Systems analysis of methylerythritol-phosphate pathway flux in E. coli: Insights into the role of oxidative stress and the validity of lycopene as an isoprenoid reporter metabolite

Microbial Cell Factories

Volumn 14, Issue 1, 2015, Pages

  Bongers, Mareike ^a   Chrysanthopoulos, Panagiotis K ^a   Behrendorff, James B Y H ^a   Hodson, Mark P ^a   Vickers, Claudia E ^a   Nielsen, Lars K ^a  

^a UNIVERSITY OF QUEENSLAND   (Australia)

Author keywords

Escherichia coli; Isoprenoids; Lycopene; Methylerythritol phosphate pathway; Oxidative stress; ROS; RpoS

Indexed keywords

LYCOPENE; REACTIVE OXYGEN METABOLITE; BACTERIAL PROTEIN; CAROTENOID; ERYTHRITOL; ESCHERICHIA COLI PROTEIN; IRON SULFUR PROTEIN; SIGMA FACTOR; SIGMA FACTOR KATF PROTEIN, BACTERIA; TERPENE;

ALCOHOL METABOLISM; ARTICLE; BACTERIAL STRAIN; BIOACCUMULATION; CONTROLLED STUDY; ESCHERICHIA COLI; GENE INACTIVATION; GENETIC COMPLEMENTATION; GENOMICS; METABOLIC ENGINEERING; METABOLOMICS; METHYLERYTHRITOL PHOSPHATE PATHWAY; NONHUMAN; OXIDATION REDUCTION STATE; OXIDATIVE STRESS; PROTEOMICS; RPOS GENE; SYSTEM ANALYSIS; WILD TYPE; ANALOGS AND DERIVATIVES; CHEMISTRY; DEFICIENCY; GENETICS; HIGH PERFORMANCE LIQUID CHROMATOGRAPHY; METABOLISM; TANDEM MASS SPECTROMETRY;

BACTERIAL PROTEINS; CAROTENOIDS; CHROMATOGRAPHY, HIGH PRESSURE LIQUID; ERYTHRITOL; ESCHERICHIA COLI; ESCHERICHIA COLI PROTEINS; IRON-SULFUR PROTEINS; METABOLIC ENGINEERING; OXIDATIVE STRESS; PROTEOMICS; REACTIVE OXYGEN SPECIES; SIGMA FACTOR; TANDEM MASS SPECTROMETRY; TERPENES;

EID: 84960423472     PISSN: None     EISSN: 14752859     Source Type: Journal    
DOI: 10.1186/s12934-015-0381-7     Document Type: Article

References (79)

1. Vickers C, Behrendorff JYH, Bongers M, Brennan TR, Bruschi M, Nielsen L. Production of industrially relevant isoprenoid compounds in engineered microbes. In: Kamm B, editor. Microorganisms in biorefineries, vol. 26. Berlin Heidelberg: Springer; 2015. p. 303-34 (Microbiology Monographs).
2. Immethun CM, Hoynes-O'Connor AG, Balassy A, Moon TS. Microbial production of isoprenoids enabled by synthetic biology. Front Microbiol. 2013;4:75.
3. Westfall PJ. Production of amorphadiene in yeast, and its conversion to dihydroartemisinic acid, precursor to the antimalarial agent artemisinin. Proc Natl Acad Sci. 2012;109:E111-8.
4. Ajikumar PK, Xiao WH, Tyo KEJ, Wang Y, Simeon F, Leonard E, Mucha O, Phon TH, Pfeifer B, Stephanopoulos G. Isoprenoid pathway optimization for taxol precursor overproduction in Escherichia coli. Science. 2010;330:70-4.
5. Zhou K, Zou R, Stephanopoulos G, Too HP. Metabolite profiling identified methylerythritol cyclodiphosphate efflux as a limiting step in microbial isoprenoid production. PLOS One. 2012;7(11):e47513.
6. Zou R, Zhou K, Stephanopoulos G, Too HP. Combinatorial engineering of 1-deoxy-d-xylulose 5-phosphate pathway using cross-lapping in vitro assembly (CLIVA) Method. PLoS One. 2013;8:e79557.
7. Kim S-W, Keasling JD. Metabolic engineering of the nonmevalonate isopentenyl diphosphate synthesis pathway in Escherichia coli enhances lycopene production. Biotechnol Bioeng. 2001;72:408-15.
8. Boghigian BA, Salas D, Ajikumar PK, Stephanopoulos G, Pfeifer BA. Analysis of heterologous taxadiene production in K- and B-derived Escherichia coli. Appl Microbiol Biotechnol. 2012;93:1651-61.
9. Chae HS, Kim KH, Kim SC, Lee PC. Strain-dependent carotenoid productions in metabolically engineered Escherichia coli. Appl Biochem Biotechnol. 2010;162:2333-44.
10. Willrodt C, David C, Cornelissen S, Buhler B, Julsing MK, Schmid A. Engineering the productivity of recombinant Escherichia coli for limonene formation from glycerol in minimal media. Biotechnol J. 2014;9:1000-12.
11. Wang HH, Isaacs FJ, Carr PA, Sun ZZ, Xu G, Forest CR, Church GM. Programming cells by multiplex genome engineering and accelerated evolution. Nature. 2009;460:894-8.
12. Alper H, Jin YS, Moxley JF, Stephanopoulos G. Identifying gene targets for the metabolic engineering of lycopene biosynthesis in Escherichia coli. Metab Eng. 2005;7:155-64.
13. Alper H, Miyaoku K, Stephanopoulos G. Construction of lycopene-overproducing E. coli strains by combining systematic and combinatorial gene knockout targets. Nat Biotechnol. 2005;23:612-6.
14. Jin YS, Stephanopoulos G. Multi-dimensional gene target search for improving lycopene biosynthesis in Escherichia coli. Metab Eng. 2007;9:337-47.
15. Wang JF, Meng HL, Xiong ZQ, Zhang SL, Wang Y. Identification of novel knockout and up-regulated targets for improving isoprenoid production in E. coli. Biotechnol Lett. 2014;36:1021-7.
16. Choi HS, Lee SY, Kim TY, Woo HM. In silico identification of gene amplification targets for improvement of lycopene production. Appl Environ Microbiol. 2010;76:3097-105.
17. Yoon S-H, Lee Y-M, Kim J-E, Lee S-H, Lee J-H, Kim J-Y, Jung K-H, Shin Y-C, Keasling JD, Kim S-W. Enhanced lycopene production inEscherichia coli engineered to synthesize isopentenyl diphosphate and dimethylallyl diphosphate from mevalonate. Biotechnol Bioeng. 2006;94:1025-32.
18. Özaydn B, Burd H, Lee TS, Keasling JD. Carotenoid-based phenotypic screen of the yeast deletion collection reveals new genes with roles in isoprenoid production. Metab Eng. 2013;15:174-83.
19. Alper H, Miyaoku K, Stephanopoulos G. Construction of lycopene-overproducing E. coli strains by combining systematic and combinatorial gene knockout targets. Nat Biotechnol. 2005;23:612-6.
20. Kang MJ, Lee YM, Yoon SH, Kim JH, Ock SW, Jung KH, Shin YC, Keasling JD, Kim SW. Identification of genes affecting lycopene accumulation in Escherichia coli using a shot-gun method. Biotechnol Bioeng. 2005;91:636-42.
21. Chae HS, Kim K-H, Kim SC, Lee PC. Strain-dependent carotenoid productions in metabolically engineered Escherichia coli. Appl Biochem Biotechnol. 2010;162:2333-44.
22. Basturea GN, Dague DR, Deutscher MP, Rudd KE. YhiQ is RsmJ, the methyltransferase responsible for methylation of G1516 in 16S rRNA of E. coli. J Mol Biol. 2012;415:16-21.
23. Soupene E, van Heeswijk WC, Plumbridge J, Stewart V, Bertenthal D, Lee H, Prasad G, Paliy O, Charernnoppakul P, Kustu S. Physiological studies of Escherichia coli strain MG1655: growth defects and apparent cross-regulation of gene expression. J Bacteriol. 2003;185:5611-26.
24. Jensen KF. The Escherichia coli K-12 "wild types" W3110 and MG1655 have an rph frameshift mutation that leads to pyrimidine starvation due to low pyrE expression levels. J Bacteriol. 1993;175:3401-7.
25. Liu H, Wang Y, Tang Q, Kong W, Chung W-J, Lu T. MEP pathway-mediated isopentenol production in metabolically engineered Escherichia coli. Microb Cell Fact. 2014;13:135.
26. Yuan LZ, Rouvière PE, LaRossa RA, Suh W. Chromosomal promoter replacement of the isoprenoid pathway for enhancing carotenoid production in E. coli. Metab Eng. 2006;8:79-90.
27. Choi HS, Lee SY, Kim TY, Woo HM. In silico identification of gene amplification targets for improvement of lycopene production. Appl Environ Microbiol. 2010;76:3097-105.
28. Matthews PD, Wurtzel ET. Metabolic engineering of carotenoid accumulation in Escherichia coli by modulation of the isoprenoid precursor pool with expression of deoxyxylulose phosphate synthase. Appl Microbiol Biotechnol. 2000;53:396-400.
29. Archer CT, Kim JF, Jeong H, Park J, Vickers CE, Lee S, Nielsen LK. The genome sequence of E. coli W (ATCC 9637): comparative genome analysis and an improved genome-scale reconstruction of E. coli. BMC Genom. 2011;12:9.
30. Freddolino PL, Amini S, Tavazoie S. Newly identified genetic variations in common Escherichia coli MG1655 stock cultures. J Bacteriol. 2012;194:303-6.
31. Becker-Hapak M, Troxtel E, Hoerter J, Eisenstark A. RpoS dependent overexpression of carotenoids from Erwinia herbicola in OxyR deficient Escherichia coli. Biochem Biophys Res Commun. 1997;239:305-9.
32. Atlung T, Nielsen H, Hansen F. Characterisation of the allelic variation in the rpoS gene in thirteen K12 and six other non-pathogenic Escherichia coli strains. Mol Genet Genomics. 2002;266:873-81.
33. Dong T, Schellhorn HE. Control of RpoS in global gene expression of Escherichia coli in minimal media. Mol Genet Genomics. 2008;281:19-33.
34. Gillet LC, Navarro P, Tate S, Röst H, Selevsek N, Reiter L, Bonner R, Aebersold R. Targeted data extraction of the MS/MS Spectra generated by data-independent acquisition: a new concept for consistent and accurate proteome analysis. Mol Cell Proteom. 2012;11:O111.016717.
35. Soufi B, Krug K, Harst A, Macek B. Characterization of the E. coli proteome and its modifications during growth and ethanol stress. Front Microbiol. 2015;6:103.
36. Martínez-Antonio A, Janga SC, Thieffry D. Functional organisation of Escherichia coli transcriptional regulatory network. J Mol Biol. 2008;381:238-47.
37. Sezonov G, Joseleau-Petit D, D'Ari R. Escherichia coli physiology in Luria-Bertani Broth. J Bacteriol. 2007;189:8746-9.
38. Nystrom T. Stationary-phase physiology. Annu Rev Microbiol. 2004;58:161-81.
39. Tanaka K, Handel K, Loewen PC, Takahashi H. Identification and analysis of the rpoS-dependent promoter of katE, encoding catalase HPII in Escherichia coli. Biochim Biophy Acta (BBA) Gene Struct Expr. 1997;1352:161-6.
40. Lu C, Albano CR, Bentley WE, Rao G. Quantitative and kinetic study of oxidative stress regulons using green fluorescent protein. Biotechnol Bioeng. 2005;89:574-87.
41. Rohdich F, Zepeck F, Adam P, Hecht S, Kaiser J, Laupitz R, Grawert T, Amslinger S, Eisenreich W, Bacher A, Arigoni D. The deoxyxylulose phosphate pathway of isoprenoid biosynthesis: studies on the mechanisms of the reactions catalyzed by IspG and IspH protein. Proc Natl Acad Sci USA. 2003;100:1586-91.
42. Xiao Y, Savchenko T, Baidoo EE, Chehab WE, Hayden DM, Tolstikov V, Corwin JA, Kliebenstein DJ, Keasling JD, Dehesh K. Retrograde signaling by the plastidial metabolite MEcPP regulates expression of nuclear stress-response genes. Cell. 2012;149:1525-35.
43. Zhou K, Zou R, Stephanopoulos G, Too HP. Metabolite profiling identified methylerythritol cyclodiphosphate efflux as a limiting step in microbial isoprenoid production. PLoS One. 2012;7:e47513.
44. Fanciullino AL, Bidel LPR, Urban L. Carotenoid responses to environmental stimuli: integrating redox and carbon controls into a fruit model. Plant, Cell Environ. 2014;37:273-89.
45. Kim SJNE, Kobayashi H, Terao J, Nagao A. Formation of cleavage products by autoxidation of lycopene. Lipids. 2001;36:191-9.
46. Caris-Veyrat C, Schmid A, Carail M, Böhm V. Cleavage products of lycopene produced by in vitro oxidations: characterization and mechanisms of formation. J Agric Food Chem. 2003;51:7318-25.
47. Smirnova GV, Muzyka NG, Glukhovchenko MN, Oktyabrsky ON. Effects of menadione and hydrogen peroxide on glutathione status in growing Escherichia coli. Free Radic Biol Med. 2000;28:1009-16.
48. Collao B, Morales EH, Gil F, Calderón IL, Saavedra CP. ompW is cooperatively upregulated by MarA and SoxS in response to menadione. Microbiology. 2013;159:715-25.
49. Kappus H, Sies H. Toxic drug effects associated with oxygen metabolism: redox cycling and lipid peroxidation. Experientia. 1981;37:1233-41.
50. Hemmi H, Ohnuma S-I, Nagaoka K, Nishino T. Identification of genes affecting lycopene formation in Escherichia coli transformed with carotenoid biosynthetic genes: candidates for early genes in isoprenoid biosynthesis. J Biochem. 1998;123:1088-96.
51. Vickers C, Possell M, Nicholas Hewitt C, Mullineaux P. Genetic structure and regulation of isoprene synthase in Poplar (Populus spp.). Plant Molecular Biology. 2010;73:547-58.
52. Zhao Y, Yang J, Qin B, Li Y, Sun Y, Su S, Xian M. Biosynthesis of isoprene in Escherichia coli via methylerythritol phosphate (MEP) pathway. Appl Microbiol Biotechnol. 2011;90:1915-22.
53. Miller B, Oschinski C, Zimmer W. First isolation of an isoprene synthase gene from poplar and successful expression of the gene in Escherichia coli. Planta. 2001;213:483-7.
54. Vickers CE, Behrendorff JB, Bongers M, Brennan TC, Bruschi M, Nielsen LK. Production of industrially relevant isoprenoid compounds in engineered microbes. In: Microorganisms in biorefineries. Berlin: Springer. 2015. pp. 303-34.
55. Vickers CE, Bongers M, Bydder SF, Chrysanthopoulos P, Hodson MP. Protocols for the production and analysis of isoprenoids in bacteria and yeast. Springer Protocols Handbooks: Humana Press. 2015. pp. 1-30.
56. Zhao Y, Yang J, Qin B, Li Y, Sun Y, Su S, Xian M. Biosynthesis of isoprene in Escherichia coli via methylerythritol phosphate (MEP) pathway. Appl Microbiol Biotechnol. 2011;90:1915-22.
57. Yang J, Zhao G, Sun Y, Zheng Y, Jiang X, Liu W, Xian M. Bio-isoprene production using exogenous MVA pathway and isoprene synthase in Escherichia coli. Bioresour Technol. 2012;104:642-7.
58. Lv X, Xu H, Yu H. Significantly enhanced production of isoprene by ordered coexpression of genes dxs, dxr, and idi in Escherichia coli. Appl Microbiol Biotechnol. 2013;97(6):2357-65.
59. Beck ZQ, Cervin MA, Nielsen AT, Peres CM. Composition and methods of PGL for the increased production of isoprene. In http://www.freepatentsonlinecom/20150104853pdf. USA: Danisco US Inc., The Goodyear Tire & Rubber Company. 2015.
60. Lajoie MJ, Gregg CJ, Mosberg JA, Washington GC, Church GM. Manipulating replisome dynamics to enhance lambda Red-mediated multiplex genome engineering. Nucleic Acids Res. 2012;40:e170.
61. Carr PA, Wang HH, Sterling B, Isaacs FJ, Lajoie MJ, Xu G, Church GM, Jacobson JM. Enhanced multiplex genome engineering through co-operative oligonucleotide co-selection. Nucleic Acids Res. 2012;40:e132.
62. Wang HH, Kim H, Cong L, Jeong J, Bang D, Church GM. Genome-scale promoter engineering by coselection MAGE. Nat Methods. 2012;9:591-3.
63. Vickers CE, Possell M, Cojocariu CI, Velikova VB, Laothawornkitkul J, Ryan A, Mullineaux PM, Nicholas Hewitt C. Isoprene synthesis protects transgenic tobacco plants from oxidative stress. Plant, Cell Environ. 2009;32:520-31.
64. Cervin MA, Whited GM, Miasnikov A, Peres CM, Weyler W, Wells DH, Bott RR. Isoprene synthase variants for improved microbial production of isoprene. Google Patents. 2010.
65. Gibson DG, Young L, Chuang R-Y, Venter JC, Hutchison CA, Smith HO. Enzymatic assembly of DNA molecules up to several hundred kilobases. Nat Meth. 2009;6:343-5.
66. Sambrook J. Molecular cloning: a laboratory manual/Joseph Sambrook, David W. Russell. Cold Spring Harbor, NY: Cold Spring Harbor Laboratory. 2001.
67. Terrific Broth. Cold Spring Harbor Protocols 2006. 2006:pdb.rec8620.
68. Luo B, Groenke K, Takors R, Wandrey C, Oldiges M. Simultaneous determination of multiple intracellular metabolites in glycolysis, pentose phosphate pathway and tricarboxylic acid cycle by liquid chromatography-mass spectrometry. J Chromatogr A. 2007;1147:153-64.
69. Sangster T, Major H, Plumb R, Wilson AJ, Wilson ID. A pragmatic and readily implemented quality control strategy for HPLC-MS and GC-MS-based metabonomic analysis. Analyst. 2006;131:1075-8.
70. Hodson M, Dear G, Griffin J, Haselden J. An approach for the development and selection of chromatographic methods for high-throughput metabolomic screening of urine by ultra pressure LC-ESI-ToF-MS. Metabolomics. 2009;5:166-82.
71. Soares NC, Spat P, Krug K, Macek B. Global dynamics of the Escherichia coli proteome and phosphoproteome during growth in minimal medium. J Proteome Res. 2013;12:2611-21.
72. Wessel D, Flügge UI. A method for the quantitative recovery of protein in dilute solution in the presence of detergents and lipids. Anal Biochem. 1984;138:141-3.
73. Kappler U, Nouwens AS. The molybdoproteome of Starkeya novella-insights into the diversity and functions of molybdenum containing proteins in response to changing growth conditions. Metallomics. 2013;5:325-34.
74. Orellana CA, Marcellin E, Schulz BL, Nouwens AS, Gray PP, Nielsen LK. High-antibody-producing Chinese hamster ovary cells up-regulate intracellular protein transport and glutathione synthesis. J Proteome Res. 2015;14:609-18.
75. Basturea GN, Dague DR, Deutscher MP, Rudd KE. YhiQ is RsmJ, the methyltransferase responsible for methylation of G1516 in 16S rRNA of E. coli. J Mol Biol. 2012;415:16-21.
76. Lajoie MJ, Gregg CJ, Mosberg JA, Washington GC, Church GM. Manipulating replisome dynamics to enhance lambda Red-mediated multiplex genome engineering. Nucleic Acids Res. 2012;40:e170.
77. Cunningham FX, Sun Z, Chamovitz D, Hirschberg J, Gantt E. Molecular structure and enzymatic function of lycopene cyclase from the Cyanobacterium Synechococcus sp. strain PCC7942. Plant Cell. 1994;6:1107-21.
78. Amann E, Ochs B, Abel K-J. Tightly regulated tac promoter vectors useful for the expression of unfused and fused proteins in Escherichia coli. Gene. 1988;69:301-15.
79. Datsenko KA, Wanner BL. One-step inactivation of chromosomal genes in Escherichia coli K-12 using PCR products. Proc Natl Acad Sci. 2000;97:6640-5.