Enhanced FK506 production in Streptomyces tsukubaensis by rational feeding strategies based on comparative metabolic profiling analysis

Biotechnology and Bioengineering

Volumn 110, Issue 10, 2013, Pages 2717-2730

  Xia, Menglei ^a   Huang, Di ^a   Li, Shanshan ^a   Wen, Jianping ^a,b   Jia, Xiaoqiang ^a,b   Chen, Yunlin ^c  

^a TIANJIN UNIVERSITY   (China)

^b BEIJING UNIVERSITY OF POSTS AND TELECOMMUNICATIONS   (China)

^c BEIJING JIAOTONG UNIVERSITY   (China)

Author keywords

FK506; Metabolic profiling; Rational feeding strategies; Streptomyces tsukubaensis

Indexed keywords

BACTERIA; BIOCHEMISTRY; BIOMOLECULES; BIOSYNTHESIS; ENZYME ACTIVITY; FEEDING; FERMENTATION; METABOLISM; OPTIMIZATION; PROCESS CONTROL;

COMPARATIVE METABOLOMICS; FEEDING STRATEGIES; FK506; INDUSTRIAL FERMENTATION; INTRACELLULAR METABOLITES; METABOLIC PROFILING; METABOLITE CONCENTRATIONS; STREPTOMYCES TSUKUBAENSIS;

METABOLITES;

ACYL COENZYME A; ASCOMYCIN; SHIKIMIC ACID; TACROLIMUS; AMINO ACID; CULTURE MEDIUM; FATTY ACID;

AMINO ACID METABOLISM; ARTICLE; BACTERIUM CULTURE; BIOSYNTHESIS; CARBON METABOLISM; CULTURE MEDIUM; FATTY ACID METABOLISM; FERMENTATION; GAS CHROMATOGRAPHY; HIGH PERFORMANCE LIQUID CHROMATOGRAPHY; LIQUID CHROMATOGRAPHY; MASS SPECTROMETRY; METABOLITE; METABOLOME; METABOLOMICS; NONHUMAN; PROCESS OPTIMIZATION; STREPTOMYCES TSUKUBAENSIS; TANDEM MASS SPECTROMETRY; BIOENGINEERING; METABOLISM; PHYSIOLOGY; PROCEDURES; STREPTOMYCES; METABOLIC PROFILING; METHODOLOGY; RATIONAL FEEDING STRATEGIES;

STREPTOMYCES; STREPTOMYCES TSUKUBAENSIS;

AMINO ACIDS; BIOENGINEERING; CULTURE MEDIA; FATTY ACIDS; FERMENTATION; METABOLIC NETWORKS AND PATHWAYS; METABOLOME; METABOLOMICS; SHIKIMIC ACID; STREPTOMYCES; TACROLIMUS;

FK506; METABOLIC PROFILING; RATIONAL FEEDING STRATEGIES; STREPTOMYCES TSUKUBAENSIS;

EID: 84896414984     PISSN: 00063592     EISSN: 10970290     Source Type: Journal    
DOI: 10.1002/bit.24941     Document Type: Article

References (50)

1. Andexer JN, Kendrew SG, Nur-e-Alam M, Lazos O, Foster TA, Zimmermann AS, Warneck TD, Suthar D, Coates NJ, Koehn FE, Skotnicki JS, Carter GT, Gregory MA, Martin CJ, Moss SJ, Leadlay PF, Wilkinson B. 2011. Biosynthesis of the immunosuppressants FK506, FK520, and rapamycin involves a previously undescribed family of enzymes acting on chorismate. Proc Natl Acad Sci USA 108:4776-4781.
2. Baker M. 2011. Metabolomics: From small molecules to big ideas. Nat Methods 8:117-121.
3. Ball WJ, Atkinson DE. 1975. Adenylate energy charge in Saccharomyces cerevisiae during starvation. J Bacteriol 121:975-982.
4. Bolten CJ, Kiefer P, Letisse F, Portais JC, Wittmann C. 2007. Sampling for metabolome analysis of microorganisms. Anal Chem 79:3843-3849.
5. Brauer MJ, Yuan J, Bennett BD, Lu W, Kimball E, Botstein D, Rabinowitz JD. 2006. Conservation of the metabolomic response to starvation across two divergent microbes. Proc Natl Acad Sci USA 103:19302-19307.
6. Braus GH. 1991. Aromatic amino acid biosynthesis in the yeast Saccharomyces cerevisiae: A model system for the regulation of a eukaryotic biosynthetic pathway. Microbiol Rev 55:349-370.
7. Cheng YR, Fang A, Demain AL. 1995. Effect of amino acids on rapamycin biosynthesis by Streptomyces hygroscopicus. Appl Microbiol Biotechnol 43:1096-1098.
8. Chong WPK, Thng SH, Hiu AP, Lee DY, Chan ECY, Ho YS. 2012. LC-MS-based metabolic characterization of high monoclonal antibody-producing Chinese hamster ovary cells. Biotechnol Bioeng 109:3103-3111.
9. Christoph W, Jan W, Eriola B, Jens K, Daniela B, Ursula R, Rinas U, PÜHler A. 2007. Response of fluxome and metabolome to temperature-induced recombinant protein synthesis in Escherichia coli. J Biotechnol 132:375-384.
10. Dayem LC, Carney JR, Santi DV, Pfeifer BA, Khosla C, Kealey JT. 2002. Metabolic engineering of a methylmalonyl-CoA mutase-epimerase pathway for complex polyketide biosynthesis in Escherichia coli. Biochemistry 41:5193-5201.
11. Dietmair S, Hodson MP, Quek LE, Timmins NE, Chrysanthopoulos P, Jacob SS, Gray P, Nielsen LK. 2012. Metabolite profiling of CHO cells with different growth characteristics. Biotechnol Bioeng 109:1404-1414.
12. Ding MZ, Zhou X, Yuan YJ. 2010. Metabolome profiling reveals adaptive evolution of Saccharomyces cerevisiae during repeated vacuum fermentations. Metabolomics 6:42-55.
13. Ding MZ, Wang X, Yang Y, Yuan YJ. 2012. Comparative metabolic profiling of parental and inhibitors-tolerant yeasts during lignocellulosic ethanol fermentation. Metabolomics 8:232-243.
14. Dotzlaf JE, Metzger LS, Foglesong MA. 1984. Incorporation of amino acid-derived carbon into tylactone by Streptomyces fradiae GS14. Antimicrob Agents Chemother 25:216-220.
15. DuBois M, Gilles KA, Hamilton JK, Rebers PA, Smith F. 1956. Colorimetric method for determination of sugars and related substances. Anal Chem 28:350-356.
16. Fang A, Demain AL. 1995. Exogenous shikimic acid stimulates rapamycin biosynthesis in Streptomyces hygroscopicus. Folia Microbiol (Praha) 40:607-610.
17. Goranovič D, Kosec G, Mrak P, Fujs Š, Horvat J, Kuščer E, Kopitar G, Petković H. 2010. Origin of the allyl group in FK506 biosynthesis. J Biol Chem 285:14292-14300.
18. Graf R, Mehmann B, Braus GH. 1993. Analysis of feedback-resistant anthranilate synthases from Saccharomyces cerevisiae. J Bacteriol 175:1061-1068.
19. Jeong E, Kim HW, Nam JY, Shin HS. 2010. Enhancement of bioenergy production and effluent quality by integrating optimized acidification with submerged anaerobic membrane bioreactor. Bioresour Technol 101:S7-S12.
20. Jung W, Yoo Y, Park J, Park S, Han A, Ban Y, Kim E, Kim E, Yoon Y. 2011. A combined approach of classical mutagenesis and rational metabolic engineering improves rapamycin biosynthesis and provides insights into methylmalonyl-CoA precursor supply pathway in Streptomyces hygroscopicus ATCC 29253. Appl Microbiol Biotechnol 91:1389-1397.
21. Kim HS, Park YI. 2007. Lipase activity and tacrolimus production in Streptomyces clavuligerus CKD 1119 mutant strains. J Microbiol Biotechnol 17:1638-1644.
22. Kim HS, Park YI. 2008. Isolation and identification of a novel microorganism producing the immunosuppressant tacrolimus. J Biosci Bioeng 105:418-421.
23. Kim CJ, Chang YK, Chun GT. 2000. Enhancement of kasugamycin production by pH shock in batch cultures of Streptomyces kasugaensis. Biotechnol Prog 16:548-552.
24. Kim S, Shin MH, Hossain MA, Yun EJ, Lee H, Kim KH. 2011. Metabolite profiling of sucrose effect on the metabolism of Melissa officinalis by gas chromatography-mass spectrometry. Anal Bioanal Chem 399:3519-3528.
25. Kim S, Lee DY, Wohlgemuth G, Park HS, Fiehn O, Kim KH. 2013. Evaluation and optimization of metabolome sample preparation methods for Saccharomyces cerevisiae. Anal Chem 85:2169-2176.
26. Kino T, Hatanaka H, Hashimoto M, Nishiyama M, Goto T, Okuhara M, Kohsaka M, Aoki H, Imanaka H. 1987. FK-506, a novel immunosuppressant isolated from a Streptomyces. I. Fermentation, isolation, and physico-chemical and biological characteristics. J Antibiot (Tokyo) 40:1249-1255.
27. Korneli C, Bolten CJ, Godard T, Franco-Lara E, Wittmann C. 2012. Debottlenecking recombinant protein production in Bacillus megaterium under large-scale conditions-Targeted precursor feeding designed from metabolomics. Biotechnol Bioeng 109:1538-1550.
28. Kosec G, Goranovič D, Mrak P, Fujs Š, Kuščer E, Horvat J, Kopitar G, Petković H. 2012. Novel chemobiosynthetic approach for exclusive production of FK506. Metab Eng 14:39-46.
29. Li C, Florova G, Akopiants K, Reynolds KA. 2004. Crotonyl-coenzyme A reductase provides methylmalonyl-CoA precursors for monensin biosynthesis by Streptomyces cinnamonensis in an oil-based extended fermentation. Microbiology 150:3463-3472.
30. Li H, Ma ML, Luo S, Zhang RM, Han P, Hu W. 2012. Metabolic responses to ethanol in Saccharomyces cerevisiae using a gas chromatography tandem mass spectrometry-based metabolomics approach. Int J Biochem Cell Biol 44:1087-1096.
31. Liu J, Farmer JD, Jr., Lane WS, Friedman J, Weissman I, Schreiber SL. 1991. Calcineurin is a common target of cyclophilin-cyclosporin A and FKBP-FK506 complexes. Cell 66:807-815.
32. Lu S, Wang J, Niu Y, Yang J, Zhou J, Yuan Y. 2012. Metabolic profiling reveals growth related FAME productivity and quality of Chlorella sorokiniana with different inoculum sizes. Biotechnol Bioeng 109:1651-1662.
33. Mo S, Ban YH, Park JW, Yoo YJ, Yoon YJ. 2009. Enhanced FK506 production in Streptomyces clavuligerus CKD1119 by engineering the supply of methylmalonyl-CoA precursor. J Ind Microbiol Biotechnol 36:1473-1482.
34. Mo S, Kim DH, Lee JH, Park JW, Basnet DB, Ban YH, Yoo YJ, Chen SW, Park SR, Choi EA, Kim E, Jin YY, Lee SK, Park JY, Liu Y, Lee MO, Lee KS, Kim SJ, Kim D, Park BC, Lee SG, Kwon HJ, Suh JW, Moore BS, Lim SK, Yoon YJ. 2011. Biosynthesis of the allylmalonyl-CoA extender unit for the FK506 polyketide synthase proceeds through a dedicated polyketide synthase and facilitates the mutasynthesis of analogues. J Am Chem Soc 133:976-985.
35. Motamedi H, Shafiee A. 1998. The biosynthetic gene cluster for the macrolactone ring of the immunosuppressant FK506. Eur J Biochem 256:528-534.
36. Motamedi H, Shafiee A, Cai SJ, Streicher SL, Arison BH, Miller RR. 1996. Characterization of methyltransferase and hydroxylase genes involved in the biosynthesis of the immunosuppressants FK506 and FK520. J Bacteriol 178:5243-5248.
37. Motamedi H, Cai SJ, Shafiee A, Elliston KO. 1997. Structural organization of a multifunctional polyketide synthase involved in the biosynthesis of the macrolide immunosuppressant FK506. Eur J Biochem 244:74-80.
38. Nester EW, Jensen RA. 1966. Control of aromatic acid biosynthesis in Bacillus subtilis: Sequential feedback inhibition. J Bacteriol 91:1594-1598.
39. Park YS, Momose I, Tsunoda K, Okabe M. 1994. Enhancement of cephamycin C production using soybean oil as the sole carbon source. Appl Microbiol Biotechnol 40:773-779.
40. Park JW, Jung WS, Park SR, Park BC, Yoon YJ. 2007. Analysis of intracellular short organic acid-coenzyme A esters from actinomycetes using liquid chromatography-electrospray ionization-mass spectrometry. J Mass Spectrom 42:1136-1147.
41. Parsons WH, Sigal NH, Wyvratt MJ. 1993. FK506-a novel immunosuppressant. Ann N Y Acad Sci 685:22-36.
42. Reeves AR, Cernota WH, Brikun IA, Wesley RK, Mark Weber J. 2004. Engineering precursor flow for increased erythromycin production in Aeromicrobium erythreum. Metab Eng 6:300-312.
43. Selvarasu S, Ho YS, Chong WP, Wong NS, Yusufi FN, Lee YY, Yap MG, Lee DY. 2012. Combined in silico modeling and metabolomics analysis to characterize fed-batch CHO cell culture. Biotechnol Bioeng 109:1415-1429.
44. Singh BP, Behera BK. 2009. Regulation of tacrolimus production by altering primary source of carbons and amino acids. Lett Appl Microbiol 49:254-259.
45. Smart KF, Aggio RBM, Van Houtte JR, Villas-Boas SG. 2010. Analytical platform for metabolome analysis of microbial cells using methyl chloroformate derivatization followed by gas chromatography-mass spectrometry. Nat Protoc 5:1709-1729.
46. Tang L, Zhang YX, Hutchinson CR. 1994. Amino acid catabolism and antibiotic synthesis: Valine is a source of precursors for macrolide biosynthesis in Streptomyces ambofaciens and Streptomyces fradiae. J Bacteriol 176:6107-6119.
47. Wamelink MMC, Struys EA, Huck JHJ, Roos B, Van der Knaap MS, Jakobs C, Verhoeven NM. 2005. Quantification of sugar phosphate intermediates of the pentose phosphate pathway by LC-MS/MS: Application to two new inherited defects of metabolism. J Chromatogr B Analyt Technol Biomed Life Sci 823:18-25.
48. Wentzel A, Sletta H, Consortium S, Ellingsen TE, Bruheim P. 2012. Intracellular metabolite pool changes in response to nutrient depletion induced metabolic switching in Streptomyces coelicolor. Metabolites 2:178-194.
49. Yoon YJ, Choi CY. 1997. Nutrient effects on FK-506, a new immunosuppressant, production by Streptomyces sp. in a defined medium. J Ferment Bioeng 83:599-603.
50. Zhang W, Reynolds KA. 2001. MeaA, a putative coenzyme B12-dependent mutase, provides methylmalonyl coenzyme A for monensin biosynthesis in Streptomyces cinnamonensis. J Bacteriol 183:2071-2080.