfman, N.; Worrell, V.; Ingram, L. O. Journal of Bacteriology, Vol. 174, Issue 22 https://doi.org/10.1128/JB.174.22.7370-7378.1992	journal	November 1992
Mutational analysis of segmental stabilization of transcripts from the Zymomonas mobilis gap-pgk operon Burchhardt, G.; Keshav, K. F.; Yomano, L. Journal of Bacteriology, Vol. 175, Issue 8 https://doi.org/10.1128/JB.175.8.2327-2333.1993	journal	April 1993
GLYCOLYTIC ENZYMES IN ZYMOMONAS MOBILIS Raps, Shirley; DeMoss, R. D. Journal of Bacteriology, Vol. 84, Issue 1 https://doi.org/10.1128/JB.84.1.115-118.1962	journal	July 1962
Influence of Aeration and of Pantothenate on Growth Yields of Zymomonas mobilis Belaïch, Jean-Pierre; Senez, Jacques C. Journal of Bacteriology, Vol. 89, Issue 5 https://doi.org/10.1128/JB.89.5.1195-1200.1965	journal	January 1965
Expression of a Lactose Transposon (Tn951) in Zymomonas mobilis† Carey, V. C.; Walia, S. K.; Ingram, L. O. Applied and Environmental Microbiology, Vol. 46, Issue 5 https://doi.org/10.1128/aem.46.5.1163-1168.1983	journal	January 1983
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Production of Acetaldehyde by Zymomonas mobilis Wecker, Matt S. A.; Zall, Robert R. Applied and Environmental Microbiology, Vol. 53, Issue 12 https://doi.org/10.1128/aem.53.12.2815-2820.1987	journal	January 1987
Genetic improvement of Escherichia coli for ethanol production: chromosomal integration of Zymomonas mobilis genes encoding pyruvate decarboxylase and alcohol dehydrogenase II. Ohta, K.; Beall, D. S.; Mejia, J. P. Applied and Environmental Microbiology, Vol. 57, Issue 4 https://doi.org/10.1128/aem.57.4.893-900.1991	journal	January 1991
Expression of an L-alanine dehydrogenase gene in Zymomonas mobilis and excretion of L-alanine Uhlenbusch, I.; Sahm, H.; Sprenger, G. A. Applied and Environmental Microbiology, Vol. 57, Issue 5 https://doi.org/10.1128/aem.57.5.1360-1366.1991	journal	May 1991
Production of beta-carotene in Zymomonas mobilis and Agrobacterium tumefaciens by introduction of the biosynthesis genes from Erwinia uredovora. Misawa, N.; Yamano, S.; Ikenaga, H. Applied and Environmental Microbiology, Vol. 57, Issue 6 https://doi.org/10.1128/aem.57.6.1847-1849.1991	journal	January 1991
The Ice Nucleation Gene from Pseudomonas syringae as a Sensitive Gene Reporter for Promoter Analysis in Zymomonas mobilis. Drainas, C.; Vartholomatos, G.; Panopoulos, N. J. Applied and environmental microbiology, Vol. 61, Issue 1 https://doi.org/10.1128/aem.61.1.273-277.1995	journal	January 1995
Expression of the Escherichia coli pmi gene, encoding phosphomannose-isomerase in Zymomonas mobilis, leads to utilization of mannose as a novel growth substrate, which can be used as a selective marker Weisser, P.; Krämer, R.; Sprenger, G. A. Applied and Environmental Microbiology, Vol. 62, Issue 11 https://doi.org/10.1128/aem.62.11.4155-4161.1996	journal	November 1996
Development of an arabinose-fermenting Zymomonas mobilis strain by metabolic pathway engineering. Deanda, K.; Zhang, M.; Eddy, C. Applied and environmental microbiology, Vol. 62, Issue 12 https://doi.org/10.1128/aem.62.12.4465-4470.1996	journal	January 1996
The biology of Zymomonas. Swings, J.; De Ley, J. Bacteriological Reviews, Vol. 41, Issue 1 https://doi.org/10.1128/br.41.1.1-46.1977	journal	January 1977
Draft Genome Sequence of Zymomonas mobilis ZM481 (ATCC 31823) Zhao, Ning; Pan, Yongxu; Liu, Hongguang Genome Announcements, Vol. 4, Issue 2 https://doi.org/10.1128/genomeA.00193-16	journal	April 2016
Genome Sequence of Zymomonas mobilis subsp. mobilis NRRL B-1960 Chacon-Vargas, Katherine; Chirino, Alexandra A.; Davis, Meghan M. Genome Announcements, Vol. 5, Issue 30 https://doi.org/10.1128/genomeA.00562-17	journal	July 2017
Glyceraldehyde-3-phosphate dehydrogenase gene from Zymomonas mobilis: cloning, sequencing, and identification of promoter region. Conway, T.; Sewell, G. W.; Ingram, L. O. Journal of Bacteriology, Vol. 169, Issue 12 https://doi.org/10.1128/jb.169.12.5653-5662.1987	journal	December 1987
Promoter and nucleotide sequences of the Zymomonas mobilis pyruvate decarboxylase. Conway, T.; Osman, Y. A.; Konnan, J. I. Journal of Bacteriology, Vol. 169, Issue 3 https://doi.org/10.1128/jb.169.3.949-954.1987	journal	January 1987
Gene expression in Zymomonas mobilis: promoter structure and identification of membrane anchor sequences forming functional lacZ' fusion proteins. Conway, T.; Osman, Y. A.; Ingram, L. O. Journal of Bacteriology, Vol. 169, Issue 6 https://doi.org/10.1128/jb.169.6.2327-2335.1987	journal	June 1987
Phosphoglycerate kinase gene from Zymomonas mobilis: cloning, sequencing, and localization within the gap operon. Conway, T.; Ingram, L. O. Journal of Bacteriology, Vol. 170, Issue 4 https://doi.org/10.1128/jb.170.4.1926-1933.1988	journal	April 1988
Cloning, sequencing, and characterization of the principal acid phosphatase, the phoC+ product, from Zymomonas mobilis. Pond, J. L.; Eddy, C. K.; Mackenzie, K. F. Journal of Bacteriology, Vol. 171, Issue 2 https://doi.org/10.1128/jb.171.2.767-774.1989	journal	February 1989
Expression of Zymomonas mobilis adhB (encoding alcohol dehydrogenase II) and adhB-lacZ operon fusions in recombinant Z. mobilis. Mackenzie, K. F.; Conway, T.; Aldrich, H. C. Journal of Bacteriology, Vol. 171, Issue 9 https://doi.org/10.1128/jb.171.9.4577-4582.1989	journal	September 1989
Sequence and genetic organization of a Zymomonas mobilis gene cluster that encodes several enzymes of glucose metabolism Barnell, W. O.; Yi, K. C.; Conway, T. Journal of Bacteriology, Vol. 172, Issue 12 https://doi.org/10.1128/jb.172.12.7227-7240.1990	journal	December 1990
Use of the tac promoter and lacIq for the controlled expression of Zymomonas mobilis fermentative genes in Escherichia coli and Zymomonas mobilis. Arfman, N.; Worrell, V.; Ingram, L. O. Journal of Bacteriology, Vol. 174, Issue 22 https://doi.org/10.1128/jb.174.22.7370-7378.1992	journal	November 1992
Mutational analysis of segmental stabilization of transcripts from the Zymomonas mobilis gap-pgk operon Burchhardt, G.; Keshav, K. F.; Yomano, L. Journal of Bacteriology, Vol. 175, Issue 8 https://doi.org/10.1128/jb.175.8.2327-2333.1993	journal	April 1993
GLYCOLYTIC ENZYMES IN ZYMOMONAS MOBILIS Raps, Shirley; DeMoss, R. D. Journal of Bacteriology, Vol. 84, Issue 1 https://doi.org/10.1128/jb.84.1.115-118.1962	journal	July 1962
Influence of Aeration and of Pantothenate on Growth Yields of Zymomonas mobilis Belaïch, Jean-Pierre; Senez, Jacques C. Journal of Bacteriology, Vol. 89, Issue 5 https://doi.org/10.1128/jb.89.5.1195-1200.1965	journal	January 1965
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Cellulosic Ethanol Production by Recombinant Cellulolytic Bacteria Harbouring pdc and adh II Genes of Zymomonas mobilis Piriya, P. Sobana; Vasan, P. Thirumalai; Padma, V. S. Biotechnology Research International, Vol. 2012 https://doi.org/10.1155/2012/817549	journal	January 2012
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Effect of acetic acid on ethanol production by Zymomonas mobilis mutant strains through continuous adaptation Liu, Yu-Fan; Hsieh, Chia-Wen; Chang, Yao-Sheng BMC Biotechnology, Vol. 17, Issue 1 https://doi.org/10.1186/s12896-017-0385-y	journal	August 2017
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Transcriptome analysis of Zymomonas mobilis ZM4 reveals mechanisms of tolerance and detoxification of phenolic aldehyde inhibitors from lignocellulose pretreatment Yi, Xia; Gu, Hanqi; Gao, Qiuqiang Biotechnology for Biofuels, Vol. 8, Issue 1 https://doi.org/10.1186/s13068-015-0333-9	journal	September 2015
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Complete genome sequence and the expression pattern of plasmids of the model ethanologen Zymomonas mobilis ZM4 and its xylose-utilizing derivatives 8b and 2032 Yang, Shihui; Vera, Jessica M.; Grass, Jeff Biotechnology for Biofuels, Vol. 11, Issue 1 https://doi.org/10.1186/s13068-018-1116-x	journal	May 2018
Secretive expression of heterologous β-glucosidase in Zymomonas mobilis Luo, Zichen; Bao, Jie Bioresources and Bioprocessing, Vol. 2, Issue 1 https://doi.org/10.1186/s40643-015-0053-9	journal	June 2015
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Recombinant L-Asparaginase from Zymomonas mobilis: A Potential New Antileukemic Agent Produced in Escherichia coli Einsfeldt, Karen; Baptista, Isis Cavalcante; Pereira, Juliana Christina Castanheira Vicente PLOS ONE, Vol. 11, Issue 6 https://doi.org/10.1371/journal.pone.0156692	journal	June 2016
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