Resolving phenylalanine metabolism sheds light on natural synthesis of penicillin G in Penicillium chrysogenum

Eukaryotic Cell

Volumn 11, Issue 2, 2012, Pages 238-249

  Veiga, Tânia ^a,b   Solis Escalante, Daniel ^a,b   Romagnoli, Gabriele ^a,b   Pierick, Angela Ten ^a,b   Hanemaaijer, Mark ^a,b   Deshmuhk, Amit ^a,b   Wahl, Aljoscha ^a,b   Pronk, Jack T ^a,b   Daran, Jean Marc ^a,b  

^a DELFT UNIVERSITY OF TECHNOLOGY   (Netherlands)

^b KLUYVER CENTRE FOR GENOMICS OF INDUSTRIAL FERMENTATION   (Netherlands)

Author keywords

[No Author keywords available]

Indexed keywords

CARBOXYLYASE; PENICILLIN G; PHENYLACETIC ACID DERIVATIVE; PHENYLALANINE; PHENYLPYRUVIC ACID; TRANSCRIPTOME;

ARTICLE; DECARBOXYLATION; ENZYMOLOGY; GENETICS; METABOLIC ENGINEERING; METABOLISM; PENICILLIUM CHRYSOGENUM; SACCHAROMYCES CEREVISIAE;

CARBOXY-LYASES; DECARBOXYLATION; METABOLIC ENGINEERING; PENICILLIN G; PENICILLIUM CHRYSOGENUM; PHENYLACETATES; PHENYLALANINE; PHENYLPYRUVIC ACIDS; SACCHAROMYCES CEREVISIAE; TRANSCRIPTOME;

PENICILLIUM CHRYSOGENUM; SACCHAROMYCES CEREVISIAE;

EID: 84856661252     PISSN: 15359778     EISSN: None     Source Type: Journal    
DOI: 10.1128/EC.05285-11     Document Type: Article

References (78)

1. Alberti S, Gitler AD, Lindquist S. 2007. A suite of Gateway cloning vectors for high-throughput genetic analysis in Saccharomyces cerevisiae. Yeast 24:913-919.
2. Arias-Barrau E, et al. 2004. The homogentisate pathway: a central cata-bolic pathway involved in the degradation of L-phenylalanine, L-tyrosine, and 3-hydroxyphenylacetate in Pseudomonas putida. J. Bacteriol. 186: 5062-5077.
3. Backus MP, Stauffer JF. 1955. The production and selection of a family of strains in Penicillium chrysogenum. Mycologia 47:429-463.
4. Behrens OK, Corse J. 1948. Biosynthesis of penicillins; utilization of deuterophenylacetyl-N15-dl-valine in penicillin biosynthesis. J. Biol. Chem. 175:765-769.
5. Behrens OK, et al. 1948. Biosynthesis of penicillins; biological precursors for benzylpenicillin (penicillin G). J. Biol. Chem. 175:751-764.
6. Boer VM, et al. 2007. Transcriptional responses of Saccharomyces cerevi-siae to preferred and nonpreferred nitrogen sources in glucose-limited chemostat cultures. FEMS Yeast Res. 7:604-620.
7. Boiteux A, Hess B. 1970. Allosteric properties of yeast pyruvate decar-boxylase. FEBS Lett. 9:293-296.
8. Boon WR, Calam CT, Gudgeon H, Levi AA. 1948. Penicillin: analysis of the crude product by partition chromatography. 2. Chromatographic analysis of the penicillins from two strains of Penicillium notatum. Biochem. J. 43:262-265.
9. Chain E, et al. 1940. Penicillin as a chemotherapeutic agent. Lancet 2:226-228.
10. Christensen LH, Mandrup G, Nielsen J, Villadsen J. 1994. A robust liquid chromatographic method for measurement of medium components during penicillin fermentations. Anal. Chim. Acta 296:51-62.
11. Committee on Medical Research OSRDW, Medical Research Council. 1945. Chemistry of penicillin. Science 102:627-629.
12. Daran-Lapujade P, Daran JM, van Maris AJ, de Winde JH, Pronk JT. 2009. Chemostat-based micro-array analysis in baker's yeast. Adv. Mi-crob. Physiol. 54:257-311.
13. de Jonge LP, et al. 2011. Scale-down of penicillin production in Penicil-lium chrysogenum. Biotechnol. J. 6:944-958.
14. Douma RD, et al. 2011. Degeneration of penicillin production in ethanol-limited chemostat cultivations of Penicillium chrysogenum: a systems biology approach. BMC Syst. Biol. 5:132.
15. Douma RD, et al. 2010. Intracellular metabolite determination in the presence of extracellular abundance: application to the penicillin biosynthesis pathway in Penicillium chrysogenum. Biotechnol. Bioeng. 107:105-115.
16. Entian KD, Kötter P. 2007. Yeast genetic strain and plasmid collections. Methods Microbiol. 36:629-666.
17. Fernandez-Canon JM, Penalva MA. 1995. Fungal metabolic model for human type I hereditary tyrosinaemia. Proc. Natl. Acad. Sci. U. S. A. 92: 9132-9136.
18. Fernandez-Canon JM, Penalva MA. 1995. Molecular characterization of a gene encoding a homogentisate dioxygenase from Aspergillus nidulans and identification of its human and plant homologues. J. Biol. Chem. 270:21199-21205.
19. Ferrer-Sevillano F, Fernandez-Canon JM. 2007. Novel phacB-encoded cytochrome P450 monooxygenase from Aspergillus nidulans with 3-hydroxyphenylacetate 6-hydroxylase and 3,4-dihydroxyphenylacetate 6-hydroxylase activities. Eukaryot. Cell 6:514-520.
20. Fleming A. 1929. On the antibacterial action of cultures of a Penicillium, with special reference to their use in the isolation of B. influenza. Exp. Pathol. 10:226-236.
21. Flikweert MT, et al. 1996. Pyruvate decarboxylase: an indispensable enzyme for growth of Saccharomyces cerevisiaeon glucose. Yeast 12:247-257.
22. Gietz RD, Schiestl RH. 2007. High-efficiency yeast transformation using the LiAc/SS carrier DNA/PEG method. Nat. Protoc. 2:31-34.
23. Gombert AK, et al. 2011. Functional characterization of the oxaloacetase encoding gene and elimination of oxalate formation in the beta-lactam producer Penicillium chrysogenum. Fungal Genet. Biol. 48:831-839.
24. Gonzalez B, Francois J, Renaud M. 1997. A rapid and reliable method for metabolite extraction in yeast using boiling buffered ethanol. Yeast 13: 1347-1355.
25. Gordon M, Pan S, Virgona A, Numerof P. 1953. Biosynthesis of penicillin. I. Role of phenylacetic acid. Science 118:43.
26. Harris DM, et al. 2009. Exploring and dissecting genome-wide gene expression responses of Penicillium chrysogenum to phenylacetic acid consumption and penicillin G production. BMC Genomics 10:75-95.
27. Harris DM, et al. 2009. Engineering of Penicillium chrysogenum for fermentative production of a novel carbamoylated cephem antibiotic precursor. Metab. Eng. 11:125-137.
28. Hazelwood LA, Daran JM, van Maris AJA, Pronk JT, Dickinson JR. 2008. The Ehrlich pathway for fusel alcohol production: a century of research on Saccharomyces cerevisiae metabolism. Appl. Environ. Microbiol. 74:2259-2265.
29. Hill VA. 1910. The possible effects of the aggregation of the molecules of hæmoglobin on its dissociation curves. J. Physiol. 40(Suppl.):1-7.
30. Hohmann S. 1991. Characterization of PDC6, a third structural gene for pyruvate decarboxylase in Saccharomyces cerevisiae. J. Bacteriol. 173:7963-7969.
31. Hohmann S, Cederberg H. 1990. Autoregulation may control the expression of yeast pyruvate decarboxylase structural genes PDC1 and PDC5. Eur. J. Biochem. 188:615-621.
32. Hubner G, Weidhase R, Schellenberger A. 1978. The mechanism of substrate activation of pyruvate decarboxylase: a first approach. Eur. J. Biochem. 92:175-181.
33. Juvvadi PR, Seshime Y, Kitamoto K. 2005. Genomics reveals traces of fungal phenylpropanoid-flavonoid metabolic pathway in the filamentous fungus Aspergillus oryzae. J. Microbiol. 43:475-486.
34. Kelly JM, Drysdale MR, Sealy-Lewis HM, Jones IG, Lockington RA. 1990. Alcohol dehydrogenase III in Aspergillus nidulans is anaerobically induced and post-transcriptionally regulated. Mol. Gen. Genet. 222:323-328.
35. -)-phenylalanine by Aspergillus niger. J. Bacteriol. 128:182-191.
36. Koetsier MJ, et al. 2010. The Penicillium chrysogenum aclA gene encodes a broad-substrate-specificity acyl-coenzyme A ligase involved in activation of adipic acid, a side-chain precursor for cephem antibiotics. Fungal Genet. Biol. 47:33-42.
37. Lange HC, et al. 2001. Improved rapid sampling for in vivo kinetics of intracellular metabolites in Saccharomyces cerevisiae. Biotechnol. Bioeng. 75:406-415.
38. Larkin MA, et al. 2007. Clustal W and Clustal X version 2.0. Bioinfor-matics 23:2947-2948.
39. Lee CJ, Yeh HJ, Yang WY, Kan CR. 1994. Separation of penicillin G from phenylacetic acid in a supported liquid membrane system. Biotechnol. Bioeng. 43:309-313.
40. Lein J. 1986. The Panlabs penicillin strain improvement program. Biotechnol. Ser. 1986:105-139.
41. Lockington RA, Borlace GN, Kelly JM. 1997. Pyruvate decarboxylase and anaerobic survival in Aspergillus nidulans. Gene 191:61-67.
42. Lowry O, Rosebrough N, Farr A, Randall R. 1951. Protein measurement with the Folin phenol reagent. J. Biol. Chem. 193:265-275.
43. Lutke-Eversloh T, Stephanopoulos G. 2005. Feedback inhibition of cho-rismate mutase/prephenate dehydrogenase (TyrA) of Escherichia coli: generation and characterization of tyrosine-insensitive mutants. Appl. Environ. Microbiol. 71:7224-7228.
44. Luttik MA, et al. 2008. Alleviation of feedback inhibition in Saccharomyces cerevisiae aromatic amino acid biosynthesis: quantification of metabolic impact. Metab. Eng. 10:141-153.
45. Mashego MR, van Gulik WM, Vinke JL, Heijnen JJ. 2003. Critical evaluation of sampling techniques for residual glucose determination in carbon-limited chemostat culture of Saccharomyces cerevisiae. Biotechnol. Bioeng. 83:395-399.
46. Mingot JM, Penalva MA, Fernandez-Canon JM. 1999. Disruption of phacA, an Aspergillus nidulans gene encoding a novel cytochrome P450 monooxygenase catalyzing phenylacetate 2-hydroxylation, results in penicillin overproduction. J. Biol. Chem. 274:14545-14550.
47. Moore K, Rao PV, Towers GH. 1967. Degradation of phenylalanine and tyrosine by Basidiomycetes. Life Sci. 6:2629-2633.
48. Moore K, Rao PV, Towers GH. 1968. Degradation of phenylalanine and tyrosine by Sporobolomyces roseus. Biochem. J. 106:507-514.
49. Moore K, Towers GH. 1967. Degradation of aromatic amino acids by fungi. I. Fate of L-phenylalanine in Schizophyllum commune. Can. J. Biochem. 45:1659-1665.
50. Moyer AJ, Coghill RD. 1946. Penicillin: IX. The laboratory scale production of penicillin in submerged cultures by Penicillium notatum Westling (NRRL 832). J. Bacteriol. 51:79.
51. Moyer AJ, Coghill RD. 1946. Penicillin: VIII. Production of penicillin in surface cultures. J. Bacteriol. 51:57.
52. Moyer AJ, Coghill RD. 1947. Penicillin: X. The effect of phenylacetic acid on penicillin production. J. Bacteriol. 53:329-341.
53. Mumberg D, Muller R, Funk M. 1995. Yeast vectors for the controlled expression of heterologous proteins in different genetic backgrounds. Gene 156:119-122.
54. Nasution U, van Gulik WM, Proell A, van Winden WA, Heijnen JJ. 2006. Generating short-term kinetic responses of primary metabolism of Penicillium chrysogenum through glucose perturbation in the bioscope mini reactor. Metab. Eng. 8:395-405.
55. Newbert RW, Barton B, Greaves P, Harper J, Turner G. 1997. Analysis of a commercially improved Penicillium chrysogenum strain series: involvement of recombinogenic regions in amplification and deletion of the penicillin biosynthesis gene cluster. J. Ind. Microbiol. Biotechnol. 19:18-27.
56. Noh K, Wahl A, Wiechert W. 2006. Computational tools for isotopically in stationary 13C labeling experiments under metabolic steady state conditions. Metab. Eng. 8:554-577.
57. Owen S, Johnson M. 1955. The effect of temperature changes on the production of penicillin by Penicillium chrysogenum W49-133. Appl. Mi-crobiol. 3:375-379.
58. Packer HL, Keshavarz-Moore E, Lilly MD, Thomas CR. 1992. Estimation of cell volume and biomass of Penicillium chrysogenum using image analysis. Biotechnol. Bioeng. 39:384-391.
59. Perlman D. 1966. Chemically defined media for antibiotic production. Ann. N. Y. Acad. Sci. 139:258-269.
60. Postma E, Verduyn C, Scheffers WA, Van Dijken JP. 1989. Enzymic analysis of the crabtree effect in glucose-limited chemostat cultures of Saccharomyces cerevisiae. Appl. Environ. Microbiol. 55:468-477.
61. Rodriguez-Saiz M, et al. 2001. Reduced function of a phenylacetate-oxidizing cytochrome p450 caused strong genetic improvement in early phylogeny of penicillin-producing strains. J. Bacteriol. 183:5465-5471.
62. Rodriguez-Saiz M, Diez B, Barredo JL. 2005. Why did the Fleming strain fail in penicillin industry? Fungal Genet. Biol. 42:464-470.
63. Sambrook J, Fritsch E, Maniatis T. 1989. Molecular cloning: a laboratory manual. Cold Spring Harbor Laboratory Press, Cold Spring Harbor, NY.
64. Schull TL, Fettinger JC, Knight DA. 1996. Synthesis and characterization of palladium(II) and platinum(II) complexes containing water-soluble hybrid phosphine-phosphonate ligands. Inorg. Chem. 35:6717-6723.
65. Seshime Y, Juvvadi PR, Fujii I, Kitamoto K. 2005. Genomic evidences for the existence of a phenylpropanoid metabolic pathway in Aspergillus oryzae. Biochem. Biophys. Res. Commun. 337:747-751.
66. Singh K, Johnson MJ. 1948. Evaluation of precursors for penicillin G. J. Bacteriol. 56:339 -355.
67. Skory CD. 2003. Induction of Rhizopus oryzae pyruvate decarboxylase genes. Curr. Microbiol. 47:59-64.
68. Snoek IS, et al. 2009. Construction of an hdfA Penicillium chrysogenum strain impaired in non-homologous end-joining and analysis of its potential for functional analysis studies. Fungal Genet. Biol. 46:418-426.
69. Stone RW, Farrell MA. 1946. Synthetic media for penicillin production. Science 104:445-446.
70. Tusher VG, Tibshirani R, Chu G. 2001. Significance analysis of microar-rays applied to the ionizing radiation response. Proc. Natl. Acad. Sci. U. S. A. 98:5116-5121.
71. van den Berg MA, et al. 2008. Genome sequencing and analysis of the filamentous fungus Penicillium chrysogenum. Nat. Biotechnol. 26:1161-1168.
72. van Gulik WM, de Laat WT, Vinke JL, Heijnen JJ. 2000. Application of metabolic flux analysis for the identification of metabolic bottlenecks in the biosynthesis of penicillin-G. Biotechnol. Bioeng. 68:602-618.
73. Verduyn C, Postma E, Scheffers WA, Van Dijken JP. 1992. Effect of benzoic acid on metabolic fluxes in yeasts: a continuous-culture study on the regulation of respiration and alcoholic fermentation. Yeast 8:501-517.
74. Vuralhan Z, et al. 2005. Physiological characterization of the ARO10-dependent, broad-substrate-specificity 2-oxo acid decarboxylase activity of Saccharomyces cerevisiae. Appl. Environ. Microbiol. 71:3276-3284.
75. Vuralhan Z, Morais MA, Tai SL, Piper MD, Pronk JT. 2003. Identification and characterizationof phenylpyruvate decarboxylase genes inSac-charomyces cerevisiae. Appl. Environ. Microbiol. 69:4534-4541.
76. 13C flux analysis: mass isotope correction, data consistency checking, and precursor relationships. Biotechnol. Bioeng. 85:259-268.
77. White S, Berry DR, McNeil B. 1999. Effect of phenylacetic acid feeding on the process of cellular autolysis in submerged batch cultures of Penicil-lium chrysogenum. J. Biotechnol. 75:173-185.
78. 13C-labeled cell extracts as internal standards. Anal. Biochem. 336:164-171.