Genomic, Transcriptional, and Phenotypic Analysis of the Glucose Derepressed Clostridium beijerinckii Mutant Exhibiting Acid Crash Phenotype

Seo, Seung‐Oh; Janssen, Holger; Magis, Andrew; Wang, Yi; Lu, Ting; Price, Nathan D.; Jin, Yong‐Su; Blaschek, Hans P.

doi:10.1002/biot.201700182

Genomic, Transcriptional, and Phenotypic Analysis of the Glucose Derepressed Clostridium beijerinckii Mutant Exhibiting Acid Crash Phenotype

Journal Article · Mon Oct 09 04:00:00 EDT 2017 · Biotechnology Journal

DOI:https://doi.org/10.1002/biot.201700182· OSTI ID:1398726

^[1]; Janssen, Holger ^[2]; Magis, Andrew ^[3]; Wang, Yi ^[4]; Lu, Ting ^[5]; Price, Nathan D. ^[3]; Jin, Yong‐Su ^[1]; Blaschek, Hans P. ^[6]

Department of Food Science and Human Nutrition University of Illinois at Urbana‐Champaign Urbana IL 61801 USA, Carl R. Woese Institute for Genomic Biology University of Illinois at Urbana‐Champaign Urbana IL 61801 USA
Department of Food Science and Human Nutrition University of Illinois at Urbana‐Champaign Urbana IL 61801 USA
Institute for Systems Biology Seattle WA USA
Biosystems Engineering Department Auburn University Auburn AL 36849 USA
Carl R. Woese Institute for Genomic Biology University of Illinois at Urbana‐Champaign Urbana IL 61801 USA, Department of Bioengineering and Department of Physics University of Illinois at Urbana‐Champaign Urbana IL 61801 USA
Department of Food Science and Human Nutrition University of Illinois at Urbana‐Champaign Urbana IL 61801 USA, The Integrated Bioprocessing Research Laboratory (IBRL) University of Illinois at Urbana‐Champaign Urbana IL 61801 USA

Clostridium beijerinckii is a predominant solventogenic bacterium that is used for the ABE fermentation. Various C. beijerinckii mutants are constructed for desirable phenotypes. The C. beijerinckii mutant BA105 harboring a glucose derepression phenotype was previously isolated and demonstrated the enhanced amylolytic activity in the presence of glucose. Despite its potential use, BA105 is not further characterized and utilized. Therefore, the authors investigate fermentation phenotypes of BA105 in this study. Under the typical batch fermentation conditions, BA105 consistently exhibits acid crash phenotype resulting in limited glucose uptake and cell growth. However, when the culture pH is maintained above 5.5, BA105 exhibits the increased glucose uptake and butanol production than did the wild‐type. To further analyze BA105, the authors perform genome sequencing and RNA sequencing. Genome analysis identifies two SNPs unique to BA105, in the upstream region of AbrB regulator (Cbei_4885) and the ROK family glucokinase (Cbei_4895) which are involved in catabolite repression and regulation of sugar metabolism. Transcriptional analysis of BA105 reveals significant differential expression of the genes associated with the PTS sugar transport system and acid production. This study improves understanding of the acid crash phenomenon and provides the genetic basis underlying the catabolite derepression phenotype of C. beijericnkii .

View Accepted Manuscript (Publisher)

Sponsoring Organization:: USDOE

OSTI ID:: 1398726

Journal Information:: Biotechnology Journal, Journal Name: Biotechnology Journal Journal Issue: 11 Vol. 12; ISSN 1860-6768

Publisher:: Wiley Blackwell (John Wiley & Sons)Copyright Statement

Country of Publication:: Germany

Language:: English

References (41)

CRISPR-based genome editing and expression control systems in Clostridium acetobutylicum and Clostridium beijerinckii Li, Qi; Chen, Jun; Minton, Nigel P. Biotechnology Journal, Vol. 11, Issue 7 https://doi.org/10.1002/biot.201600053	journal	June 2016
Characterization of a Clostridium beijerinckii spo0A mutant and its application for butyl butyrate production : Butyl Butyrate Production by Seo, Seung-Oh; Wang, Yi; Lu, Ting Biotechnology and Bioengineering, Vol. 114, Issue 1 https://doi.org/10.1002/bit.26057	journal	August 2016
Macromolecular Assembly of the Transition State Regulator AbrB in Its Unbound and Complexed States Probed by Microelectrospray Ionization Mass Spectrometry Benson, Linda M.; Vaughn, Jeffrey L.; Strauch, Mark A. Analytical Biochemistry, Vol. 306, Issue 2 https://doi.org/10.1006/abio.2002.5704	journal	July 2002
Microbial genome analyses: comparative transport capabilities in eighteen prokaryotes 1 1Edited by G. von Heijne Paulsen, Ian T.; Nguyen, Lily; Sliwinski, Marek K. Journal of Molecular Biology, Vol. 301, Issue 1 https://doi.org/10.1006/jmbi.2000.3961	journal	August 2000
Resistance to 2-deoxyglucose in yeast: A direct selection of mutants lacking glucose-phosphorylating enzymes Loba, Zita; Maitra, P. K. MGG Molecular & General Genetics, Vol. 157, Issue 3 https://doi.org/10.1007/BF00268666	journal	January 1977
Purification and characterization of the pyruvate-ferredoxin oxidoreductase from Clostridium acetobutylicum Meinecke, B.; Bertram, J.; Gottschalk, G. Archives of Microbiology, Vol. 152, Issue 3 https://doi.org/10.1007/BF00409658	journal	August 1989
Buffering as a means for increasing growth and butanol production byClostridium acetobutylicum Bryant, Dennis L.; Blaschek, Hans P. Journal of Industrial Microbiology, Vol. 3, Issue 1 https://doi.org/10.1007/BF01569442	journal	February 1988
Roles of three AbrBs in regulating two-phase Clostridium acetobutylicum fermentation Xue, Qiong; Yang, Yunpeng; Chen, Jun Applied Microbiology and Biotechnology, Vol. 100, Issue 21 https://doi.org/10.1007/s00253-016-7638-x	journal	June 2016
Clostridium beijerinckii mutant obtained by atmospheric pressure glow discharge producing high proportions of butanol and solvent yields Guo, Ting; Tang, Yan; Xi, Yong-lan Biotechnology Letters, Vol. 33, Issue 12 https://doi.org/10.1007/s10529-011-0702-9	journal	July 2011
Enhancement of butanol tolerance and butanol yield in Clostridium acetobutylicum mutant NT642 obtained by nitrogen ion beam implantation Liu, Xiao-Bo; Gu, Qiu-Ya; Yu, Xiao-Bin Journal of Microbiology, Vol. 50, Issue 6 https://doi.org/10.1007/s12275-012-2289-9	journal	December 2012
Bacterial Genome Editing with CRISPR-Cas9: Deletion, Integration, Single Nucleotide Modification, and Desirable “Clean” Mutant Selection in Clostridium beijerinckii as an Example Wang, Yi; Zhang, Zhong-Tian; Seo, Seung-Oh ACS Synthetic Biology, Vol. 5, Issue 7 https://doi.org/10.1021/acssynbio.6b00060	journal	April 2016
Production of Acetone Butanol Ethanol (ABE) by a Hyper-Producing Mutant Strain of Clostridium beijerinckii BA101 and Recovery by Pervaporation Qureshi, N.; Blaschek, H. P. Biotechnology Progress, Vol. 15, Issue 4 https://doi.org/10.1021/bp990080e	journal	August 1999
Highly efficient RNA-guided base editing in mouse embryos Kim, Kyoungmi; Ryu, Seuk-Min; Kim, Sang-Tae Nature Biotechnology, Vol. 35, Issue 5 https://doi.org/10.1038/nbt.3816	journal	February 2017
Recent advances in ABE fermentation: hyper-butanol producing Clostridium beijerinckii BA101 Qureshi, N.; Blaschek, Hp Journal of Industrial Microbiology and Biotechnology, Vol. 27, Issue 5 https://doi.org/10.1038/sj.jim.7000114	journal	November 2001
Degeneration of solventogenic Clostridium strains monitored by Fourier transform infrared spectroscopy of bacterial cells Schuster, Kc; Goodacre, R.; Gapes, Jr Journal of Industrial Microbiology and Biotechnology, Vol. 27, Issue 5 https://doi.org/10.1038/sj.jim.7000146	journal	November 2001
Spo0A directly controls the switch from acid to solvent production in solvent-forming clostridia Ravagnani, Adriana; Jennert, Katrin C. B.; Steiner, Elisabeth Molecular Microbiology, Vol. 37, Issue 5 https://doi.org/10.1046/j.1365-2958.2000.02071.x	journal	September 2000
Integrated, systems metabolic picture of acetone-butanol-ethanol fermentation by Clostridium acetobutylicum Liao, Chen; Seo, Seung-Oh; Celik, Venhar Proceedings of the National Academy of Sciences, Vol. 112, Issue 27 https://doi.org/10.1073/pnas.1423143112	journal	June 2015
The SpoOA protein of Bacillus subtilis is a repressor of the abrB gene. Strauch, M.; Webb, V.; Spiegelman, G. Proceedings of the National Academy of Sciences, Vol. 87, Issue 5 https://doi.org/10.1073/pnas.87.5.1801	journal	March 1990
The Sequence Alignment/Map format and SAMtools Li, H.; Handsaker, B.; Wysoker, A. Bioinformatics, Vol. 25, Issue 16 https://doi.org/10.1093/bioinformatics/btp352	journal	June 2009
Comparative phenotypic analysis and genome sequence of Clostridium beijerinckii SA-1, an offspring of NCIMB 8052 Sandoval-Espinola, W. J.; Makwana, S. T.; Chinn, M. S. Microbiology, Vol. 159, Issue Pt_12 https://doi.org/10.1099/mic.0.069534-0	journal	September 2013
Structure of the gene for the transition state regulator, abrB: regulator synthesis is controlled by the spo0A sporulation gene in Bacillus subtilis Perego, M.; Spiegelman, G. B.; Hoch, J. A. Molecular Microbiology, Vol. 2, Issue 6 https://doi.org/10.1111/j.1365-2958.1988.tb00079.x	journal	November 1988
The glucose kinase gene of Streptomyces coelicolor A3(2): its nucleotide sequence, transcriptional analysis and role in glucose repression Angell, S.; Schwarz, E.; Bibb, M. J. Molecular Microbiology, Vol. 6, Issue 19 https://doi.org/10.1111/j.1365-2958.1992.tb01463.x	journal	October 1992
Alternative strategies of 2-deoxyglucose resistance and low affinity glucose transport in the ruminal bacteria, Streptococcus bovis and Selenomonas ruminantium Cook, Gregory M.; Russell, James B. FEMS Microbiology Letters, Vol. 123, Issue 1-2 https://doi.org/10.1111/j.1574-6968.1994.tb07223.x	journal	October 1994
Transcriptional Analysis of Clostridium beijerinckii NCIMB 8052 and the Hyper-Butanol-Producing Mutant BA101 during the Shift from Acidogenesis to Solventogenesis Shi, Z.; Blaschek, H. P. Applied and Environmental Microbiology, Vol. 74, Issue 24 https://doi.org/10.1128/AEM.01948-08	journal	October 2008
Butanol Production by a Butanol-Tolerant Strain of Clostridium acetobutylicum in Extruded Corn Broth Lin, Yun-Long; Blaschek, Hans P. Applied and Environmental Microbiology, Vol. 45, Issue 3 https://doi.org/10.1128/AEM.45.3.966-973.1983	journal	January 1983
Isolation and characterization of Clostridium acetobutylicum mutants with enhanced amylolytic activity. Annous, B. A.; Blaschek, H. P. Applied and Environmental Microbiology, Vol. 57, Issue 9 https://doi.org/10.1128/AEM.57.9.2544-2548.1991	journal	January 1991
Enhanced Butanol Production by Clostridium beijerinckii BA101 Grown in Semidefined P2 Medium Containing 6 Percent Maltodextrin or Glucose. Formanek, J.; Mackie, R.; Blaschek, H. P. Applied and environmental microbiology, Vol. 63, Issue 6 https://doi.org/10.1128/AEM.63.6.2306-2310.1997	journal	January 1997
Glucose Uptake in Clostridium beijerinckii NCIMB 8052 and the Solvent-Hyperproducing Mutant BA101 Lee, J.; Blaschek, H. P. Applied and Environmental Microbiology, Vol. 67, Issue 11 https://doi.org/10.1128/AEM.67.11.5025-5031.2001	journal	November 2001
Expression of abrB310 and sinR, and Effects of Decreased abrB310 Expression on the Transition from Acidogenesis to Solventogenesis, in Clostridium acetobutylicum ATCC 824 Scotcher, M. C.; Rudolph, F. B.; Bennett, G. N. Applied and Environmental Microbiology, Vol. 71, Issue 4 https://doi.org/10.1128/AEM.71.4.1987-1995.2005	journal	April 2005
Evidence for the Presence of an Alternative Glucose Transport System in Clostridium beijerinckii NCIMB 8052 and the Solvent-Hyperproducing Mutant BA101 Lee, J.; Mitchell, W. J.; Tangney, M. Applied and Environmental Microbiology, Vol. 71, Issue 6 https://doi.org/10.1128/AEM.71.6.3384-3387.2005	journal	June 2005
Transcription of the pst Operon of Clostridium acetobutylicum Is Dependent on Phosphate Concentration and pH Fischer, R. -J.; Oehmcke, S.; Meyer, U. Journal of Bacteriology, Vol. 188, Issue 15 https://doi.org/10.1128/JB.00491-06	journal	July 2006
Mutations That Confer Resistance to 2-Deoxyglucose Reduce the Specific Activity of Hexokinase from Myxococcus xanthus Youderian, Philip; Lawes, Matthew C.; Creighton, Chad Journal of Bacteriology, Vol. 181, Issue 7 https://doi.org/10.1128/JB.181.7.2225-2235.1999	journal	April 1999
Genome Sequence and Comparative Analysis of the Solvent-Producing Bacterium Clostridium acetobutylicum Nolling, J.; Breton, G.; Omelchenko, M. V. Journal of Bacteriology, Vol. 183, Issue 16 https://doi.org/10.1128/JB.183.16.4823-4838.2001	journal	August 2001
Modulation of Bacillus subtilis catabolite repression by transition state regulatory protein AbrB. Fisher, S. H.; Strauch, M. A.; Atkinson, M. R. Journal of Bacteriology, Vol. 176, Issue 7 https://doi.org/10.1128/jb.176.7.1903-1912.1994	journal	April 1994
Glucose kinase-dependent catabolite repression in Staphylococcus xylosus. Wagner, E.; Marcandier, S.; Egeter, O. Journal of Bacteriology, Vol. 177, Issue 21 https://doi.org/10.1128/jb.177.21.6144-6152.1995	journal	November 1995
Contribution of glucose kinase to glucose repression of xylose utilization in Bacillus megaterium. Späth, C.; Kraus, A.; Hillen, W. Journal of Bacteriology, Vol. 179, Issue 23 https://doi.org/10.1128/jb.179.23.7603-7605.1997	journal	December 1997
Enhanced Butanol Production Obtained by Reinforcing the Direct Butanol-Forming Route in Clostridium acetobutylicum Jang, Yu-Sin; Lee, Jin Young; Lee, Joungmin mBio, Vol. 3, Issue 5 https://doi.org/10.1128/mBio.00314-12	journal	October 2012
Genetic Networks Controlling the Initiation of Sporulation and the Development of Genetic Competence in Bacillus subtilis Grossman, Alan D. Annual Review of Genetics, Vol. 29, Issue 1 https://doi.org/10.1146/annurev.ge.29.120195.002401	journal	December 1995
Single-nucleotide resolution analysis of the transcriptome structure of Clostridium beijerinckii NCIMB 8052 using RNA-Seq Wang, Yi; Li, Xiangzhen; Mao, Yuejian BMC Genomics, Vol. 12, Issue 1 https://doi.org/10.1186/1471-2164-12-479	journal	September 2011
Genome-wide dynamic transcriptional profiling in Clostridium beijerinckii NCIMB 8052 using single-nucleotide resolution RNA-Seq Wang, Yi; Li, Xiangzhen; Mao, Yuejian BMC Genomics, Vol. 13, Issue 1 https://doi.org/10.1186/1471-2164-13-102	journal	January 2012
A comparison of three pH control methods for revealing effects of undissociated butyric acid on specific butanol production rate in batch fermentation of Clostridium acetobutylicum Yang, Xuepeng; Tu, Maobing; Xie, Rui AMB Express, Vol. 3, Issue 1 https://doi.org/10.1186/2191-0855-3-3	journal	January 2013

Similar Records

Characterization of a Clostridium beijerinckii spo0A mutant and its application for butyl butyrate production

Journal Article · Wed Aug 17 00:00:00 EDT 2016 · Biotechnology and Bioengineering · OSTI ID:1401466

Multiplex growth rate phenotyping of synthetic mutants in selection to engineer glucose and xylose co‐utilization in Escherichia coli

Journal Article · Wed Dec 14 23:00:00 EST 2016 · Biotechnology and Bioengineering · OSTI ID:1400465

Complete Genome Sequence of Solvent-Tolerant Clostridium beijerinckii Strain SA-1

Journal Article · Wed Dec 17 23:00:00 EST 2014 · Genome Announcements · OSTI ID:1629632

Genomic, Transcriptional, and Phenotypic Analysis of the Glucose Derepressed Clostridium beijerinckii Mutant Exhibiting Acid Crash Phenotype

Citation Formats

References (41)

Similar Records

Related Subjects