Gene expression analysis of Corynebacterium glutamicum subjected to long-term lactic acid adaptation

Jakob K, Satorhelyi P, Lange C, Wendisch VF, Silakowski B, Scherer S, Neuhaus K (2007)
Journal of Bacteriology 189(15): 5582-5590.

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Zeitschriftenaufsatz | Veröffentlicht | Englisch
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Abstract / Bemerkung
Corynebacteria form an important part of the red smear cheese microbial surface consortium. To gain a better understanding of molecular adaptation due to low pH induced by lactose fermentation, the global gene expression profile of Corynebacterium glutamicum adapted to pH 5.7 with lactic acid under continuous growth in a chemostat was characterized by DNA microarray analysis. Expression of a total of 116 genes was increased and that of 90 genes was decreased compared to pH 7.5 without lactic acid, representing 7% of the genes in the genome. The up-regulated genes encode mainly transcriptional regulators, proteins responsible for export, import, and metabolism, and several proteins of unknown function. As much as 45% of the up-regulated open reading frames code for hypothetical proteins. These results were validated using real-time reverse transcription-PCR. To characterize the functions of 38 up-regulated genes, 36 single-crossover disruption mutants were generated and analyzed for their lactic acid sensitivities. However, only a sigB knockout mutant showed a highly significant negative effect on growth at low pH, suggesting a function in organic-acid adaptation. A sigE mutant already displayed growth retardation at neutral pH but grew better at acidic pH than the sigB mutant. The lack of acid-sensitive phenotypes in 34 out of 36 disrupted genes suggests either a considerable redundancy in acid adaptation response or coincidental effects. Other up-regulated genes included genes for ion transporters and metabolic pathways, including carbohydrate and respiratory metabolism. The enhanced expression of the nrd (ribonucleotide reductase) operon and a DNA ATPase repair protein implies a cellular response to combat acid-induced DNA damage. Surprisingly, multiple iron uptake systems (totaling 15% of the genes induced >= 2-fold) were induced at low pH. This induction was shown to be coincidental and could be attributed to iron-sequestering effects in complex media at low pH.
Erscheinungsjahr
Zeitschriftentitel
Journal of Bacteriology
Band
189
Ausgabe
15
Seite(n)
5582-5590
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PUB-ID

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Jakob K, Satorhelyi P, Lange C, et al. Gene expression analysis of Corynebacterium glutamicum subjected to long-term lactic acid adaptation. Journal of Bacteriology. 2007;189(15):5582-5590.
Jakob, K., Satorhelyi, P., Lange, C., Wendisch, V. F., Silakowski, B., Scherer, S., & Neuhaus, K. (2007). Gene expression analysis of Corynebacterium glutamicum subjected to long-term lactic acid adaptation. Journal of Bacteriology, 189(15), 5582-5590. doi:10.1128/Jb.00082-07
Jakob, K., Satorhelyi, P., Lange, C., Wendisch, V. F., Silakowski, B., Scherer, S., and Neuhaus, K. (2007). Gene expression analysis of Corynebacterium glutamicum subjected to long-term lactic acid adaptation. Journal of Bacteriology 189, 5582-5590.
Jakob, K., et al., 2007. Gene expression analysis of Corynebacterium glutamicum subjected to long-term lactic acid adaptation. Journal of Bacteriology, 189(15), p 5582-5590.
K. Jakob, et al., “Gene expression analysis of Corynebacterium glutamicum subjected to long-term lactic acid adaptation”, Journal of Bacteriology, vol. 189, 2007, pp. 5582-5590.
Jakob, K., Satorhelyi, P., Lange, C., Wendisch, V.F., Silakowski, B., Scherer, S., Neuhaus, K.: Gene expression analysis of Corynebacterium glutamicum subjected to long-term lactic acid adaptation. Journal of Bacteriology. 189, 5582-5590 (2007).
Jakob, K., Satorhelyi, P., Lange, C., Wendisch, Volker F., Silakowski, B., Scherer, S., and Neuhaus, K. “Gene expression analysis of Corynebacterium glutamicum subjected to long-term lactic acid adaptation”. Journal of Bacteriology 189.15 (2007): 5582-5590.

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Daten bereitgestellt von Europe PubMed Central.

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Wang X, Peng F, Dong G, Sun Y, Dai X, Yang Y, Liu X, Bai Z., FEMS Microbiol Lett 365(8), 2018
PMID: 29420726
Activity of a Holin-Endolysin System in the Insecticidal Pathogenicity Island of Yersinia enterocolitica.
Springer K, Reuter S, Knüpfer M, Schmauder L, Sänger PA, Felsl A, Fuchs TM., J Bacteriol 200(16), 2018
PMID: 29866807
Efficient Production of the Dicarboxylic Acid Glutarate by Corynebacterium glutamicum via a Novel Synthetic Pathway.
Pérez-García F, Jorge JMP, Dreyszas A, Risse JM, Wendisch VF., Front Microbiol 9(), 2018
PMID: 30425699
Bacterial Physiological Adaptations to Contrasting Edaphic Conditions Identified Using Landscape Scale Metagenomics.
Malik AA, Thomson BC, Whiteley AS, Bailey M, Griffiths RI., MBio 8(4), 2017
PMID: 28679747
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
Corynebacterium glutamicum Metabolic Engineering with CRISPR Interference (CRISPRi).
Cleto S, Jensen JV, Wendisch VF, Lu TK., ACS Synth Biol 5(5), 2016
PMID: 26829286
Anaerobic growth of Corynebacterium glutamicum via mixed-acid fermentation.
Michel A, Koch-Koerfges A, Krumbach K, Brocker M, Bott M., Appl Environ Microbiol 81(21), 2015
PMID: 26276118
Metabolic engineering of Corynebacterium glutamicum for glycolate production.
Zahoor A, Otten A, Wendisch VF., J Biotechnol 192 Pt B(), 2014
PMID: 24486442
σ(ECF) factors of gram-positive bacteria: a focus on Bacillus subtilis and the CMNR group.
Souza BM, Castro TL, Carvalho RD, Seyffert N, Silva A, Miyoshi A, Azevedo V., Virulence 5(5), 2014
PMID: 24921931
Evolutionary potential, cross-stress behavior and the genetic basis of acquired stress resistance in Escherichia coli.
Dragosits M, Mozhayskiy V, Quinones-Soto S, Park J, Tagkopoulos I., Mol Syst Biol 9(), 2013
PMID: 23385483
The Response of Enterococcus faecalis V583 to Chloramphenicol Treatment.
Aakra A, Vebø H, Indahl U, Snipen L, Gjerstad O, Lunde M, Nes IF., Int J Microbiol 2010(), 2010
PMID: 20628561
Maturing dynamics of surface microflora in Fontina PDO cheese studied by culture-dependent and -independent methods.
Dolci P, Barmaz A, Zenato S, Pramotton R, Alessandria V, Cocolin L, Rantsiou K, Ambrosoli R., J Appl Microbiol 106(1), 2009
PMID: 19054234
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, Krämer R, Trötschel C, Poetsch A, Rückert C, Hüser A, Persicke M, Seiferling D, Kalinowski J, Marin K., BMC Genomics 10(), 2009
PMID: 20025733

53 References

Daten bereitgestellt von Europe PubMed Central.

Acid stress responses in enterobacteria.
Bearson S, Bearson B, Foster JW., FEMS Microbiol. Lett. 147(2), 1997
PMID: 9119190
Bioenergetic mechanism for nisin resistance, induced by the acid tolerance response of Listeria monocytogenes.
Bonnet M, Rafi MM, Chikindas ML, Montville TJ., Appl. Environ. Microbiol. 72(4), 2006
PMID: 16597957
Regulation of cytoplasmic pH in bacteria.
Booth IR., Microbiol. Rev. 49(4), 1985
PMID: 3912654

AUTHOR UNKNOWN, 2004
Transcriptional analysis of long-term adaptation of Yersinia enterocolitica to low-temperature growth.
Bresolin G, Neuhaus K, Scherer S, Fuchs TM., J. Bacteriol. 188(8), 2006
PMID: 16585756
Acid stress in the food pathogen Bacillus cereus.
Browne N, Dowds BC., J. Appl. Microbiol. 92(3), 2002
PMID: 11872115
Surviving the acid test: responses of gram-positive bacteria to low pH.
Cotter PD, Hill C., Microbiol. Mol. Biol. Rev. 67(3), 2003
PMID: 12966143
pH regulation by Streptococcus mutans.
Dashper SG, Reynolds EC., J. Dent. Res. 71(5), 1992
PMID: 1607433
The UV-B stimulon of the terrestrial cyanobacterium Nostoc commune comprises early shock proteins and late acclimation proteins.
Ehling-Schulz M, Schulz S, Wait R, Gorg A, Scherer S., Mol. Microbiol. 46(3), 2002
PMID: 12410839
Role of Listeria monocytogenes sigma(B) in survival of lethal acidic conditions and in the acquired acid tolerance response.
Ferreira A, Sue D, O'Byrne CP, Boor KJ., Appl. Environ. Microbiol. 69(5), 2003
PMID: 12732538
Escherichia coli acid resistance: tales of an amateur acidophile.
Foster JW., Nat. Rev. Microbiol. 2(11), 2004
PMID: 15494746

AUTHOR UNKNOWN, 2000
Identification of proteins induced at low pH in Lactococcus lactis.
Frees D, Vogensen FK, Ingmer H., Int. J. Food Microbiol. 87(3), 2003
PMID: 14527802
Induction of an AP endonuclease activity in Streptococcus mutans during growth at low pH.
Hahn K, Faustoferri RC, Quivey RG Jr., Mol. Microbiol. 31(5), 1999
PMID: 10200967
The Brevibacterium flavum sigma factor SigB has a role in the environmental stress response.
Halgasova N, Bukovska G, Ugorcakova J, Timko J, Kormanec J., FEMS Microbiol. Lett. 216(1), 2002
PMID: 12423756
uvrA is an acid-inducible gene involved in the adaptive response to low pH in Streptococcus mutans.
Hanna MN, Ferguson RJ, Li YH, Cvitkovitch DG., J. Bacteriol. 183(20), 2001
PMID: 11566996

AUTHOR UNKNOWN, 2000
General stress response of Bacillus subtilis and other bacteria.
Hecker M, Volker U., Adv. Microb. Physiol. 44(), 2001
PMID: 11407115
Industrial production of amino acids by coryneform bacteria.
Hermann T., J. Biotechnol. 104(1-3), 2003
PMID: 12948636
The phosphate starvation stimulon of Corynebacterium glutamicum determined by DNA microarray analyses.
Ishige T, Krause M, Bott M, Wendisch VF, Sahm H., J. Bacteriol. 185(15), 2003
PMID: 12867461
Changes in protein synthesis and morphology during acid adaptation of Propionibacterium freudenreichii.
Jan G, Leverrier P, Pichereau V, Boyaval P., Appl. Environ. Microbiol. 67(5), 2001
PMID: 11319077
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
Global expression profiling and physiological characterization of Corynebacterium glutamicum grown in the presence of L-valine.
Lange C, Rittmann D, Wendisch VF, Bott M, Sahm H., Appl. Environ. Microbiol. 69(5), 2003
PMID: 12732517
Stress-responsive proteins are upregulated in Streptococcus mutans during acid tolerance.
Len AC, Harty DW, Jacques NA., Microbiology (Reading, Engl.) 150(Pt 5), 2004
PMID: 15133096

AUTHOR UNKNOWN, 1989
Expression, secretion, and processing of staphylococcal nuclease by Corynebacterium glutamicum.
Liebl W, Sinskey AJ, Schleifer KH., J. Bacteriol. 174(6), 1992
PMID: 1548234
Identification of Listeria monocytogenes genes expressed in response to growth at low temperature.
Liu S, Graham JE, Bigelow L, Morse PD 2nd, Wilkinson BJ., Appl. Environ. Microbiol. 68(4), 2002
PMID: 11916687
The Mycobacterium tuberculosis ECF sigma factor sigmaE: role in global gene expression and survival in macrophages.
Manganelli R, Voskuil MI, Schoolnik GK, Smith I., Mol. Microbiol. 41(2), 2001
PMID: 11489128
The promoter of the operon encoding the F0F1 ATPase of Streptococcus pneumoniae is inducible by pH.
Martin-Galiano AJ, Ferrandiz MJ, de la Campa AG., Mol. Microbiol. 41(6), 2001
PMID: 11580837
Transcriptional analysis of the acid tolerance response in Streptococcus pneumoniae.
Martin-Galiano AJ, Overweg K, Ferrandiz MJ, Reuter M, Wells JM, de la Campa AG., Microbiology (Reading, Engl.) 151(Pt 12), 2005
PMID: 16339938
Antibiotic resistance caused by gram-negative multidrug efflux pumps.
Nikaido H., Clin. Infect. Dis. 27 Suppl 1(), 1998
PMID: 9710669
Unravelling the multiple effects of lactic acid stress on Lactobacillus plantarum by transcription profiling.
Pieterse B, Leer RJ, Schuren FH, van der Werf MJ., Microbiology (Reading, Engl.) 151(Pt 12), 2005
PMID: 16339934
DNA microarray analyses of the long-term adaptive response of Escherichia coli to acetate and propionate.
Polen T, Rittmann D, Wendisch VF, Sahm H., Appl. Environ. Microbiol. 69(3), 2003
PMID: 12620868
Genomewide expression analysis in amino acid-producing bacteria using DNA microarrays.
Polen T, Wendisch VF., Appl. Biochem. Biotechnol. 118(1-3), 2004
PMID: 15304751
Periplasmic stress and ECF sigma factors.
Raivio TL, Silhavy TJ., Annu. Rev. Microbiol. 55(), 2001
PMID: 11544368
Validation of array-based gene expression profiles by real-time (kinetic) RT-PCR.
Rajeevan MS, Vernon SD, Taysavang N, Unger ER., J Mol Diagn 3(1), 2001
PMID: 11227069
The alternative sigma factor SigH regulates major components of oxidative and heat stress responses in Mycobacterium tuberculosis.
Raman S, Song T, Puyang X, Bardarov S, Jacobs WR Jr, Husson RN., J. Bacteriol. 183(20), 2001
PMID: 11567012
Acid resistance in Escherichia coli.
Richard HT, Foster JW., Adv. Appl. Microbiol. 52(), 2003
PMID: 12964244
Role of the acid tolerance response in virulence of Salmonella typhimurium.
Wilmes-Riesenberg MR, Bearson B, Foster JW, Curtis R 3rd., Infect. Immun. 64(4), 1996
PMID: 8606063
The Bacillus subtilis genes for ribonucleotide reductase are similar to the genes for the second class I NrdE/NrdF enzymes of Enterobacteriaceae.
Scotti C, Valbuzzi A, Perego M, Galizzi A, Albertini AM., Microbiology (Reading, Engl.) 142 ( Pt 11)(), 1996
PMID: 8969495
Two-component signal transduction.
Stock AM, Robinson VL, Goudreau PN., Annu. Rev. Biochem. 69(), 2000
PMID: 10966457
Stress responses in lactic acid bacteria.
van de Guchte M, Serror P, Chervaux C, Smokvina T, Ehrlich SD, Maguin E., Antonie Van Leeuwenhoek 82(1-4), 2002
PMID: 12369188

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