Tools for advanced and targeted genetic manipulation of the β-lactam antibiotic producer Acremonium chrysogenum

Journal of Biotechnology

Volumn 169, Issue 1, 2014, Pages 51-62

  Bloemendal, S ^a,b   Loper D ^a,b   Terfehr, D ^a,b   Kopke, K ^a,b   Kluge, J ^a,b   Teichert, I ^b   Kuck U ^a,b  

^a INSTITUTE FOR MICROELECTRONICS   (Austria)

^b RUHR UNIVERSITY BOCHUM   (Germany)

Author keywords

Acremonium chrysogenum; Cephalosporin C; FLP FRT recombination system; Inducible promoter; Targeted insertion of foreign DNA

Indexed keywords

ACREMONIUM; CEPHALOSPORIN C; GROWTH CHARACTERISTIC; HOMOLOGOUS RECOMBINATION; INDUCIBLE PROMOTER; MORPHOLOGICAL CHANGES; PHARMACEUTICAL INDUSTRY; RECOMBINATION SYSTEM;

BIODEGRADATION; DNA; FUNGI; GENES; GENETIC ENGINEERING; TOOLS;

ANTIBIOTICS;

BETA LACTAM ANTIBIOTIC; CEPHALOSPORIN C; GENOMIC DNA; XYLOSE;

ARTICLE; CEPHALOSPORIUM ACREMONIUM; DRUG INDUSTRY; GENE DELETION; GENE EXPRESSION; GENE INSERTION; GENE TARGETING; GENETIC ENGINEERING; GENETIC MANIPULATION; HOMOLOGOUS RECOMBINATION; IMAGE ANALYSIS; LIFESTYLE; NONHUMAN; OSMOTIC STRESS; PRIORITY JOURNAL; PROMOTER REGION; REPORTER GENE; SEQUENCE ANALYSIS;

ACREMONIUM CHRYSOGENUM; CEPHALOSPORIN C; FLP/FRT RECOMBINATION SYSTEM; INDUCIBLE PROMOTER; TARGETED INSERTION OF FOREIGN DNA;

ACREMONIUM; ANTI-BACTERIAL AGENTS; BETA-LACTAMS; GENE DELETION; GENE EXPRESSION REGULATION; GENE TARGETING; GENETIC ENGINEERING; PROMOTER REGIONS, GENETIC;

EID: 84888779657     PISSN: 01681656     EISSN: 18734863     Source Type: Journal    
DOI: 10.1016/j.jbiotec.2013.10.036     Document Type: Article

References (79)

1. Abraham E.P., Newton G.G.F., Olson B.H., Schuurmans D.M., Schenck J.R., Hargie M.P., Fisher M.W., Fusari S.A. Identity of cephalosporin N and synnematin B. Nature 1955, 176:551.
2. Altschul S.F., Madden T.L., Schäffer A.A., Zhang J., Zhang Z., Miller W., Lipman D.J. Gapped BLAST and PSI-BLAST: a new generation of protein database search programs. Nucleic Acids Res. 1997, 25:3389-3402.
3. Aravind L., Koonin E.V. SAP - a putative DNA-binding motif involved in chromosomal organization. Trends Biochem. Sci. 2000, 25:112-114.
4. Aravind L., Koonin E.V. Prokaryotic homologs of the eukaryotic DNA-end-binding protein Ku, novel domains in the Ku protein and prediction of a prokaryotic double-strand break repair system. Genome Res. 2001, 11:1365-1374.
5. Bayram Ö., Krappmann S., Ni M., Bok J.W., Helmstaedt K., Valerius O., Braus-Stromeyer S., Kwon N.J., Keller N.P., Yu J.H., Braus G.H. VelB/VeA/LaeA complex coordinates light signal with fungal development and secondary metabolism. Science 2008, 320:1504-1506.
6. Becker D.M., Lundblad V. Introduction of DNA into yeast cells. Current Protocols in Molecular Biology 1994, 13.17.01-13.17.10. Wiley, New York, NY. F.M. Ausubel, R. Brent, R.E. Kingston, D.D. Moore, J.G. Seidman, J.A. Smith, K. Struhl (Eds.).
7. Bloemendal S., Bernhards Y., Bartho K., Dettmann A., Voigt O., Teichert I., Seiler S., Wolters D.A., Pöggeler S., Kück U. A homologue of the human STRIPAK complex controls sexual development in fungi. Mol. Microbiol. 2012, 84:310-323.
8. Böhm J., Hoff B., O'Gorman C.M., Wolfers S., Klix V., Binger D., Zadra I., Kürnsteiner H., Pöggeler S., Dyer P.S., Kück U. Sexual reproduction and mating-type-mediated strain development in the penicillin-producing fungus Penicillium chrysogenum. Proc. Natl. Acad. Sci. U. S. A. 2013, 110:1476-1481.
9. Bullock W.O., Fernandez J.M., Short J.M. XL1-Blue: a high efficiency plasmid transforming recA Escherichia coli strain with β-galactosidase selection. Biotechniques 1987, 5:376-378.
10. Christianson T.W., Sikorski R.S., Dante M., Shero J.H., Hieter P. Multifunctional yeast high-copy-number shuttle vectors. Gene 1992, 110:119-122.
11. Colot H.V., Park G., Turner G.E., Ringelberg C., Crew C.M., Litvinkova L., Weiss R.L., Borkovich K.A., Dunlap J.C. A high-throughput gene knockout procedure for Neurospora reveals functions for multiple transcription factors. Proc. Natl. Acad. Sci. U. S. A. 2006, 103:10352-10357.
12. Cox M.M. The FLP protein of the yeast 2-μm plasmid: expression of a eukaryotic genetic recombination system in Escherichia coli. Proc. Natl. Acad. Sci. U. S. A. 1983, 80:4223-4227.
13. Demain A.L. Antibiotics: natural products essential to human health. Med. Res. Rev. 2009, 29:821-842.
14. Dennison P.M., Ramsdale M., Manson C.L., Brown A.J. Gene disruption in Candida albicans using a synthetic, codon-optimised Cre-loxP system. Fungal Genet. Biol. 2005, 42:737-748.
15. Dreyer J., Eichhorn H., Friedlin E., Kürnsteiner H., Kück U. A homologue of the Aspergillus velvet gene regulates both cephalosporin C biosynthesis and hyphal fragmentation in Acremonium chrysogenum. Appl. Environ. Microbiol. 2007, 73:3412-3422.
16. Elander R.P. Industrial production of β-lactam antibiotics. Appl. Microbiol. Biotechnol. 2003, 61:385-392.
17. Esser K. Cryptogams - Cyanobacteria, Algae, Fungi, Lichens 1982, Cambridge University Press, London, England.
18. Fairhead C., Llorente B., Denis F., Soler M., Dujon B. New vectors for combinatorial deletions in yeast chromosomes and for gap-repair cloning using 'split-marker' recombination. Yeast 1996, 12:1439-1457.
19. Fedoryshyn M., Petzke L., Welle E., Bechthold A., Luzhetskyy A. Marker removal from actinomycetes genome using Flp recombinase. Gene 2008, 419:43-47.
20. Golic K.G., Lindquist S. The FLP recombinase of yeast catalyzes site-specific recombination in the Drosophila genome. Cell 1989, 59:499-509.
21. Gough J., Karplus K., Hughey R., Chothia C. Assignment of homology to genome sequences using a library of hidden Markov models that represent all proteins of known structure. J. Mol. Biol. 2001, 313:903-919.
22. P. J. Biotechnol. 2013, 163:77-80.
23. Gu Y., Jin S., Gao Y., Weaver D.T., Alt F.W. Ku70-deficient embryonic stem cells have increased ionizing radiosensitivity, defective DNA end-binding activity, and inability to support V(D)J recombination. Proc. Natl. Acad. Sci. U. S. A. 1997, 94:8076-8081.
24. Haarmann T., Lorenz N., Tudzynski P. Use of a nonhomologous end joining deficient strain (δku70) of the ergot fungus Claviceps purpurea for identification of a nonribosomal peptide synthetase gene involved in ergotamine biosynthesis. Fungal Genet. Biol. 2008, 45:35-44.
25. Hoff B., Schmitt E.K., Kück U. CPCR1, but not its interacting transcription factor AcFKH1, controls fungal arthrospore formation in Acremonium chrysogenum. Mol. Microbiol. 2005, 56:1220-1233.
26. Hoff B., Pöggeler S., Kück U. Eighty years after its discovery, Fleming's Penicillium strain discloses the secret of its sex. Eukaryot. Cell 2008, 7:465-470.
27. Hoff B., Kamerewerd J., Sigl C., Mitterbauer R., Zadra I., Kürnsteiner H., Kück 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.
28. Hoff B., Kamerewerd J., Sigl C., Zadra I., Kück U. Homologous recombination in the antibiotic producer Penicillium chrysogenum: strain δPcku70 shows up-regulation of genes from the HOG pathway. Appl. Microbiol. Biotechnol. 2010, 85:1081-1094.
29. Idiris A., Bi K., Tohda H., Kumagai H., Giga-Hama Y. Construction of a protease-deficient strain set for the fission yeast Schizosaccharomyces pombe, useful for effective production of protease-sensitive heterologous proteins. Yeast 2006, 23:83-99.
30. Idiris A., Tohda H., Bi K.W., Isoai A., Kumagai H., Giga-Hama Y. Enhanced productivity of protease-sensitive heterologous proteins by disruption of multiple protease genes in the fission yeast Schizosaccharomyces pombe. Appl. Microbiol. Biotechnol. 2006, 73:404-420.
31. Iiizumi S., Kurosawa A., So S., Ishii Y., Chikaraishi Y., Ishii A., Koyama H., Adachi N. Impact of non-homologous end-joining deficiency on random and targeted DNA integration: implications for gene targeting. Nucleic Acids Res. 2008, 36:6333-6342.
32. Ishibashi K., Suzuki K., Ando Y., Takakura C., Inoue H. Nonhomologous chromosomal integration of foreign DNA is completely dependent on MUS-53 (human Lig4 homolog) in Neurospora. Proc. Natl. Acad. Sci. U. S. A. 2006, 103:14871-14876.
33. Jeong J.S., Mitchell T.K., Dean R.A. The Magnaporthe grisea snodprot1 homolog, MSP1, is required for virulence. FEMS Microbiol. Lett. 2007, 273:157-165.
34. Khrunyk Y., Münch K., Schipper K., Lupas A.N., Kahmann R. The use of FLP-mediated recombination for the functional analysis of an effector gene family in the biotrophic smut fungus Ustilago maydis. New Phytol. 2010, 187:957-968.
35. Klix V., Nowrousian M., Ringelberg C., Loros J.J., Dunlap J.C., Pöggeler S. Functional characterization of MAT1-1-specific mating-type genes in the homothallic ascomycete Sordaria macrospora provides new insights into essential and non-essential sexual regulators. Eukaryot. Cell 2010, 9:894-905.
36. Kopke K., Hoff B., Kück U. Application of the Saccharomyces cerevisiae FLP/FRT recombination system in filamentous fungi for marker recycling and construction of knockout strains devoid of heterologous genes. Appl. Environ. Microbiol. 2010, 76:4664-4674.
37. Kopke K., Hoff B., Bloemendal S., Katschorowski A., Kamerewerd J., Kück U. Members of the Penicillium chrysogenum velvet complex play functionally opposing roles in the regulation of penicillin biosynthesis and conidiation. Eukaryot. Cell 2013, 12:299-310.
38. Krappmann S. Gene targeting in filamentous fungi: the benefits of impaired repair. Fungal Biol. Rev. 2007, 21:25-29.
39. Krappmann S., Sasse C., Braus G.H. Gene targeting in Aspergillus fumigatus by homologous recombination is facilitated in a nonhomologous end-joining-deficient genetic background. Eukaryot. Cell 2006, 5:212-215.
40. Kück U., Hoff B. Application of the nourseothricin acetyltransferase gene (nat1) as dominant marker for the transformation of filamentous fungi. Fungal Genet. Newslett. 2006, 53:9-11.
41. Kück U., Hoff B. New tools for the genetic manipulation of filamentous fungi. Appl. Microbiol. Biotechnol. 2010, 86:51-62.
42. Liu T., Wang T., Li X., Liu X. Improved heterologous gene expression in Trichoderma reesei by cellobiohydrolase I gene (cbh1) promoter optimization. Acta Biochim. Biophys. Sin. 2008, 40:158-165.
43. Lloyd A.M., Davis R.W. Functional expression of the yeast FLP/FRT site-specific recombination system in Nicotiana tabacum. Mol. Gen. Genet. 1994, 242:653-657.
44. Madera M., Vogel C., Kummerfeld S.K., Chothia C., Gough J. The SUPERFAMILY database in 2004: additions and improvements. Nucleic Acids Res. 2004, 32:D235-D239.
45. Morschhäuser J., Michel S., Staib P. Sequential gene disruption in Candida albicans by FLP-mediated site-specific recombination. Mol. Microbiol. 1999, 32:547-556.
46. Nash C.H., Huber F.M. Antibiotic synthesis and morphological differentiation of Cephalosporium acremonium. Appl. Microbiol. 1971, 22:6-10.
47. Newton G.G.F., Abraham E.P. Cephalosporin C, a new antibiotic containing sulphur and D-α-aminoadipic acid. Nature 1955, 175:548.
48. Nicholas K.B., Nicholas H.B., Deerfield D.W. GeneDoc: analysis and visualization of genetic variation. EMBNEW. News 1997, 4:14.
49. Ninomiya Y., Suzuki K., Ishii C., Inoue H. Highly efficient gene replacements in Neurospora strains deficient for nonhomologous end-joining. Proc. Natl. Acad. Sci. U. S. A. 2004, 101:12248-12253.
50. Nowak C., Kück U. Development of an homologous transformation system for Acremonium chrysogenum based on the β-tubulin gene. Curr. Genet. 1994, 25:34-40.
51. Nowak C., Radzio R., Kück U. DNA-mediated transformation of a fungus employing a vector devoid of bacterial DNA sequences. Appl. Microbiol. Biotechnol. 1995, 43:1077-1081.
52. Nowrousian M., Ringelberg C., Dunlap J.C., Loros J.J., Kück U. Cross-species microarray hybridization to identify developmentally regulated genes in the filamentous fungus Sordaria macrospora. Mol. Genet. Genom. 2005, 273:137-149.
53. Nowrousian M., Frank S., Koers S., Strauch P., Weitner T., Ringelberg C., Dunlap J.C., Loros J.J., Kück U. The novel ER membrane protein PRO41 is essential for sexual development in the filamentous fungus Sordaria macrospora. Mol. Microbiol. 2007, 64:923-937.
54. Nowrousian M., Stajich J.E., Chu M., Engh I., Espagne E., Halliday K., Kamerewerd J., Kempken F., Knab B., Kuo H.C., Osiewacz H.D., Pöggeler S., Read N.D., Seiler S., Smith K.M., Zickler D., Kück U., Freitag M. De novo assembly of a 40Mb eukaryotic genome from short sequence reads: Sordaria macrospora, a model organism for fungal morphogenesis. PLoS Genet. 2010, 6:e1000891.
55. Ogasawara W., Shida Y., Furukawa T., Shimada R., Nakagawa S., Kawamura M., Yagyu T., Kosuge A., Xu J., Nogawa M., Okada H., Morikawa Y. Cloning, functional expression and promoter analysis of xylanase III gene from Trichoderma reesei. Appl. Microbiol. Biotechnol. 2006, 72:995-1003.
56. O'Gorman S., Fox D.T., Wahl G.M. Recombinase-mediated gene activation and site-specific integration in mammalian cells. Science 1991, 251:1351-1355.
57. Onions A.H.S., Brady B.L. Taxonomy of Penicillium and Acremonium. Penicillium and Acremonium 1987, 1-36. Plenum Press, New York. J.F. Peberdy (Ed.).
58. Pöggeler S., Kück U. Highly efficient generation of signal transduction knockout mutants using a fungal strain deficient in the mammalian ku70 ortholog. Gene 2006, 378:1-10.
59. Radzio R., Kück U. Efficient synthesis of the blood-coagulation inhibitor hirudin in the filamentous fungus Acremonium chrysogenum. Appl. Microbiol. Biotechnol. 1997, 48:58-65.
60. Rech C., Engh I., Kück U. Detection of hyphal fusion in filamentous fungi using differently fluorescence-labeled histones. Curr. Genet. 2007, 52:259-266.
61. Sambrook J., Russell D.W. Molecular cloning: a laboratory manual 2001, Cold Spring Harbor Laboratory Press, Cold Spring Harbor, NY. third ed.
62. Schmitt E.K., Kück U. The fungal CPCR1 protein, which binds specifically to β-lactam biosynthesis genes, is related to human regulatory factor×transcription factors. J. Biol. Chem. 2000, 275:9348-9357.
63. Schmitt E.K., Bunse A., Janus D., Hoff B., Friedlin E., Kürnsteiner H., Kück U. Winged helix transcription factor CPCR1 is involved in regulation of β-lactam biosynthesis in the fungus Acremonium chrysogenum. Eukaryot. Cell 2004, 3:121-134.
64. Schuster A., Schmoll M. Biology and biotechnology of Trichoderma. Appl. Microbiol. Biotechnol. 2010, 87:787-799.
65. Seidl V., Seibel C., Kubicek C.P., Schmoll M. Sexual development in the industrial workhorse Trichoderma reesei. Proc. Natl. Acad. Sci. U. S. A. 2009, 106:13909-13914.
66. Shoji J.Y., Maruyama J., Arioka M., Kitamoto K. Development of Aspergillus oryzae thiA promoter as a tool for molecular biological studies. FEMS Microbiol. Lett. 2005, 244:41-46.
67. Skatrud P.L., Queener S.W., Carr L.G., Fisher D.L. Efficient integrative transformation of Cephalosporium acremonium. Curr. Genet. 1987, 12:337-348.
68. Song H., Niederweis M. Functional expression of the Flp recombinase in Mycobacterium bovis BCG. Gene 2007, 399:112-119.
69. Stinnett S.M., Espeso E.A., Cobeno L., Araújo-Bazán L., Calvo A.M. Aspergillus nidulans VeA subcellular localization is dependent on the importin α carrier and on light. Mol. Microbiol. 2007, 63:242-255.
70. Takita Y., Takahara M., Nogami S., Anraku Y., Ohya Y. Applications of the long and accurate polymerase chain reaction method in yeast molecular biology: direct sequencing of the amplified DNA and its introduction into yeast. Yeast 1997, 13:763-768.
71. Thompson J.D., Higgins D.G., Gibson T.J. CLUSTAL W: improving the sensitivity of progressive multiple sequence alignment through sequence weighting, position-specific gap penalties and weight matrix choice. Nucleic Acids Res. 1994, 22:4673-4680.
72. Törrönen A., Mach R.L., Messner R., Gonzalez R., Kalkkinen N., Harkki A., Kubicek C.P. The two major xylanases from Trichoderma reesei: characterization of both enzymes and genes. Nat. Biotechnol. 1992, 10:1461-1465.
73. Wach A., Brachat A., Pohlmann R., Philippsen P. New heterologous modules for classical or PCR-based gene disruptions in Saccharomyces cerevisiae. Yeast 1994, 10:1793-1808.
74. Walker J.R., Corpina R.A., Goldberg J. Structure of the Ku heterodimer bound to DNA and its implications for double-strand break repair. Nature 2001, 412:607-614.
75. Walz M., Kück U. Polymorphic karyotypes in related Acremonium strains. Curr. Genet. 1991, 19:73-76.
76. Walz M., Kück U. Targeted integration into the Acremonium chrysogenum genome: disruption of the pcbC gene. Curr. Genet. 1993, 24:421-427.
77. Whittaker C.A., Hynes R.O. Distribution and evolution of von Willebrand/integrin A domains: widely dispersed domains with roles in cell adhesion and elsewhere. Mol. Biol. Cell 2002, 13:3369-3387.
78. Yarden O., Plamann M., Ebbole D.J., Yanofsky C. cot-1, a gene required for hyphal elongation in Neurospora crassa, encodes a protein kinase. EMBO J. 1992, 11:2159-2166.
79. Zadra I., Abt B., Parson W., Haas H. xylP promoter-based expression system and its use for antisense downregulation of the Penicillium chrysogenum nitrogen regulator NRE. Appl. Environ. Microbiol. 2000, 66:4810-4816.