Complex and extensive post-transcriptional regulation revealed by integrative proteomic and transcriptomic analysis of metabolite stress response in Clostridium acetobutylicum
Abstract
Clostridium acetobutylicum is a model organism for both clostridial biology and solvent production. The organism is exposed to its own toxic metabolites butyrate and butanol, which trigger an adaptive stress response. Integrative analysis of proteomic and RNAseq data may provide novel insights into post-transcriptional regulation.
- Authors:
- Publication Date:
- Research Org.:
- Univ. of Delaware, Newark, DE (United States)
- Sponsoring Org.:
- USDOE
- OSTI Identifier:
- 1618624
- Alternate Identifier(s):
- OSTI ID: 1454687
- Grant/Contract Number:
- DESC0007092; sc0007092
- Resource Type:
- Published Article
- Journal Name:
- Biotechnology for Biofuels
- Additional Journal Information:
- Journal Name: Biotechnology for Biofuels Journal Volume: 8 Journal Issue: 1; Journal ID: ISSN 1754-6834
- Publisher:
- Springer Science + Business Media
- Country of Publication:
- Netherlands
- Language:
- English
- Subject:
- 59 BASIC BIOLOGICAL SCIENCES
Citation Formats
Venkataramanan, Keerthi P., Min, Lie, Hou, Shuyu, Jones, Shawn W., Ralston, Matthew T., Lee, Kelvin H., and Papoutsakis, E. Terry. Complex and extensive post-transcriptional regulation revealed by integrative proteomic and transcriptomic analysis of metabolite stress response in Clostridium acetobutylicum. Netherlands: N. p., 2015.
Web. doi:10.1186/s13068-015-0260-9.
Venkataramanan, Keerthi P., Min, Lie, Hou, Shuyu, Jones, Shawn W., Ralston, Matthew T., Lee, Kelvin H., & Papoutsakis, E. Terry. Complex and extensive post-transcriptional regulation revealed by integrative proteomic and transcriptomic analysis of metabolite stress response in Clostridium acetobutylicum. Netherlands. https://doi.org/10.1186/s13068-015-0260-9
Venkataramanan, Keerthi P., Min, Lie, Hou, Shuyu, Jones, Shawn W., Ralston, Matthew T., Lee, Kelvin H., and Papoutsakis, E. Terry. Wed .
"Complex and extensive post-transcriptional regulation revealed by integrative proteomic and transcriptomic analysis of metabolite stress response in Clostridium acetobutylicum". Netherlands. https://doi.org/10.1186/s13068-015-0260-9.
@article{osti_1618624,
title = {Complex and extensive post-transcriptional regulation revealed by integrative proteomic and transcriptomic analysis of metabolite stress response in Clostridium acetobutylicum},
author = {Venkataramanan, Keerthi P. and Min, Lie and Hou, Shuyu and Jones, Shawn W. and Ralston, Matthew T. and Lee, Kelvin H. and Papoutsakis, E. Terry},
abstractNote = {Clostridium acetobutylicum is a model organism for both clostridial biology and solvent production. The organism is exposed to its own toxic metabolites butyrate and butanol, which trigger an adaptive stress response. Integrative analysis of proteomic and RNAseq data may provide novel insights into post-transcriptional regulation.},
doi = {10.1186/s13068-015-0260-9},
journal = {Biotechnology for Biofuels},
number = 1,
volume = 8,
place = {Netherlands},
year = {Wed Jun 10 00:00:00 EDT 2015},
month = {Wed Jun 10 00:00:00 EDT 2015}
}
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https://doi.org/10.1186/s13068-015-0260-9
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Works referenced in this record:
Exploring the Heterologous Genomic Space for Building, Stepwise, Complex, Multicomponent Tolerance to Toxic Chemicals
journal, November 2013
- Zingaro, Kyle A.; Nicolaou, Sergios A.; Yuan, Yongbo
- ACS Synthetic Biology, Vol. 3, Issue 7
Clostridia: the importance of their exceptional substrate and metabolite diversity for biofuel and biorefinery applications
journal, June 2012
- Tracy, Bryan P.; Jones, Shawn W.; Fast, Alan G.
- Current Opinion in Biotechnology, Vol. 23, Issue 3
Selective Translation of Leaderless mRNAs by Specialized Ribosomes Generated by MazF in Escherichia coli
journal, September 2011
- Vesper, Oliver; Amitai, Shahar; Belitsky, Maria
- Cell, Vol. 147, Issue 1
The influence of ribosome-binding-site elements on translational efficiency in Bacillus subtilis and Escherichia coli in vivo
journal, May 1992
- Vellanoweth, Robert Luis; Rabinowitz, Jesse C.
- Molecular Microbiology, Vol. 6, Issue 9
Exploring glycopeptide-resistance in Staphylococcus aureus: a combined proteomics and transcriptomics approach for the identification of resistance-related markers
journal, November 2006
- Scherl, Alexander; François, Patrice; Charbonnier, Yvan
- BMC Genomics, Vol. 7, Issue 1
The small RNA, DsrA, is essential for the low temperature expression of RpoS during exponential growth in Escherichia coli.
journal, August 1996
- Sledjeski, D. D.; Gupta, A.; Gottesman, S.
- The EMBO Journal, Vol. 15, Issue 15
Toward a Semisynthetic Stress Response System To Engineer Microbial Solvent Tolerance
journal, October 2012
- Zingaro, Kyle A.; Papoutsakis, Eleftherios Terry
- mBio, Vol. 3, Issue 5
Workflow for quantitative proteomic analysis of Clostridium acetobutylicum ATCC 824 using iTRAQ tags
journal, June 2013
- Hou, Shuyu; Jones, Shawn W.; Choe, Leila H.
- Methods, Vol. 61, Issue 3
Comparative shotgun proteomic analysis of Clostridium acetobutylicum from butanol fermentation using glucose and xylose
journal, January 2011
- Sivagnanam, Kumaran; Raghavan, Vijaya GS; Shah, Manesh
- Proteome Science, Vol. 9, Issue 1
Transcriptome and proteome quantification of a tumor model provides novel insights into post‐transcriptional gene regulation
journal, January 2013
- Jüschke, Christoph; Dohnal, Ilse; Pichler, Peter
- Genome Biology, Vol. 14, Issue 11
Trimmomatic: a flexible trimmer for Illumina sequence data
journal, April 2014
- Bolger, Anthony M.; Lohse, Marc; Usadel, Bjoern
- Bioinformatics, Vol. 30, Issue 15
Transcriptional organization of the Clostridium acetobutylicum genome
journal, March 2004
- Paredes, C. J.
- Nucleic Acids Research, Vol. 32, Issue 6
Reductive dioxygen scavenging by flavo-diiron proteins of Clostridium acetobutylicum
journal, December 2008
- Hillmann, Falk; Riebe, Oliver; Fischer, Ralf-Jörg
- FEBS Letters, Vol. 583, Issue 1
Characterization of Clostridium acetobutylicum Protein Interaction Network from Butanol Fermentation
journal, January 2013
- Sivagnanam, Kumaran
- Journal of Analytical & Bioanalytical Techniques, Vol. 04, Issue 03
The anatomy of microbial cell state transitions in response to oxygen
journal, September 2007
- Schmid, A. K.; Reiss, D. J.; Kaur, A.
- Genome Research, Vol. 17, Issue 10
Application of new metabolic engineering tools for Clostridium acetobutylicum
journal, May 2014
- Lütke-Eversloh, Tina
- Applied Microbiology and Biotechnology, Vol. 98, Issue 13
Global mapping of transcription start sites and promoter motifs in the symbiotic α-proteobacterium Sinorhizobium meliloti 1021
journal, January 2013
- Schlüter, Jan-Philip; Reinkensmeier, Jan; Barnett, Melanie J.
- BMC Genomics, Vol. 14, Issue 1
Phosphoproteomic investigation of a solvent producing bacterium Clostridium acetobutylicum
journal, May 2012
- Bai, Xue; Ji, Zhihong
- Applied Microbiology and Biotechnology, Vol. 95, Issue 1
Leaderless genes in bacteria: clue to the evolution of translation initiation mechanisms in prokaryotes
journal, July 2011
- Zheng, Xiaobin; Hu, Gang-Qing; She, Zhen-Su
- BMC Genomics, Vol. 12, Issue 1
Prodigal: prokaryotic gene recognition and translation initiation site identification
journal, March 2010
- Hyatt, Doug; Chen, Gwo-Liang; LoCascio, Philip F.
- BMC Bioinformatics, Vol. 11, Issue 1
The heat shock response of Synechocystis sp. PCC 6803 analysed by transcriptomics and proteomics
journal, March 2006
- Suzuki, I.
- Journal of Experimental Botany, Vol. 57, Issue 7
Small RNA Regulators and the Bacterial Response to Stress
journal, January 2006
- Gottesman, S.; McCULLEN, C. A.; Guillier, M.
- Cold Spring Harbor Symposia on Quantitative Biology, Vol. 71, Issue 0
Oxidative stress response in Clostridium perfringens
journal, June 2004
- Jean, D.
- Microbiology, Vol. 150, Issue 6
The transcriptional landscape and small RNAs of Salmonella enterica serovar Typhimurium
journal, April 2012
- Kroger, C.; Dillon, S. C.; Cameron, A. D. S.
- Proceedings of the National Academy of Sciences, Vol. 109, Issue 20
Adaptation of Bacillus subtilis to growth at low temperature: a combined transcriptomic and proteomic appraisal
journal, March 2006
- Budde, I.
- Microbiology, Vol. 152, Issue 3
Computational analysis of bacterial RNA-Seq data
journal, May 2013
- McClure, Ryan; Balasubramanian, Divya; Sun, Yan
- Nucleic Acids Research, Vol. 41, Issue 14
A small RNA regulates multiple ABC transporter mRNAs by targeting C/A-rich elements inside and upstream of ribosome-binding sites
journal, November 2007
- Sharma, C. M.; Darfeuille, F.; Plantinga, T. H.
- Genes & Development, Vol. 21, Issue 21
Systems Biology Analysis of Zymomonas mobilis ZM4 Ethanol Stress Responses
journal, July 2013
- Yang, Shihui; Pan, Chongle; Tschaplinski, Timothy J.
- PLoS ONE, Vol. 8, Issue 7
Uncovering Genes with Divergent mRNA-Protein Dynamics in Streptomyces coelicolor
journal, May 2008
- Jayapal, Karthik P.; Philp, Robin J.; Kok, Yee-Jiun
- PLoS ONE, Vol. 3, Issue 5
TM4: A Free, Open-Source System for Microarray Data Management and Analysis
journal, February 2003
- Saeed, A. I.; Sharov, V.; White, J.
- BioTechniques, Vol. 34, Issue 2
The transcriptional program underlying the physiology of clostridial sporulation
journal, January 2008
- Jones, Shawn W.; Paredes, Carlos J.; Tracy, Bryan
- Genome Biology, Vol. 9, Issue 7
GroESL overexpression imparts Escherichia coli tolerance to i-, n-, and 2-butanol, 1,2,4-butanetriol and ethanol with complex and unpredictable patterns
journal, January 2013
- Zingaro, Kyle A.; Terry Papoutsakis, Eleftherios
- Metabolic Engineering, Vol. 15
Genome-wide Mapping of Transcriptional Start Sites Defines an Extensive Leaderless Transcriptome in Mycobacterium tuberculosis
journal, November 2013
- Cortes, Teresa; Schubert, Olga T.; Rose, Graham
- Cell Reports, Vol. 5, Issue 4
Homeoviscous response of Clostridium pasteurianum to butanol toxicity during glycerol fermentation
journal, June 2014
- Venkataramanan, Keerthi P.; Kurniawan, Yogi; Boatman, Judy J.
- Journal of Biotechnology, Vol. 179
A transcriptional study of acidogenic chemostat cells of Clostridium acetobutylicum – Cellular behavior in adaptation to n-butanol
journal, October 2012
- Schwarz, Katrin M.; Kuit, Wouter; Grimmler, Christina
- Journal of Biotechnology, Vol. 161, Issue 3
Terminator still moving forward: expanding roles for Rho factor
journal, April 2013
- Boudvillain, Marc; Figueroa-Bossi, Nara; Bossi, Lionello
- Current Opinion in Microbiology, Vol. 16, Issue 2
Dissecting the assays to assess microbial tolerance to toxic chemicals in bioprocessing
journal, November 2013
- Zingaro, Kyle A.; Nicolaou, Sergios A.; Papoutsakis, Eleftherios T.
- Trends in Biotechnology, Vol. 31, Issue 11
The rubrerythrin-like protein Hsp21 of Clostridium acetobutylicum is a general stress protein
journal, February 2006
- Hillmann, Falk; Fischer, Ralf-Jörg; Bahl, Hubert
- Archives of Microbiology, Vol. 185, Issue 4
Codon bias and heterologous protein expression
journal, July 2004
- Gustafsson, Claes; Govindarajan, Sridhar; Minshull, Jeremy
- Trends in Biotechnology, Vol. 22, Issue 7
Leaderless mRNAs in bacteria: surprises in ribosomal recruitment and translational control
journal, January 2002
- Moll, Isabella; Grill, Sonja; Gualerzi, Claudio O.
- Molecular Microbiology, Vol. 43, Issue 1
Toward a protein profile of Escherichia coli: Comparison to its transcription profile
journal, July 2003
- Corbin, R. W.; Paliy, O.; Yang, F.
- Proceedings of the National Academy of Sciences, Vol. 100, Issue 16
Capturing the response of Clostridium acetobutylicumto chemical stressors using a regulated genome-scale metabolic model
journal, October 2014
- Dash, Satyakam; Mueller, Thomas J.; Venkataramanan, Keerthi P.
- Biotechnology for Biofuels, Vol. 7, Issue 1
RNA Polymerase Elongation Factors
journal, October 2008
- Roberts, Jeffrey W.; Shankar, Smita; Filter, Joshua J.
- Annual Review of Microbiology, Vol. 62, Issue 1
Synthetic tolerance: three noncoding small RNAs, DsrA, ArcZ and RprA, acting supra-additively against acid stress
journal, July 2013
- Gaida, S. M.; Al-Hinai, M. A.; Indurthi, D. C.
- Nucleic Acids Research, Vol. 41, Issue 18
Significance analysis of microarrays applied to the ionizing radiation response
journal, April 2001
- Tusher, V. G.; Tibshirani, R.; Chu, G.
- Proceedings of the National Academy of Sciences, Vol. 98, Issue 9, p. 5116-5121
The redox-sensing protein Rex, a transcriptional regulator of solventogenesis in Clostridium acetobutylicum
journal, May 2012
- Wietzke, Mandy; Bahl, Hubert
- Applied Microbiology and Biotechnology, Vol. 96, Issue 3
Dynamical Analysis of Gene Networks Requires Both mRNA and Protein Expression Information
journal, October 1999
- Hatzimanikatis, Vassily; Lee, Kelvin H.
- Metabolic Engineering, Vol. 1, Issue 4
Comparative analysis on the membrane proteome of Clostridium acetobutylicum wild type strain and its butanol-tolerant mutant
journal, January 2011
- Mao, Shaoming; Luo, Yuanming; Bao, Guanhui
- Molecular BioSystems, Vol. 7, Issue 5
Global transcriptional changes of Clostridium acetobutylicum cultures with increased butanol:acetone ratios
journal, May 2012
- Hönicke, Daniel; Janssen, Holger; Grimmler, Christina
- New Biotechnology, Vol. 29, Issue 4
Proteomic analyses of the phase transition from acidogenesis to solventogenesis using solventogenic and non-solventogenic Clostridium acetobutylicum strains
journal, April 2014
- Jang, Yu-Sin; Han, Mee-Jung; Lee, Joungmin
- Applied Microbiology and Biotechnology, Vol. 98, Issue 11
Engineering solventogenic clostridia
journal, October 2008
- Papoutsakis, Eleftherios T.
- Current Opinion in Biotechnology, Vol. 19, Issue 5, p. 420-429
Integrating multiple 'omics' analysis for microbial biology: application and methodologies
journal, November 2009
- Zhang, W.; Li, F.; Nie, L.
- Microbiology, Vol. 156, Issue 2
Selective translation during stress in Escherichia coli
journal, November 2012
- Moll, Isabella; Engelberg-Kulka, Hanna
- Trends in Biochemical Sciences, Vol. 37, Issue 11
A transcriptional study of acidogenic chemostat cells of Clostridium acetobutylicum—Solvent stress caused by a transient n-butanol pulse
journal, October 2012
- Janssen, Holger; Grimmler, Christina; Ehrenreich, Armin
- Journal of Biotechnology, Vol. 161, Issue 3
Transcriptional Analysis of Butanol Stress and Tolerance in Clostridium acetobutylicum
journal, March 2004
- Tomas, C. A.; Beamish, J.; Papoutsakis, E. T.
- Journal of Bacteriology, Vol. 186, Issue 7
Regulation of transcriptome, translation, and proteome in response to environmental stress in fission yeast
journal, January 2012
- Lackner, Daniel H.; Schmidt, Michael W.; Wu, Shuangding
- Genome Biology, Vol. 13, Issue 4
Maintenance of pH by a butanol-tolerant mutant of Clostridium beijerinckii
journal, February 2005
- Wang, F.
- Microbiology, Vol. 151, Issue 2
Proteome analysis and comparison of Clostridium acetobutylicum ATCC 824 and Spo0A strain variants
journal, November 2005
- Sullivan, Leighann; Bennett, George N.
- Journal of Industrial Microbiology & Biotechnology, Vol. 33, Issue 4
Exploring the combinatorial genomic space in Escherichia coli for ethanol tolerance
journal, September 2012
- Nicolaou, Sergios A.; Gaida, Stefan M.; Papoutsakis, Eleftherios T.
- Biotechnology Journal, Vol. 7, Issue 11
Transcription factors and genetic circuits orchestrating the complex, multilayered response of Clostridium acetobutylicum to butanol and butyrate stress
journal, January 2013
- Wang, Qinghua; Venkataramanan, Keerthi; Huang, Hongzhan
- BMC Systems Biology, Vol. 7, Issue 1
Transcriptional Program of Early Sporulation and Stationary-Phase Events in Clostridium acetobutylicum
journal, September 2005
- Alsaker, K. V.; Papoutsakis, E. T.
- Journal of Bacteriology, Vol. 187, Issue 20
The Clostridium small RNome that responds to stress: the paradigm and importance of toxic metabolite stress in C. acetobutylicum
journal, January 2013
- Venkataramanan, Keerthi P.; Jones, Shawn W.; McCormick, Kevin P.
- BMC Genomics, Vol. 14, Issue 1
Transport of Substrates and Metabolites and Their Effect on Cell Metabolism (in Butyric-Acid and Methylotrophic Fermentations)
journal, November 1987
- Papoutsakis, E. T.; Bussineau, C. M.; Chu, I-M.
- Annals of the New York Academy of Sciences, Vol. 506, Issue 1 Biochemical E
A proteomic and transcriptional view of acidogenic and solventogenic steady-state cells of Clostridium acetobutylicum in a chemostat culture
journal, July 2010
- Janssen, Holger; Döring, Christina; Ehrenreich, Armin
- Applied Microbiology and Biotechnology, Vol. 87, Issue 6
Works referencing / citing this record:
Quantitative proteomic analysis of the influence of lignin on biofuel production by Clostridium acetobutylicum ATCC 824
journal, May 2016
- Raut, Mahendra P.; Couto, Narciso; Pham, Trong K.
- Biotechnology for Biofuels, Vol. 9, Issue 1
RNAseq-based transcriptome assembly of Clostridium acetobutylicum for functional genome annotation and discovery
journal, October 2018
- Ralston, Matthew T.; Papoutsakis, Eleftherios T.
- AIChE Journal, Vol. 64, Issue 12
The effects of disruption in membrane lipid biosynthetic genes on 1-butanol tolerance of Bacillus subtilis
journal, August 2018
- Vinayavekhin, Nawaporn; Vangnai, Alisa S.
- Applied Microbiology and Biotechnology, Vol. 102, Issue 21
Large-scale and significant expression from pseudogenes in Sodalis glossinidius – a facultative bacterial endosymbiont
journal, January 2020
- Goodhead, Ian; Blow, Frances; Brownridge, Philip
- Microbial Genomics, Vol. 6, Issue 1