Deciphering the Adaptation of Corynebacterium glutamicum in Transition from Aerobiosis via Microaerobiosis to Anaerobiosis

Lange J, Muench E, Mueller J, Busche T, Kalinowski J, Takors R, Blombach B (2018)
GENES 9(6): 297.

Zeitschriftenaufsatz | Veröffentlicht | Englisch
 
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Autor*in
Lange, Julian; Muench, Eugenia; Mueller, Jan; Busche, TobiasUniBi; Kalinowski, JörnUniBi; Takors, Ralf; Blombach, Bastian
Abstract / Bemerkung
Zero-growth processes are a promising strategy for the production of reduced molecules and depict a steady transition from aerobic to anaerobic conditions. To investigate the adaptation of Corynebacterium glutamicum to altering oxygen availabilities, we conceived a triple-phase fermentation process that describes a gradual reduction of dissolved oxygen with a shift from aerobiosis via microaerobiosis to anaerobiosis. The distinct process phases were clearly bordered by the bacteria's physiologic response such as reduced growth rate, biomass substrate yield and altered yield of fermentation products. During the process, sequential samples were drawn at six points and analyzed via RNA-sequencing, for metabolite concentrations and for enzyme activities. We found transcriptional alterations of almost 50% (1421 genes) of the entire protein coding genes and observed an upregulation of fermentative pathways, a rearrangement of respiration, and mitigation of the basic cellular mechanisms such as transcription, translation and replication as a transient response related to the installed oxygen dependent process phases. To investigate the regulatory regime, 18 transcriptionally altered (putative) transcriptional regulators were deleted, but none of the deletion strains showed noticeable growth kinetics under an oxygen restricted environment. However, the described transcriptional adaptation of C. glutamicum resolved to varying oxygen availabilities provides a useful basis for future process and strain engineering.
Stichworte
Corynebacterium glutamicum; transcriptional response; aerobiosis; microaerobiosis; anaerobiosis; triple-phase process
Erscheinungsjahr
2018
Zeitschriftentitel
GENES
Band
9
Ausgabe
6
Art.-Nr.
297
ISSN
2073-4425
Page URI
https://pub.uni-bielefeld.de/record/2930282

Zitieren

Lange J, Muench E, Mueller J, et al. Deciphering the Adaptation of Corynebacterium glutamicum in Transition from Aerobiosis via Microaerobiosis to Anaerobiosis. GENES. 2018;9(6): 297.
Lange, J., Muench, E., Mueller, J., Busche, T., Kalinowski, J., Takors, R., & Blombach, B. (2018). Deciphering the Adaptation of Corynebacterium glutamicum in Transition from Aerobiosis via Microaerobiosis to Anaerobiosis. GENES, 9(6), 297. doi:10.3390/genes9060297
Lange, Julian, Muench, Eugenia, Mueller, Jan, Busche, Tobias, Kalinowski, Jörn, Takors, Ralf, and Blombach, Bastian. 2018. “Deciphering the Adaptation of Corynebacterium glutamicum in Transition from Aerobiosis via Microaerobiosis to Anaerobiosis”. GENES 9 (6): 297.
Lange, J., Muench, E., Mueller, J., Busche, T., Kalinowski, J., Takors, R., and Blombach, B. (2018). Deciphering the Adaptation of Corynebacterium glutamicum in Transition from Aerobiosis via Microaerobiosis to Anaerobiosis. GENES 9:297.
Lange, J., et al., 2018. Deciphering the Adaptation of Corynebacterium glutamicum in Transition from Aerobiosis via Microaerobiosis to Anaerobiosis. GENES, 9(6): 297.
J. Lange, et al., “Deciphering the Adaptation of Corynebacterium glutamicum in Transition from Aerobiosis via Microaerobiosis to Anaerobiosis”, GENES, vol. 9, 2018, : 297.
Lange, J., Muench, E., Mueller, J., Busche, T., Kalinowski, J., Takors, R., Blombach, B.: Deciphering the Adaptation of Corynebacterium glutamicum in Transition from Aerobiosis via Microaerobiosis to Anaerobiosis. GENES. 9, : 297 (2018).
Lange, Julian, Muench, Eugenia, Mueller, Jan, Busche, Tobias, Kalinowski, Jörn, Takors, Ralf, and Blombach, Bastian. “Deciphering the Adaptation of Corynebacterium glutamicum in Transition from Aerobiosis via Microaerobiosis to Anaerobiosis”. GENES 9.6 (2018): 297.

118 References

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FY2015 Market and Other Information
AUTHOR UNKNOWN, 0
Corynebacterium taxonomy
Liebl W.., 2005
Anaerobic growth of Corynebacterium glutamicum using nitrate as a terminal electron acceptor.
Nishimura T, Vertes AA, Shinoda Y, Inui M, Yukawa H., Appl. Microbiol. Biotechnol. 75(4), 2007
PMID: 17347820
Engineering Corynebacterium glutamicum for the production of pyruvate.
Wieschalka S, Blombach B, Eikmanns BJ., Appl. Microbiol. Biotechnol. 94(2), 2012
PMID: 22228312
Biotechnological application of Corynebacterium glutamicum under oxygen deprivation
Jojima T., Inui M., Yukawa H.., 2015
Corynebacterium glutamicum tailored for efficient isobutanol production.
Blombach B, Riester T, Wieschalka S, Ziert C, Youn JW, Wendisch VF, Eikmanns BJ., Appl. Environ. Microbiol. 77(10), 2011
PMID: 21441331
Strain optimization for efficient isobutanol production using Corynebacterium glutamicum under oxygen deprivation.
Yamamoto S, Suda M, Niimi S, Inui M, Yukawa H., Biotechnol. Bioeng. 110(11), 2013
PMID: 23737329
Zero-growth bioprocesses—A challenge for microbial production strains and bioprocess engineering
Lange J., Takors R., Blombach B.., 2017
A novel whole-phase succinate fermentation strategy with high volumetric productivity in engineered Escherichia coli.
Li Y, Li M, Zhang X, Yang P, Liang Q, Qi Q., Bioresour. Technol. 149(), 2013
PMID: 24125798
Bio-based production of organic acids with Corynebacterium glutamicum.
Wieschalka S, Blombach B, Bott M, Eikmanns BJ., Microb Biotechnol 6(2), 2012
PMID: 23199277
Aerobiosis–anaerobiosis transition has a significant impact on organic acid production by Corynebacterium glutamicum
Kaboré A.-K., Olmos E., Fick M., Blanchard F., Guedon E., Delaunay S.., 2016
CO₂ /HCO₃⁻ perturbations of simulated large scale gradients in a scale-down device cause fast transcriptional responses in Corynebacterium glutamicum.
Buchholz J, Graf M, Freund A, Busche T, Kalinowski J, Blombach B, Takors R., Appl. Microbiol. Biotechnol. 98(20), 2014
PMID: 25139448
Response of Corynebacterium glutamicum exposed to oscillating cultivation conditions in a two- and a novel three-compartment scale-down bioreactor.
Lemoine A, Maya Martιnez-Iturralde N, Spann R, Neubauer P, Junne S., Biotechnol. Bioeng. 112(6), 2015
PMID: 25728062
Metabolic profile of 1,5-diaminopentane producing Corynebacterium glutamicum under scale-down conditions: Blueprint for robustness to bioreactor inhomogeneities.
Limberg MH, Schulte J, Aryani T, Mahr R, Baumgart M, Bott M, Wiechert W, Oldiges M., Biotechnol. Bioeng. 114(3), 2016
PMID: 27641904
Substrate gradient formation in the large-scale bioreactor lowers cell yield and increases by-product formation
Bylund F., Collet E., Enfors S.-O., Larsson G.., 1998
Stoichiometric analysis and experimental investigation of glycerol bioconversion to 1,3-propanediol by Klebsiella pneumoniae under microaerobic conditions
Chen X., Xiu Z., Wang J., Zhang D., Xu P.., 2003
Aeration strategy: a need for very high ethanol performance in Saccharomyces cerevisiae fed-batch process.
Alfenore S, Cameleyre X, Benbadis L, Bideaux C, Uribelarrea JL, Goma G, Molina-Jouve C, Guillouet SE., Appl. Microbiol. Biotechnol. 63(5), 2003
PMID: 12879304
Enhanced production of 2,3-butanediol by engineered Bacillus subtilis.
Biswas R, Yamaoka M, Nakayama H, Kondo T, Yoshida K, Bisaria VS, Kondo A., Appl. Microbiol. Biotechnol. 94(3), 2012
PMID: 22361854
Monitoring microaerobic denitrification of Pseudomonas aeruginosa by online NAD(P)H fluorescence.
Ju LK, Chen F, Xia Q., J. Ind. Microbiol. Biotechnol. 32(11-12), 2005
PMID: 16228188

Hewitt L.F.., 1950
The use of redox potential in water treatment processes
Goncharuk V.V., Bagrii V.A., Mel’nik L.A., Chebotareva R.D., Bashtan S.Y.., 2010
Transcriptional profiling of Corynebacterium glutamicum metabolism during organic acid production under oxygen deprivation conditions.
Inui M, Suda M, Okino S, Nonaka H, Puskas LG, Vertes AA, Yukawa H., Microbiology (Reading, Engl.) 153(Pt 8), 2007
PMID: 17660414
Aerobic growth at nanomolar oxygen concentrations.
Stolper DA, Revsbech NP, Canfield DE., Proc. Natl. Acad. Sci. U.S.A. 107(44), 2010
PMID: 20974919
Emerging Corynebacterium glutamicum systems biology.
Wendisch VF, Bott M, Kalinowski J, Oldiges M, Wiechert W., J. Biotechnol. 124(1), 2006
PMID: 16406159
Genome engineering of Corynebacterium glutamicum
Suzuki N., Inui M.., 2013

Burkovski A.., 2015
CRISPR/Cas9-coupled recombineering for metabolic engineering of Corynebacterium glutamicum.
Cho JS, Choi KR, Prabowo CPS, Shin JH, Yang D, Jang J, Lee SY., Metab. Eng. 42(), 2017
PMID: 28649005
Production of amino acids - Genetic and metabolic engineering approaches.
Lee JH, Wendisch VF., Bioresour. Technol. 245(Pt B), 2017
PMID: 28552565
Iron-sulfur cluster disassembly in the FNR protein of Escherichia coli by O2: [4Fe-4S] to [2Fe-2S] conversion with loss of biological activity.
Khoroshilova N, Popescu C, Munck E, Beinert H, Kiley PJ., Proc. Natl. Acad. Sci. U.S.A. 94(12), 1997
PMID: 9177174
FNR is a direct oxygen sensor having a biphasic response curve.
Jordan PA, Thomson AJ, Ralph ET, Guest JR, Green J., FEBS Lett. 416(3), 1997
PMID: 9373183
The ArcBA two-component system of Escherichia coli is regulated by the redox state of both the ubiquinone and the menaquinone pool.
Bekker M, Alexeeva S, Laan W, Sawers G, Teixeira de Mattos J, Hellingwerf K., J. Bacteriol. 192(3), 2009
PMID: 19933363
The aerobic/anaerobic interface.
Sawers G., Curr. Opin. Microbiol. 2(2), 1999
PMID: 10322162
A signal transducer for aerotaxis in Escherichia coli.
Bibikov SI, Biran R, Rudd KE, Parkinson JS., J. Bacteriol. 179(12), 1997
PMID: 9190831
Quinones as the redox signal for the arc two-component system of bacteria.
Georgellis D, Kwon O, Lin EC., Science 292(5525), 2001
PMID: 11423658
Mechanisms for sensing and responding to oxygen deprivation
Patschkowski T., Bates D.M., Kiley P.J.., 2000
Transition of Escherichia coli from aerobic to micro-aerobic conditions involves fast and slow reacting regulatory components.
Partridge JD, Sanguinetti G, Dibden DP, Roberts RE, Poole RK, Green J., J. Biol. Chem. 282(15), 2007
PMID: 17307737
A mathematical model of metabolism and regulation provides a systems-level view of how Escherichia coli responds to oxygen.
Ederer M, Steinsiek S, Stagge S, Rolfe MD, Ter Beek A, Knies D, Teixeira de Mattos MJ, Sauter T, Green J, Poole RK, Bettenbrock K, Sawodny O., Front Microbiol 5(), 2014
PMID: 24723921
Diversity of metabolic shift in response to oxygen deprivation in Corynebacterium glutamicum and its close relatives.
Yamamoto S, Sakai M, Inui M, Yukawa H., Appl. Microbiol. Biotechnol. 90(3), 2011
PMID: 21327408
Development and experimental verification of a genome-scale metabolic model for Corynebacterium glutamicum.
Shinfuku Y, Sorpitiporn N, Sono M, Furusawa C, Hirasawa T, Shimizu H., Microb. Cell Fact. 8(), 2009
PMID: 19646286
pH fluctuations imperil the robustness of C. glutamicum to short term oxygen limitation.
Limberg MH, Joachim M, Klein B, Wiechert W, Oldiges M., J. Biotechnol. 259(), 2017
PMID: 28837821
Process inhomogeneity leads to rapid side product turnover in cultivation of Corynebacterium glutamicum.
Kaß F, Junne S, Neubauer P, Wiechert W, Oldiges M., Microb. Cell Fact. 13(), 2014
PMID: 24410842
Assessment of robustness against dissolved oxygen/substrate oscillations for C. glutamicum DM1933 in two-compartment bioreactor.
Kaß F, Hariskos I, Michel A, Brandt HJ, Spann R, Junne S, Wiechert W, Neubauer P, Oldiges M., Bioprocess Biosyst Eng 37(6), 2013
PMID: 24218302
Living with heterogeneities in bioreactors: understanding the effects of environmental gradients on cells.
Lara AR, Galindo E, Ramirez OT, Palomares LA., Mol. Biotechnol. 34(3), 2006
PMID: 17284782
Scale-up of microbial processes: impacts, tools and open questions.
Takors R., J. Biotechnol. 160(1-2), 2011
PMID: 22206982

Sambrook J., Russell D.W.., 2001
Amplification of three threonine biosynthesis genes in Corynebacterium glutamicum and its influence on carbon flux in different strains.
Eikmanns BJ, Metzger M, Reinscheid D, Kircher M, Sahm H., Appl. Microbiol. Biotechnol. 34(5), 1991
PMID: 1369320
Functional genomics of pH homeostasis in Corynebacterium glutamicum revealed novel links between pH response, oxidative stress, iron homeostasis and methionine synthesis.
Follmann M, Ochrombel I, Kramer R, Trotschel C, Poetsch A, Ruckert C, Huser A, Persicke M, Seiferling D, Kalinowski J, Marin K., BMC Genomics 10(), 2009
PMID: 20025733
Platform engineering of Corynebacterium glutamicum with reduced pyruvate dehydrogenase complex activity for improved production of L-lysine, L-valine, and 2-ketoisovalerate.
Buchholz J, Schwentner A, Brunnenkan B, Gabris C, Grimm S, Gerstmeir R, Takors R, Eikmanns BJ, Blombach B., Appl. Environ. Microbiol. 79(18), 2013
PMID: 23835179
Metabolic approaches for the optimisation of recombinant fermentation processes.
Cserjan-Puschmann M, Kramer W, Duerrschmid E, Striedner G, Bayer K., Appl. Microbiol. Biotechnol. 53(1), 1999
PMID: 10645624
Engineering E. coli for large-scale production - Strategies considering ATP expenses and transcriptional responses.
Loffler M, Simen JD, Jager G, Schaferhoff K, Freund A, Takors R., Metab. Eng. 38(), 2016
PMID: 27378496
In-depth profiling of lysine-producing Corynebacterium glutamicum by combined analysis of the transcriptome, metabolome, and fluxome.
Kromer JO, Sorgenfrei O, Klopprogge K, Heinzle E, Wittmann C., J. Bacteriol. 186(6), 2004
PMID: 14996808
Trimmomatic: a flexible trimmer for Illumina sequence data.
Bolger AM, Lohse M, Usadel B., Bioinformatics 30(15), 2014
PMID: 24695404
Fast gapped-read alignment with Bowtie 2.
Langmead B, Salzberg SL., Nat. Methods 9(4), 2012
PMID: 22388286
The Sequence Alignment/Map format and SAMtools.
Li H, Handsaker B, Wysoker A, Fennell T, Ruan J, Homer N, Marth G, Abecasis G, Durbin R; 1000 Genome Project Data Processing Subgroup., Bioinformatics 25(16), 2009
PMID: 19505943
ReadXplorer 2-detailed read mapping analysis and visualization from one single source.
Hilker R, Stadermann KB, Schwengers O, Anisiforov E, Jaenicke S, Weisshaar B, Zimmermann T, Goesmann A., Bioinformatics 32(24), 2016
PMID: 27540267
Dissecting specific and global transcriptional regulation of bacterial gene expression.
Gerosa L, Kochanowski K, Heinemann M, Sauer U., Mol. Syst. Biol. 9(), 2013
PMID: 23591774
Improving the carbon balance of fermentations by total carbon analyses
Buchholz J., Graf M., Blombach B., Takors R.., 2014
On the diagrammatic and mechanical representation of propositions and reasonings
Venn J.., 1880
The complete Corynebacterium glutamicum ATCC 13032 genome sequence and its impact on the production of L-aspartate-derived amino acids and vitamins.
Kalinowski J, Bathe B, Bartels D, Bischoff N, Bott M, Burkovski A, Dusch N, Eggeling L, Eikmanns BJ, Gaigalat L, Goesmann A, Hartmann M, Huthmacher K, Kramer R, Linke B, McHardy AC, Meyer F, Mockel B, Pfefferle W, Puhler A, Rey DA, Ruckert C, Rupp O, Sahm H, Wendisch VF, Wiegrabe I, Tauch A., J. Biotechnol. 104(1-3), 2003
PMID: 12948626
Comparative 13C metabolic flux analysis of pyruvate dehydrogenase complex-deficient, L-valine-producing Corynebacterium glutamicum.
Bartek T, Blombach B, Lang S, Eikmanns BJ, Wiechert W, Oldiges M, Noh K, Noack S., Appl. Environ. Microbiol. 77(18), 2011
PMID: 21784914
Carbon flux analysis by 13C nuclear magnetic resonance to determine the effect of CO2 on anaerobic succinate production by Corynebacterium glutamicum.
Rados D, Turner DL, Fonseca LL, Carvalho AL, Blombach B, Eikmanns BJ, Neves AR, Santos H., Appl. Environ. Microbiol. 80(10), 2014
PMID: 24610842
Functional analysis of all aminotransferase proteins inferred from the genome sequence of Corynebacterium glutamicum.
Marienhagen J, Kennerknecht N, Sahm H, Eggeling L., J. Bacteriol. 187(22), 2005
PMID: 16267288
Menaquinol oxidase activity and primary structure of cytochrome bd from the amino-acid fermenting bacterium Corynebacterium glutamicum.
Kusumoto K, Sakiyama M, Sakamoto J, Noguchi S, Sone N., Arch. Microbiol. 173(5-6), 2000
PMID: 10896219
The respiratory chain of Corynebacterium glutamicum.
Bott M, Niebisch A., J. Biotechnol. 104(1-3), 2003
PMID: 12948635
Respiratory energy metabolism
Bott M., Niebisch A.., 2005
CoryneRegNet 6.0--Updated database content, new analysis methods and novel features focusing on community demands.
Pauling J, Rottger R, Tauch A, Azevedo V, Baumbach J., Nucleic Acids Res. 40(Database issue), 2011
PMID: 22080556
The COG database: a tool for genome-scale analysis of protein functions and evolution.
Tatusov RL, Galperin MY, Natale DA, Koonin EV., Nucleic Acids Res. 28(1), 2000
PMID: 10592175
GenDB--an open source genome annotation system for prokaryote genomes.
Meyer F, Goesmann A, McHardy AC, Bartels D, Bekel T, Clausen J, Kalinowski J, Linke B, Rupp O, Giegerich R, Puhler A., Nucleic Acids Res. 31(8), 2003
PMID: 12682369
Ribosomal RNA and ribosomal proteins in corynebacteria.
Martin JF, Barreiro C, Gonzalez-Lavado E, Barriuso M., J. Biotechnol. 104(1-3), 2003
PMID: 12948628
Comprehensive analysis of the Corynebacterium glutamicum transcriptome using an improved RNAseq technique.
Pfeifer-Sancar K, Mentz A, Ruckert C, Kalinowski J., BMC Genomics 14(), 2013
PMID: 24341750
Group 2 sigma factor SigB of Corynebacterium glutamicum positively regulates glucose metabolism under conditions of oxygen deprivation.
Ehira S, Shirai T, Teramoto H, Inui M, Yukawa H., Appl. Environ. Microbiol. 74(16), 2008
PMID: 18567683
Elucidation of genes relevant to the microaerobic growth of Corynebacterium glutamicum.
Ikeda M, Baba M, Tsukamoto N, Komatsu T, Mitsuhashi S, Takeno S., Biosci. Biotechnol. Biochem. 73(12), 2009
PMID: 19966452
Role of cytochrome bd oxidase from Corynebacterium glutamicum in growth and lysine production.
Kabus A, Niebisch A, Bott M., Appl. Environ. Microbiol. 73(3), 2006
PMID: 17142369
RamB, a novel transcriptional regulator of genes involved in acetate metabolism of Corynebacterium glutamicum.
Gerstmeir R, Cramer A, Dangel P, Schaffer S, Eikmanns BJ., J. Bacteriol. 186(9), 2004
PMID: 15090522
Bacterial redox sensors.
Green J, Paget MS., Nat. Rev. Microbiol. 2(12), 2004
PMID: 15550941
Physiological roles of sigma factor SigD in Corynebacterium glutamicum.
Taniguchi H, Busche T, Patschkowski T, Niehaus K, Patek M, Kalinowski J, Wendisch VF., BMC Microbiol. 17(1), 2017
PMID: 28701150
Enzymatic assembly of DNA molecules up to several hundred kilobases.
Gibson DG, Young L, Chuang RY, Venter JC, Hutchison CA 3rd, Smith HO., Nat. Methods 6(5), 2009
PMID: 19363495
Enzymatic assembly of overlapping DNA fragments.
Gibson DG., Meth. Enzymol. 498(), 2011
PMID: 21601685
Primer-directed enzymatic amplification of DNA with a thermostable DNA polymerase.
Saiki RK, Gelfand DH, Stoffel S, Scharf SJ, Higuchi R, Horn GT, Mullis KB, Erlich HA., Science 239(4839), 1988
PMID: 2448875
Specific synthesis of DNA in vitro via a polymerase-catalyzed chain reaction.
Mullis KB, Faloona FA., Meth. Enzymol. 155(), 1987
PMID: 3431465
High efficiency transformation of E. coli by high voltage electroporation.
Dower WJ, Miller JF, Ragsdale CW., Nucleic Acids Res. 16(13), 1988
PMID: 3041370
Efficient electrotransformation of corynebacterium diphtheriae with a mini-replicon derived from the Corynebacterium glutamicum plasmid pGA1.
Tauch A, Kirchner O, Loffler B, Gotker S, Puhler A, Kalinowski J., Curr. Microbiol. 45(5), 2002
PMID: 12232668
High efficiency electroporation of intact Corynebacterium glutamicum cells.
Liebl W, Bayerl A, Schein B, Stillner U, Schleifer KH., FEMS Microbiol. Lett. 53(3), 1989
PMID: 2612892
Experiments
Eggeling L., Reyes O.., 2005
Studies on transformation of Escherichia coli with plasmids.
Hanahan D., J. Mol. Biol. 166(4), 1983
PMID: 6345791
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