Global transcriptomic analysis of an engineered Escherichia coli strain lacking the phosphoenolpyruvate: Carbohydrate phosphotransferase system during shikimic acid production in rich culture medium

Microbial Cell Factories

Volumn 13, Issue 1, 2014, Pages

  Cortés Tolalpa, Larisa ^a   Gutiérrez Ríos, Rosa María ^a   Martínez, Luz María ^a   De Anda, Ramón ^a   Gosset, Guillermo ^a   Bolívar, Francisco ^a   Escalante, Adelfo ^a  

^a INSTITUTO DE BIOTECNOLOGÍA   (Mexico)

Author keywords

Batch fermentor culture; Complex fermentation broth; Escherichia coli PTS strain; Global transcriptomic analysis; Microarrays; Regulatory network; Shikimic acid production

Indexed keywords

AROMATIC AMINO ACID; CARBOHYDRATE PHOSPHOTRANSFERASE; GLUCOSE; IRON; NUCLEOSIDE; NUCLEOTIDE; PHOSPHOENOLPYRUVATE; PHOSPHOTRANSFERASE; SHIKIMIC ACID; SUGAR; SULFUR; TRYPTOPHAN; UNCLASSIFIED DRUG;

ACIDITY; ARTICLE; BACTERIAL GROWTH; BACTERIAL STRAIN; BACTERIUM CULTURE; BATCH FERMENTATION; BATCH REACTOR; BIOSYNTHESIS; CARBON METABOLISM; CATABOLISM; CULTURE MEDIUM; ESCHERICHIA COLI; GENE CONTROL; GENETIC ENGINEERING; GROWTH CURVE; IRON TRANSPORT; NONHUMAN; SUPERNATANT; TRANSCRIPTOMICS; UPREGULATION;

ESCHERICHIA COLI;

AMINO ACIDS; BATCH CELL CULTURE TECHNIQUES; CULTURE MEDIA; ESCHERICHIA COLI; ESCHERICHIA COLI PROTEINS; GENE EXPRESSION PROFILING; GENE REGULATORY NETWORKS; GENETIC ENGINEERING; PHOSPHOENOLPYRUVATE; PHOSPHOENOLPYRUVATE SUGAR PHOSPHOTRANSFERASE SYSTEM; SHIKIMIC ACID; UP-REGULATION;

EID: 84898599172     PISSN: None     EISSN: 14752859     Source Type: Journal    
DOI: 10.1186/1475-2859-13-28     Document Type: Article

References (82)

1. Herrmann KM, Weaver LM: The shikimate pathway. Annu Rev Plant Physiol Plant Mol Biol 1999, 50:473-503.
2. Richards TA, Dacks JB, Campbell SA, Blanchard JL, Foster PG, McLeod R, Roberts CW: Evolutionary origins of the eukaryotic shikimate pathway: gene fusions, horizontal gene transfer, and endosymbiotic replacements. Eukaryot Cell 2006, 5:1517-1531.
3. Krämer M, Bongaerts J, Bovenberg R, Kremer S, Müller U, Orf S, Wubbolts M, Raeven L: Metabolic engineering for microbial production of shikimic acid. Metab Eng 2003, 5:277-283.
4. Ghosh S, Chisti Y, Banerjee UC: Production of shikimic acid. Biotechnol Adv 2012, 30:1425-1431.
5. Tripathi P, Rawat G, Yadav S, Saxena RK: Fermentative production of shikimic acid: a paradigm shift of production concept from plant route to microbial route. Bioprocess Biosyst Eng 2013, 11:1665-1673.
6. Abbott A: Avian flu special: what's in the medicine cabinet? Nature 2005, 435:407-409
7. Luo M: Structural biology: antiviral drugs fit for a purpose. Nature 2006, 443:37-38.
8. Chandran SS, Yi J, Draths KM, von Daeniken R, Weber W, Frost JW: Phosphoenolpyruvate availability and the biosynthesis of shikimic acid. Biotechnol Prog 2003, 19:808-814.
9. Johansson L, Lindskog A, Silfversparre G, Cimander C, Nielsen KF, Lidén G: Shikimic acid production by a modified strain of E. coli (W3110.shik1) under phosphate-limited and carbon-limited conditions. Biotechnol Bioeng 2005, 92:541-552.
10. Escalante A, Calderón R, Valdivia A, De AR, Hernández G, Ramírez OT, Gosset G, Bolívar F: Metabolic engineering for the production of shikimic acid in an evolved Escherichia coli strain lacking the phosphoenolpyruvate: carbohydrate phosphotransferase system. Microb Cell Factories 2010, 9:21.
11. Chen K, Dou J, Tang S, Yang Y, Wang H, Fang H, Zhou C: Deletion of the aroK gene is essential for high shikimic acid accumulation through the shikimate pathway in E. coli. Bioresour Technol 2012, 119:141-147.
12. Rodriguez A, Martínez JA, Báez-Viveros JL, Flores N, Hernández-Chávez G, Ramírez OT, Gosset G, Bolivar F: Constitutive expression of selected genes from the pentose phosphate and aromatic pathways increases the shikimic acid yield in high-glucose batch cultures of an Escherichia coli strain lacking PTS and pykF. Microb Cell Factories 2013, 12:86.
13. Cui Y-Y, Ling C, Zhang Y-Y, Huang J, Liu J-Z: Production of shikimic acid from Escherichia coli through chemically inducible chromosomal evolution and cofactor metabolic engineering. Microb Cell Factories 2014, 13:21.
14. Johansson L, Lidén G: Transcriptome analysis of a shikimic acid producing strain of Escherichia coli W3110 grown under carbon- and phosphate-limited conditions. J Biotechnol 2006, 126:528-545.
15. Breitling R, Armengaud P, Amtmann A, Herzyk P: Rank products: a simple, yet powerful, new method to detect differentially regulated genes in replicated microarray experiments. FEBS Lett 2004, 573:83-92.
16. Hong F, Breitling R: A comparison of meta-analysis methods for detecting differentially expressed genes in microarray experiments. Bioinformatics 2008, 24:374-382.
17. Keseler IM, Mackie A, Peralta-Gil M, Santos-Zavaleta A, Gama-Castro S, Bonavides-Martínez C, Fulcher C, Huerta AM, Kothari A, Krummenacker M, Latendresse M, Muñiz-Rascado L, Ong Q, Paley S, Schröder I, Shearer AG, Subhraveti P, Travers M, Weerasinghe D, Weiss V, Collado-Vides J, Gunsalus RP, Paulsen I, Karp PD: EcoCyc: fusing model organism databases with systems biology. Nucleic Acids Res 2013, 41(Database issue):D605-D612.
18. Flores N, Flores S, Escalante A, de Anda R, Leal L, Malpica R, Georgellis D, Gosset G, Bolívar F: Adaptation for fast growth on glucose by differential expression of central carbon metabolism and gal regulon genes in an Escherichia coli strain lacking the phosphoenolpyruvate: carbohydrate phosphotransferase system. Metab Eng 2005, 7:70-87.
19. Báez-Viveros J, Flores N, Juárez K, Castillo-España P, Bolivar F, Gosset G: Metabolic transcription analysis of engineered Escherichia coli strains that overproduce L-phenylalanine. Microb Cell Factories 2007, 6:30.
20. Ferenci T: Hungry bacteria-definition and properties of a nutritional state. Environ Microbiol 2001, 3:605-611.
21. Bordignon E, Grote M, Schneider E: The maltose ATP-binding cassette transporter in the 21st century - towards a structural dynamic perspective on its mode of action: maltose ABC transporter in the 21st century. Mol Microbiol 2010, 77:1354-1366.
22. Yamashita S, Buchanan SK: Module 3.3.1. Solute and ion transport: outer membrane pores and receptors. In Escherichia Coli Salmonella Cell Mol Biol. Edited by Böck A, Curtiss R III, Kaper J, Karp PD, Neidhardt F, Nystrom T, Squires C, Ussery D. Washington, DC: ASM Press; 2010.
23. Zhang H-K, Lu H, Wang J, Liu G-F, Zhou J-T, Xu M-Y: Global transcriptome analysis of Escherichia coli exposed to immobilized anthraquinone-2-sulfonate and azo dye under anaerobic conditions. Appl Microbiol Biotechnol 2013, 97:6895-6905.
24. Lemieux MJ, Huang Y, Wang D-N: Glycerol-3-phosphate transporter of Escherichia coli: structure, function and regulation. Res Microbiol 2004, 155:623-629.
25. Yanofsky C, Horn V, Gollnick P: Physiological studies of tryptophan transport and tryptophanase operon induction in Escherichia coli. J Bacteriol 1991, 173:6009-6017.
26. Payne JW, Morley JS, Armitage P, Payne GM: Transport and hydrolysis of antibacterial peptide analogues in Escherichia coli: backbone-modified aminoxy peptides. J Gen Microbiol 1984, 130:2253-2265.
27. Olson ER, Dunyak DS, Jurss LM, Poorman RA: Identification and characterization of dppA, an Escherichia coli gene encoding a periplasmic dipeptide transport protein. J Bacteriol 1991, 173:234-244.
28. Guyer CA, Morgan DG, Staros JV: Binding specificity of the periplasmic oligopeptide-binding protein from Escherichia coli. J Bacteriol 1986, 168:775-779.
29. Goodell EW, Higgins CF: Uptake of cell wall peptides by Salmonella typhimurium and Escherichia coli. J Bacteriol 1987, 169:3861-3865.
30. Hiles ID, Gallagher MP, Jamieson DJ, Higgins CF: Molecular characterization of the oligopeptide permease of Salmonella typhimurium. J Mol Biol 1987, 195:125-142.
31. Angelopoulos N, Kallaras C, Apostolakis M: Effects of intracerebroventricular administration of atrial natriuretic peptide on subcortical EEG activity in conscious rabbits. Exp Brain Res Exp Hirnforsch Expérimentation Cérébrale 1996, 108:427-432.
32. Lucht JM, Bremer E: Adaptation of Escherichia coli to high osmolarity environments: osmoregulation of the high-affinity glycine betaine transport system proU. FEMS Microbiol Rev 1994, 14:3-20.
33. Verheul A, Wouters JA, Rombouts FM, Abee T: A possible role of ProP, ProU and CaiT in osmoprotection of Escherichia coli by carnitine. J Appl Microbiol 1998, 85:1036-1046.
34. Lamark T, Styrvold OB, Strøm AR: Efflux of choline and glycine betaine from osmoregulating cells of Escherichia coli. FEMS Microbiol Lett 1992, 75:149-154.
35. Moreau PL: The lysine decarboxylase CadA protects Escherichia coli starved of phosphate against fermentation acids. J Bacteriol 2007, 189:2249-2261.
36. Zimbro MJ, Power DA: Difco & BBL Manual: Manual of Microbiological Culture Media. Sparks, MD: Becton Dickinson and Co.; 2009.
37. Kredich NM, Tomkins GM: The enzymic synthesis of L-cysteine in Escherichia coli and Salmonella typhimurium. J Biol Chem 1966, 241:4955-4965.
38. Fimmel AL, Loughlin RE: Isolation and characterization of cysK mutants of Escherichia coli K12. J Gen Microbiol 1977, 103:37-43.
39. Boronat A, Britton P, Jones-Mortimer MC, Kornberg HL, Lee LG, Murfitt D, Parra F: Location on the Escherichia coli genome of a gene specifying O-acetylserine (Thiol)-lyase. J Gen Microbiol 1984, 130:673-685.
40. Flint DH, Tuminello JF, Miller TJ: Studies on the synthesis of the Fe-S cluster of dihydroxy-acid dehydratase in Escherichia coli crude extract isolation of O-acetylserine sulfhydrylases A and B and β-cystathionase based on their ability to mobilize sulfur from cysteine and to participate in Fe-S cluster synthesis. J Biol Chem 1996, 271:16053-16067.
41. Stauffer GV: Biosynthesis of serine, glycine, and one-carbon units. In Escherichia coli Salmonella Cell Mol Biol. 2nd edition. Edited by Neidhardt F. Washington, DC: ASM Press; 2005:506-513.
42. Okamura-Ikeda K, Ohmura Y, Fujiwara K, Motokawa Y: Cloning and nucleotide sequence of the gcv operon encoding the Escherichia coli glycine-cleavage system. Eur J Biochem 1993, 216:539-548.
43. Ghrist AC, Stauffer GV: The Escherichia coli glycine transport system and its role in the regulation of the glycine cleavage enzyme system. Microbiology 1995, 141:133-140.
44. Thoden JB, Raushel FM, Benning MM, Rayment I, Holden HM: The structure of carbamoyl phosphate synthetase determined to 2.1 Å resolution. Acta Crystallogr D Biol Crystallogr 1999, 55:8-24.
45. Salgado H, Peralta-Gil M, Gama-Castro S, Santos-Zavaleta A, Muniz-Rascado L, Garcia-Sotelo JS, Weiss V, Solano-Lira H, Martinez-Flores I, Medina-Rivera A, Salgado-Osorio G, Alquicira-Hernandez S, Alquicira-Hernandez K, Lopez-Fuentes A, Porron-Sotelo L, Huerta AM, Bonavides-Martinez C, Balderas-Martinez YI, Pannier L, Olvera M, Labastida A, Jimenez-Jacinto V, Vega-Alvarado L, del Moral-Chavez V, Hernandez-Alvarez A, Morett E, Collado-Vides J: RegulonDB v8.0: omics data sets, evolutionary conservation, regulatory phrases, cross-validated gold standards and more. Nucleic Acids Res 2012, 41:D203-D213.
46. Dailey FE, Cronan JE: Acetohydroxy acid synthase I, a required enzyme for isoleucine and valine biosynthesis in Escherichia coli K-12 during growth on acetate as the sole carbon source. J Bacteriol 1986, 165:453-460.
47. McFalland E, Newman E: Amino acids as carbon sources. In Escherichia coli Salmonella Cell Mol Biol. 2nd edition. Edited by Neidhardt F. Washington, DC: ASM Press; 2005:358-379.
48. Cunin R, Glansdorff N, Piérard A, Stalon V: Biosynthesis and metabolism of arginine in bacteria. Microbiol Rev 1986, 50:314-352.
49. Igarashi K, Kashiwagi K: Polyamine transport in bacteria and yeast. Biochem J 1999, 344:633-642.
50. Vassylyev DG: Crystal structure and mutational analysis of the Escherichia coli putrescine receptor. structural basis for substrate specificity. J Biol Chem 1998, 273:17604-17609.
51. Sigala JC, Flores S, Flores N, Aguilar C, de Anda R, Gosset G, Bol&ívar F: Acetate metabolism in Escherichia coli strains lacking phosphoenolpyruvate: carbohydrate phosphotransferase system; evidence of carbon recycling strategies and futile cycles. J Mol Microbiol Biotechnol 2009, 16:224-235.
52. Stancik LM, Stancik DM, Schmidt B, Barnhart DM, Yoncheva YN, Slonczewski JL: pH-Dependent expression of periplasmic proteins and amino acid catabolism in Escherichia coli. J Bacteriol 2002, 184:4246-4258.
53. Padan E, Bibi E, Ito M, Krulwich TA: Alkaline pH homeostasis in bacteria: new insights. Biochim Biophys Acta BBA - Biomembr 2005, 1717:67-88.
54. Tucker DL, Tucker N, Conway T: Gene expression profiling of the pH response in Escherichia coli. J Bacteriol 2002, 184:6551-6558.
55. Maurer LM, Yohannes E, Bondurant SS, Radmacher M, Slonczewski JL: pH regulates genes for flagellar motility, catabolism, and oxidative stress in Escherichia coli K-12. J Bacteriol 2004, 187:304-319.
56. Masuda N, Church GM: Regulatory network of acid resistance genes in Escherichia coli. Mol Microbiol 2003, 48:699-712.
57. Zhao B, Houry WA: Acid stress response in enteropathogenic gammaproteobacteria: an aptitude for survival. Biochem Cell Biol 2010, 88:301-314.
58. Kern R, Malki A, Abdallah J, Tagourti J, Richarme G: Escherichia coli HdeB is an acid stress chaperone. J Bacteriol 2006, 189:603-610.
59. Hommais F: GadE (YhiE): a novel activator involved in the response to acid environment in Escherichia coli. Microbiology 2004, 150:61-72.
60. Castanie-Cornet M-P, Penfound TA, Smith D, Elliott JF, Foster JW: Control of acid resistance in Escherichia coli. J Bacteriol 1999, 181:3525-3535.
61. Härle C, Kim I, Angerer A, Braun V: Signal transfer through three compartments: transcription initiation of the Escherichia coli ferric citrate transport system from the cell surface. EMBO J 1995, 14:1430.
62. Griggs DW, Tharp BB, Konisky J: Cloning and promoter identification of the iron-regulated cir gene of Escherichia coli. J Bacteriol 1987, 169:5343-5352.
63. Sirko A, Zatyka M, Sadowy E, Hulanicka D: Sulfate and thiosulfate transport in Escherichia coli K-12: evidence for a functional overlapping of sulfate- and thiosulfate-binding proteins. J Bacteriol 1995, 177:4134-4136.
64. Earhart CF: Uptake and metabolism of iron and molybdenum. In Escherichia coli Salmonella Cell Mol Biol. Volume 1. 2nd edition. Edited by Neidhardt F. Washington, DC: ASM Press; 2005:1075-1090.
65. Enz S, Mahren S, Stroeher UH, Braun V: Surface signaling in ferric citrate transport gene induction: interaction of the FecA, FecR, and FecI regulatory proteins. J Bacteriol 2000, 182:637-646.
66. Maier C, Bremer E, Schmid A, Benz R: Pore-forming activity of the Tsx protein from the outer membrane of Escherichia coli. Demonstration of a nucleoside-specific binding site. J Biol Chem 1988, 263:2493-2499.
67. Zalkin H, Nygaard P: Biosynthesis of purine nucleotides. In Escherichia coli Salmonella Cell Mol Biol. Volume 1. 2nd edition. Edited by Neidhardt F. Washington, DC: ASM Press; 2005:561-579.
68. Breazeale SD, Ribeiro AA, Raetz CRH: Oxidative decarboxylation of UDPglucuronic acid in extracts of polymyxin-resistant Escherichia coli originof lipid a species modified with 4-amino-4-deoxy-l-arabinose. J Biol Chem 2002, 277:2886-2896.
69. Weber A, Kögl SA, Jung K: Time-dependent proteome alterations under osmotic stress during aerobic and anaerobic growth in Escherichia coli. J Bacteriol 2006, 188:7165-7175.
70. Stenberg F, Chovanec P, Maslen SL, Robinson CV, Ilag LL, von Heijne G, Daley DO: Protein complexes of the Escherichia coli cell envelope. J Biol Chem 2005, 280:34409-34419.
71. Mates AK, Sayed AK, Foster JW: Products of the Escherichia coli acid fitness island attenuate metabolite stress at extremely low pH and mediate a cell density-dependent acid resistance. J Bacteriol 2007, 189:2759-2768.
72. Pratt LA, Hsing W, Gibson KE, Silhavy TJ: From acids to osmZ: multiple factors influence synthesis of the OmpF and OmpC porins in Escherichia coli. Mol Microbiol 1996, 20:911-917.
73. Batchelor E, Walthers D, Kenney LJ, Goulian M: The Escherichia coli CpxA-CpxR envelope stress response system regulates expression of the porins OmpF and OmpC. J Bacteriol 2005, 187:5723-5731.
74. Minty JJ, Lesnefsky AA, Lin F, Chen Y, Zaroff TA, Veloso AB, Xie B, McConnell CA, Ward RJ, Schwartz DR: Evolution combined with genomic study elucidates genetic bases of isobutanol tolerance in Escherichia coli. Microb Cell Fact 2011, 10:18.
75. Macia{ogonek}g A, Peano C, Pietrelli A, Egli T, Bellis GD, Landini P: In vitro transcription profiling of the σS subunit of bacterial RNA polymerase: re-definition of the σS regulon and identification of σS-specific promoter sequence elements. Nucleic Acids Res 2011, 39:5338-5355.
76. Weber H, Polen T, Heuveling J, Wendisch VF, Hengge R: Genome-wide analysis of the general stress response network in Escherichia coli: σSdependent genes, promoters, and sigma factor selectivity. J Bacteriol 2005, 187:1591-1603.
77. Flores N, Escalante A, de Anda R, B&áez-Viveros JL, Merino E, Franco B, Georgellis D, Gosset G, Bol&ívar F: New insights into the role of sigma factor RpoS as revealed in Escherichia coli strains lacking the phosphoenolpyruvate: carbohydrate phosphotransferase system. J Mol Microbiol Biotechnol 2008, 14:176-192.
78. Olvera L, Mendoza-Vargas A, Flores N, Olvera M, Sigala JC, Gosset G, Morett E, Bolívar F: Transcription analysis of central metabolism genes in Escherichia coli. Possible roles of σ38 in their expression, as a response to carbon limitation. PLoS ONE 2009, 4:e7466.
79. Aguilar C, Escalante A, Flores N, de Anda R, Riveros-McKay F, Gosset G, Morett E, Bolívar F: Genetic changes during a laboratory adaptive evolution process that allowed fast growth in glucose to an Escherichia coli strain lacking the major glucose transport system. BMC Genomics 2012, 13:385.
80. Weissbach A, Hurwitz J: The formation of 2-Keto-3-deoxyheptonic acid in extracts of Escherichia coli B. J Biol Chem 1959, 234:705-709.
81. Báez JL, Bolívar F, Gosset G: Determination of 3-deoxy-D-arabino-heptulosonate 7-phosphate productivity and yield from glucose in Escherichia coli devoid of the glucose phosphotransferase transport system. Biotechnol Bioeng 2001, 73:530-535.
82. Muñoz AJ, Hernández-Chávez G, de Anda R, Martínez A, Bolívar F, Gosset G: Metabolic engineering of Escherichia coli for improving L-3,4-dihydroxyphenylalanine (L-DOPA) synthesis from glucose. J Ind Microbiol Biotechnol 2011, 38:1845-1852.