Degeneration of penicillin production in ethanol-limited chemostat cultivations of Penicillium chrysogenum: A systems biology approach

BMC Systems Biology

Volumn 5, Issue , 2011, Pages

  Douma, Rutger D ^a   Batista, Joana M ^a   Touw, Kai M ^a   Kiel, Jan A K W ^b   Krikken, Arjen M ^b   Zhao, Zheng ^a   Veiga, Tânia ^a   Klaassen, Paul ^c   Bovenberg, Roel A L ^c   Daran, Jean Marc ^a   Heijnen, Joseph J ^a   van Gulik, Walter M ^a  

^a DELFT UNIVERSITY OF TECHNOLOGY   (Netherlands)

^b UNIVERSITY OF GRONINGEN   (Netherlands)

^c DSM BIOTECHNOLOGY CENTER   (Netherlands)

Author keywords

[No Author keywords available]

Indexed keywords

BACTERIA (MICROORGANISMS); PENICILLIUM CHRYSOGENUM;

ALCOHOL; PENICILLIN DERIVATIVE; TRANSCRIPTOME;

ARTICLE; BIOLOGICAL MODEL; BIOMASS; BIOREACTOR; BIOSYNTHESIS; GENE DOSAGE; GENETICS; METABOLISM; METHODOLOGY; MICROBIOLOGY; MULTIGENE FAMILY; PENICILLIUM CHRYSOGENUM; SYSTEMS BIOLOGY;

BIOMASS; BIOREACTORS; ETHANOL; GENE DOSAGE; INDUSTRIAL MICROBIOLOGY; MODELS, BIOLOGICAL; MULTIGENE FAMILY; PENICILLINS; PENICILLIUM CHRYSOGENUM; SYSTEMS BIOLOGY; TRANSCRIPTOME;

EID: 80051790521     PISSN: None     EISSN: 17520509     Source Type: Journal    
DOI: 10.1186/1752-0509-5-132     Document Type: Article

References (52)

1. Fleming A. Antibacterial Action of Cultures of A Penicillium, with Special Reference to Their Use in the Isolation of B. Influenza. Br J Exp Pathol 1928, 10:185-194.
2. Newbert RW, Barton B, Greaves P, Harper J, Turner G. 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 1997, 19:18-27. 10.1038/sj.jim.2900411, 9281849.
3. Peñalva MA, Rowlands RT, Turner G. The optimization of penicillin biosynthesis in fungi. Trends Biotechnol 1998, 16:483-489. 10.1016/S0167-7799(98)01229-3, 9830157.
4. Thykaer J, Nielsen J. Metabolic engineering of beta-lactam production. Metab Eng 2003, 5:56-69. 10.1016/S1096-7176(03)00003-X, 12749845.
5. van den Berg MA, Albang R, Albermann K, Badger JH, Daran JM, Driessen AJM, Garcia-Estrada C, Fedorova ND, Harris DM, Heijne WHM, et al. Genome sequencing and analysis of the filamentous fungus Penicillium chrysogenum. Nat Biotechnol 2008, 26:1161-1168. 10.1038/nbt.1498, 18820685.
6. Harris DM, van der Krogt ZA, Klaassen P, Raamsdonk LM, Hage S, van den Berg MA, Bovenberg RAL, Pronk JT, Daran JM. Exploring and dissecting genome-wide gene expression responses of Penicillium chrysogenum to phenylacetic acid consumption and penicillinG production. Bmc Genomics 2009, 10.
7. Kiel JAKW, van den Berg MA, Fusetti F, Poolman B, Bovenberg RAL, Veenhuis M, van der Klei IJ. Matching the proteome to the genome: the microbody of penicillin-producing Penicillium chrysogenum cells. Funct Integr Genom 2009, 9:167-184. 10.1007/s10142-009-0110-6, 21874651.
8. Jami M-S, Barreiro C, García-Estrada C, Martín J-F. Proteome Analysis of the Penicillin Producer Penicillium chrysogenum: characterization of protein changes during the industrial strain improvement. Mol Cell Proteomics 2010, 9:1182-1198. 10.1074/mcp.M900327-MCP200, 2877979, 20154335.
9. van Gulik WM, De Laat WTAM, Vinke JL, Heijnen JJ. Application of metabolic flux analysis for the identification of metabolic bottlenecks in the biosynthesis of penicillin-G. Biotechnol Bioeng 2000, 68:602-618. 10.1002/(SICI)1097-0290(20000620)68:6<602::AID-BIT3>3.0.CO;2-2, 10799985.
10. Nasution U, van Gulik WM, Ras C, Proell A, Heijnen JJ. A metabolome study of the steady-state relation between central metabolism, amino acid biosynthesis and penicillin production in Penicillium chrysogenum. Metab Eng 2008, 10:10-23. 10.1016/j.ymben.2007.07.001, 17905623.
11. Douma RD, de Jonge LP, Jonker CTH, Seifar RM, Heijnen JJ, van Gulik WM. Intracellular metabolite determination in the presence of extracellular abundance: application to the penicillin biosynthesis pathway in Penicillium chrysogenum. Biotechnol Bioeng 2010, 107:105-115. 10.1002/bit.22786, 20506508.
12. Clutterbuck PW, Lovell R, Raistrick H. The formation from glucose by members of the Penicillium chrysogenum series of a pigment, an alkali-soluble protein and penicillin - The antibacterial substance of fleming. Biochem J 1932, 26:1907-1918. 1261119, 16745019.
13. Righelato RC. Selection of Strains of Penicillium chrysogenum with Reduced Penicillin Yields in Continuous Cultures. J Appl Chem Biotechnol 1976, 26:153-159.
14. Künkel W, Berger D, Risch S, Wittmannbresinsky B. Genetic Instability of Industrial Strains of Penicillium chrysogenum. Appl Microbiol Biotechnol 1992, 36:499-502.
15. Christensen LH, Henriksen CM, Nielsen J, Villadsen J, Egelmitani M. Continuous Cultivation of Penicillium chrysogenum - Growth on Glucose and Penicillin Production. J Biotechnol 1995, 42:95-107. 10.1016/0168-1656(95)00056-V, 7576537.
16. van Gulik WM, Antoniewicz MR, De Laat WTAM, Vinke JL, Heijnen JJ. Energetics of growth and penicillin production in a high-producing strain of Penicillium chrysogenum. Biotechnol Bioeng 2001, 72:185-193. 10.1002/1097-0290(20000120)72:2<185::AID-BIT7>3.0.CO;2-M, 11114656.
17. Douma RD, Verheijen PJT, De Laat WTAM, Heijnen JJ, van Gulik WM. Dynamic Gene Expression Regulation Model for Growth and Penicillin Production in Penicillium chrysogenum. Biotechnol Bioeng 2010, 106:608-618. 10.1002/bit.22689, 20148401.
18. Robin J, Lettier G, McIntyre M, Noorman H, Nielsen J. Continuous cultivations of a Penicillium chrysogenum strain expressing the expandase gene from Streptomyces clavuligerus: Growth yields and morphological characterization. Biotechnol Bioeng 2003, 83:361-368. 10.1002/bit.10677, 12783492.
19. Gravius B, Bezmalinovic T, Hranueli D, Cullum J. Genetic Instability and Strain Degeneration in Streptomyces rimosus. Appl Environ Microbiol 1993, 59:2220-2228. 182261, 8357256.
20. Baltz RH, Seno ET. Properties of Streptomyces fradiae Mutants Blocked in Biosynthesis of the Macrolide Antibiotic Tylosin. Antimicrob Agents Chemother 1981, 20:214-225. 181666, 7283418.
21. Feng B, Friedlin E, Marzluf GA. A Reporter Gene Analysis of Penicillin Biosynthesis Gene-Expression in Penicillium Chrysogenum and Its Regulation by Nitrogen and Glucose Catabolite Repression. Appl Environ Microbiol 1994, 60:4432-4439. 202002, 7811083.
22. Gutiérrez S, Marcos AT, Casqueiro J, Kosalková K, Fernández FJ, Velasco J, Martín JF. Transcription of the pcbAB, pcbC and penDE genes of Penicillium chrysogenum AS-P-78 is repressed by glucose and the repression is not reversed by alkaline pHs. Microbiology 1999, 145:317-324. 10.1099/13500872-145-2-317, 10075414.
23. Rodríguez-Sáiz M, Barredo JL, Moreno MA, Fernández-Cañón JM, Peñalva MA, Díez B. Reduced function of a phenylacetate-oxidizing cytochrome P450 caused strong genetic improvement in early phylogeny of penicillin-producing strains. J Bacteriol 2001, 183:5465-5471. 10.1128/JB.183.19.5465-5471.2001, 95435, 11544206.
24. Zhao Z, Kuijvenhoven K, van Gulik WM, Heijnen JJ, van Winden WA, Verheijen PJ. Cytosolic NADPH balancing in Penicillium chrysogenum cultivated on mixtures of glucose and ethanol. Appl Microbiol Biotechnol 2011, 89:63-72. 10.1007/s00253-010-2851-5, 3016204, 20809073.
25. Kleijn RJ, Liu F, van Winden WA, van Gulik WM, Ras C, Heijnen JJ. Cytosolic NADPH metabolism in penicillin-G producing and non-producing chemostat cultures of Penicillium chrysogenum. Metab Eng 2007, 9:112-123. 10.1016/j.ymben.2006.08.004, 17008114.
26. Fierro F, Barredo JL, Díez B, Gutierrez S, Fernández FJ, Martín JF. The Penicillin Gene-Cluster Is Amplified in Tandem Repeats Linked by Conserved Hexanucleotide Sequences. Proc Natl Acad Sci USA 1995, 92:6200-6204. 10.1073/pnas.92.13.6200, 41670, 7597101.
27. Kiel JAKW, van der Klei IJ, van den Berg MA, Bovenberg RAL, Veenhuis M. Overproduction of a single protein, Pc-Pex 11p, results in 2-fold enhanced penicillin production by Penicillium chrysogenum. Fungal Genet Biol 2005, 42:154-164. 10.1016/j.fgb.2004.10.010, 15670713.
28. Meijer WH, Gidijala L, Fekken S, Kiel JAKW, van den Berg M, Lascaris R, Bovenberg R, van der Klei IJ. Peroxisomes are required for efficient penicillin biosynthesis in Penicillium chrysogenum. Appl Environ Microbiol 2010,
29. Kosalkova K, Garcia-Estrada C, Ullan RV, Godio RP, Feltrer R, Teijeira F, Mauriz E, Martin JF. The global regulator LaeA controls penicillin biosynthesis, pigmentation and sporulation, but not roquefortine C synthesis in Penicillium chrysogenum. Biochimie 2009, 91:214-225. 10.1016/j.biochi.2008.09.004, 18952140.
30. Hoff B, Kamerewerd J, Sigl C, Mitterbauer R, Zadra I, Kurnsteiner H, Kuck U. Two components of a velvet-like complex control hyphal morphogenesis, conidiophore development, and penicillin biosynthesis in Penicillium chrysogenum. Eukaryot Cell 2010, 9:1236-1250. 10.1128/EC.00077-10, 2918941, 20543063.
31. Bailey TL, Elkan C. Fitting a mixture model by expectation maximization to discover motifs in biopolymers. Proc Int Conf Intell Syst Mol Biol 1994, 2:28-36.
32. Barredo JL, Díez B, Alvarez E, Martín JF. Large Amplification of A 35-Kb Dna Fragment Carrying 2 Penicillin Biosynthetic Genes in High Penicillin Producing Strains of Penicillium chrysogenum. Curr Genet 1989, 16:453-459. 10.1007/BF00340725, 2515004.
33. Smith DJ, Bull JH, Edwards J, Turner G. Amplification of the Isopenicillin-N Synthetase Gene in A Strain of Penicillium chrysogenum Producing High-Levels of Penicillin. Mol Gen Genet 1989, 216:492-497. 10.1007/BF00334395, 21874636.
34. Theilgaard HBA, Kristiansen KN, Henriksen CM, Nielsen J. Purification and characterization of d-(L-a-aminoadipyl)-L-cysteinyl-D-valine synthetase from Penicillium chrysogenum. Biochem J 1997, 327:185-191. 1218779, 9355751.
35. Nasution U, van Gulik WM, Kleijn RJ, van Winden WA, Proell A, Heiinen JJ. Measurement of intracellular metabolites of primary metabolism and adenine nucleotides in chemostat cultivated Penicillium chrysogenum. Biotechnol Bioeng 2006, 94:159-166. 10.1002/bit.20842, 16508996.
36. Canelas AB, van Gulik WM, Heijnen JJ. Determination of the cytosolic free NAD/NADH ratio in Saccharomyces cerevisiae under steady-state and highly dynamic conditions. Biotechnol Bioeng 2008, 100:734-743. 10.1002/bit.21813, 18383140.
37. Theilgaard HA, Nielsen J. Metabolic control analysis of the penicillin biosynthetic pathway: the influence of the LLD-ACV: bisACV ratio on the flux control. Antonie van Leeuwenhoek Int J General Mol Microbiol 1999, 75:145-154.
38. Bartoszewska M, Kiel JA, Bovenberg RA, Veenhuis M, van der Klei IJ. Autophagy deficiency promotes beta-lactam production in Penicillium chrysogenum. Appl Environ Microbiol 2011, 77:1413-1422. 10.1128/AEM.01531-10, 3067201, 21169429.
39. Pollack JK, Harris SD, Marten MR. Autophagy in filamentous fungi. Fungal Genet Biol 2009, 46:1-8. 10.1016/j.fgb.2008.10.010, 19010432.
40. Meijer WH, van der Klei IJ, Veenhuis M, Kiel JAKW. ATG Genes Involved in Non-Selective Autophagy are Conserved from Yeast to Man, but the Selective Cvt and Pexophagy Pathways also Require Organism-Specific Genes. Autophagy 2007, 3:106-116.
41. Griffin TJ, Gygi SP, Ideker T, Rist B, Eng J, Hood L, Aebersold R. Complementary profiling of gene expression at the transcriptome and proteome levels in Saccharomyces cerevisiae. Mol Cell Proteomics 2002, 1:323-333. 10.1074/mcp.M200001-MCP200, 21874636.
42. Greenbaum D, Colangelo C, Williams K, Gerstein M. Comparing protein abundance and mRNA expression levels on a genomic scale. Genome Biol 2003, 4.
43. Garcia-Estrada C, Ullan RV, Velasco-Conde T, Godio RP, Teijeira F, Vaca I, Feltrer R, Kosalkova K, Mauriz E, Martin JF. Post-translational enzyme modification by the phosphopantetheinyl transferase is required for lysine and penicillin biosynthesis but not for roquefortine or fatty acid formation in Penicillium chrysogenum. Biochem J 2008, 415:317-324. 10.1042/BJ20080369, 18558918.
44. Christensen LH, Mandrup G, Nielsen J, Villadsen J. A Robust Liquid-Chromatographic Method for Measurement of Medium Components During Penicillin Fermentations. Anal Chim Acta 1994, 296:51-62.
45. Kresnowati MTAP, van Winden WA, Almering MJH, ten Pierick A, Ras C, Knijnenburg TA, Daran-Lapujade P, Pronk JT, Heijnen JJ, Daran JM. When transcriptome meets metabolome: fast cellular responses of yeast to sudden relief of glucose limitation. Molecular Systems Biology 2006, 2:1-12.
46. Harris DM, Diderich JA, van der Krogt ZA, Luttik MAH, Raamsdonk UM, Bovenberg RAL, van Gulik WM, van Dijken JP, Pronk JT. Enzymic analysis of NADPH metabolism in beta-lactam-producing Penicillium chrysogenum: Presence of a mitochondrial NADPH dehydrogenase. Metab Eng 2006, 8:91-101. 10.1016/j.ymben.2005.09.004, 16253533.
47. Krikken AM, Veenhuis M, van der Klei IJ. Hansenula polymorpha pex11 cells are affected in peroxisome retention. FEBS J 2009, 276:1429-1439. 10.1111/j.1742-4658.2009.06883.x, 19187239.
48. van Dam JC, Eman MR, Frank J, Lange HC, van Dedem GWK, Heijnen SJ. Analysis of glycolytic intermediates in Saccharomyces cerevisiae using anion exchange chromatography and electrospray ionization with tandem mass spectrometric detection. Anal Chim Acta 2002, 460:209-218.
49. Seifar RM, Zhao Z, van Dam J, van Winden W, van Gulik W, Heijnen JJ. Quantitative analysis of metabolites in complex biological samples using ion-pair reversed-phase liquid chromatography-isotope dilution tandem mass spectrometry. J Chromatogr, A 2008, 1187:103-110.
50. Canelas AB, ten Pierick A, Ras C, Seifar RM, van Dam JC, van Gulik WM, Heijnen JJ. Quantitative Evaluation of Intracellular Metabolite Extraction Techniques for Yeast Metabolomics. Anal Chem 2009, 81:7379-7389. 10.1021/ac900999t, 19653633.
51. Jaklitsch WM, Hampel W, Röhr M, Kubicek CP, Gamerith G. a-Aminoadipate pool concentration and penicillin biosynthesis in strains of Penicillium chrysogenum. Can J Microbiol 1986, 32:473-480. 10.1139/m86-087, 3089568.
52. Packer HL, Keshavarz-Moore E, Lilly MD, Thomas CR. Estimation of Cell Volume and Biomass of Penicillium chrysogenum Using Image-Analysis. Biotechnol Bioeng 1992, 39:384-391. 10.1002/bit.260390404, 18600959.