New promoters for strain engineering of Penicillium chrysogenum

Fungal Genetics and Biology

Volumn 89, Issue , 2016, Pages 62-71

  Polli, Fabiola ^a   Meijrink, Ben ^b   Bovenberg, Roel A L ^a,b   Driessen, Arnold J M ^a,c  

^a UNIVERSITY OF GRONINGEN   (Netherlands)

^b DSM RESOLVE   (Netherlands)

^c Kluyver Center for Genomics of Industrial Fermentation   (Netherlands)

Author keywords

Aspergillus niger; Fermentation; Penicillium chrysogenum; Promoters

Indexed keywords

GREEN FLUORESCENT PROTEIN; RED FLUORESCENT PROTEIN;

ARTICLE; ASPERGILLUS NIGER; BIOENGINEERING; CONTROLLED STUDY; FERMENTATION; FUNGAL GENOME; FUNGAL STRAIN; FUNGUS GROWTH; GENE DOSAGE; GENE EXPRESSION PROFILING; HOMOLOGOUS RECOMBINATION; IN VIVO STUDY; NONHUMAN; PENICILLIUM CHRYSOGENUM; PRIORITY JOURNAL; PROMOTER REGION; PROTEIN EXPRESSION; REPORTER GENE; SACCHAROMYCES CEREVISIAE; AMINO ACID SEQUENCE; FUNGAL GENE; GENE EXPRESSION; GENETIC ENGINEERING; GENETICS;

AMINO ACID SEQUENCE; ASPERGILLUS NIGER; FERMENTATION; GENE EXPRESSION; GENES, FUNGAL; GENES, REPORTER; GENETIC ENGINEERING; GENOME, FUNGAL; PENICILLIUM CHRYSOGENUM; PROMOTER REGIONS, GENETIC; SACCHAROMYCES CEREVISIAE;

EID: 84960086659     PISSN: 10871845     EISSN: 10960937     Source Type: Journal    
DOI: 10.1016/j.fgb.2015.12.003     Document Type: Article

References (65)

1. Andersen M.R., Nielsen M.L., Nielsen J. Metabolic model integration of the bibliome, genome, metabolome and reactome of Aspergillus niger. Mol. Syst. Biol. 2008, 4:178.
2. Balance D.J. Sequences important for gene expression in filamentous fungi. Yeast 1986, 2:229-236.
3. Barredo J.L., Cantoral J.M., Alvarez E., Díez B., Martín J.F. Cloning, sequence analysis and transcriptional study of the isopenicillin N synthase of Penicillium chrysogenum AS-P-78. Mol. Gen. Genet. 1989, 216:91-98.
4. Batta G., Barna T., Gáspári Z., Sándor S., Kövér K.E., Binder U., Sarg B., Kaiserer L., Chhillar A.K., Eigentler A., Leiter E., Hegedüs N., Pócsi I., Lindner H., Marx F. Functional aspects of the solution structure and dynamics of PAF-a highly-stable antifungal protein from Penicillium chrysogenum. FEBS J. 2009, 276:2875-2890.
5. Brakhage A.A., Adrianopoulos A., Kato M., Steidl S., Davis M.A., Tsukagoshi N., Hynes M.J. HAP-like CCAAT-binding complexes in filamentous fungi: implications for biotechnology. Fungal Genet. Biol. 1999, 27:243-252.
6. Bryant J.A., Sellars L.E., Busby S.J.W., Lee D.J. Chromosome position effects on gene expression in Escherichia coli K-12. Nucl. Acids Res. 2014, 42:11383-11392.
7. Bourdichon F., Casaregola S., Farrokh C., Frisvad J.C., Gerds M.L., Hammes W.P., Harnett J., Huys G., Laulund S., Ouwehand A., Powell I.B., Prajapati J.B., Seto Y., Ter Schure E., Van Boven A., Vankerckhoven V., Zgoda A., Tuijtelaars S., Hansen E.B. Food fermentations: microorganisms with technological beneficial use. Int. J. Food Microbiol. 2012, 154:87-97.
8. Bussey H., Sherman D., Somers J.M. Action of yeast killer factor: a resistant mutant with sensitive spheroplasts. J. Bacteriol. 1973, 113:1193-1197.
9. Cullen D., Gray G.L., Wilson L.J., Hayenga K.J., Michael H., Rey M.W., Norton S., Berka R.M. Controlled expression and secretion of bovine chymosin in Aspergillus nidulan 1987, 5:1-8.
10. De Boer P., Bastiaans J., Touw H., Kerkman R., Bronkhof J., van den Berg M., Offringa R. Highly efficient gene targeting in Penicillium chrysogenum using the bi-partite approach in δlig4 or δku70 mutants. Fungal Genet. Biol. 2010, 47:839-846.
11. Döbeli H., Andres H., Breyer N., Draeger N., Sizmann D., Zuber M.T., Weinert B., Wipf B. Recombinant fusion proteins for the industrial production of disulfide bridge containing peptides: purification, oxidation without concatamer formation, and selective cleavage. Protein Expression Purif. 1998, 12:404-414.
12. Engler C., Gruetzner R., Kandzia R., Marillonnet S. Golden gate shuffling: a one-pot DNA shuffling method based on type IIs restriction enzymes. PLoS One 2009, 4:e5553.
13. Fawcett P., Abraham E.P. Delta-(alpha-aminoadipyl) cysteinylvaline synthetase. Methods Enzymol. 1975, 43:471-473.
14. Feng B., Friedlin E., Marzluf G.A. 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.
15. Funke M., Buchenauer A., Schnakenberg U., Mokwa W., Diederichs S., Mertens A., Müller C., Kensy F., Büchs J. Microfluidic BioLector-microfluidic bioprocess control in microtiter plates. Biotechnol. Bioeng. 2010, 107:497-505.
16. Ganzlin M., Rinas U. In-depth analysis of the Aspergillus niger glucoamylase (glaA) promoter performance using high-throughput screening and controlled bioreactor cultivation techniques. J. Biotechnol. 2008, 135:266-271.
17. Gibbs P.A., Seviour R.J., Schmid F. Growth of filamentous fungi in submerged culture: problems and possible solutions. Crit. Rev. Biotechnol. 2000, 20:17-48.
18. Gietz R.D., Schiestl R.H. High-efficiency yeast transformation using the LiAc/SS carrier DNA/PEG method. Nat. Protoc. 2007, 2:31-34.
19. Goins C.L., Gerik K.J., Lodge J.K. Improvements to gene deletion in the fungal pathogen Cryptococcus neoformans: absence of Ku proteins increases homologous recombination, and co-transformation of independent DNA molecules allows rapid complementation of deletion phenotypes. Fungal Genet. Biol. 2006, 43:531-544.
20. Graessle S., Haas H., Friedlin E., Kürnsteiner H., Stöffler G., Redl B. Regulated system for heterologous gene expression in Penicillium chrysogenum. Appl. Environ. Microbiol. 1997, 63:753-756.
21. Gutiérrez S., Fierro F., Casqueiro J., Martín J.F. Gene organization and plasticity of the beta-lactam genes in different filamentous fungi. Antonie Van Leeuwenhoek 1999, 75:81-94.
22. Gorochowski T.E., van den Berg E., Kerkman R., Roubos J.A., Bovenberg R.A.L. Using synthetic biological parts and microbioreactors to explore the protein expression characteristics of Escherichia coli. ACS Synth. Biol. 2014, 3:129-139.
23. Gwynne D.I., Buxton F.P., Williams S.a., Garven S., Wayne Davies R. Genetically engineered secretion of active human interferon and a bacterial Endoglucanase from Aspergillus nidulans. Bio/Technology 1987, 5:713-719.
24. Haas H., Redl B., Friedlin E., Stöffler G. Isolation and analysis of Penicillium chrysogenum phoA gene encoding a secreted phosphate-repressible acid phosphatase. Gene 1992, 113:129-133.
25. Harju S., Fedosyuk H., Peterson K.R. Rapid isolation of yeast genomic DNA: Bust n' Grab. BMC Biotechnol. 2004, 4:8. 10.1186/1472-6750-4-8.
26. Harris D.M., van der Krogt Z.A., Klaassen P., Raamsdonk L.M., Hage S., van den Berg M.A., Bovenberg R.A.L., Pronk J.T., Daran J.-M. Exploring and dissecting genome-wide gene expression responses of Penicillium chrysogenum to phenylacetic acid consumption and penicillinG production. BMC Genomics 2009, 10:75.
27. Herrero S., Takeshita N., Fischer R. The Aspergillus nidulans CENP-E kinesin motor KipA interacts with the fungal homologue of the centromere-associated protein CENP-H at the kinetochore. Mol. Microbiol. 2011, 80:981-994.
28. Hevekerl A., Kuenz A., Vorlop K.-D. Filamentous fungi in microtiter plates-an easy way to optimize itaconic acid production with Aspergillus terreus. Appl. Microbiol. Biotechnol. 2014, 98:6983-6989.
29. Hoskins I.C., Roberts C.F. Expression of the 3-phosphoglycerate kinase gene (pgkA) of Penicillium chrysogenum. Mol. Gen. Genet. 1994, 243:270-276.
30. Lean M.C., Hans K.J.M., Meijrink B., van Scheppingen W.B., Vollebregt A., Tee K.L., van der Laan J.M., Leys D., Munro A.W., van den Berg M.A. Single-step fermentative production of the cholesterol-lowering drug pravastatin via reprogramming of Penicillium chrysogenum. Proc. Natl. Acad Sci. USA 2015, 112:2847-2852.
31. Leiter E., Szappanos H., Oberparleiter C., Kaiserer L., Csernoch L., Pusztahelyi T., Emri T., Pócsi I., Salvenmoser W., Marx F. Antifungal protein PAF severely affects the integrity of the plasma membrane of Aspergillus nidulans and induces an apoptosis-like phenotype. Antimicrob. Agents Chemother. 2005, 49:2445-2453.
32. Lu X., Sun J., Nimtz M., Wissing J., Zeng A.P., Rinas U. The intra- and extracellular proteome of Aspergillus niger growing on defined medium with xylose or maltose as carbon substrate. Microb. Cell Fact. 2010, 20(9):23.
33. Kaiserer L., Oberparleiter C., Weiler-Görz R., Burgstaller W., Leiter E., Marx F. Characterization of the Penicillium chrysogenum antifungal protein PAF. Arch. Microbiol. 2003, 180:204-210.
34. Kensy F., Engelbrecht C., Büchs J. Scale-up from microtiter plate to laboratory fermenter: evaluation by online monitoring techniques of growth and protein expression in Escherichia coli and Hansenula polymorpha fermentations. Microb. Cell Fact. 2009, 8:68.
35. Kolar M., Punt P.J., van den Hondel C.A., Schwab H. Transformation of Penicillium chrysogenum using dominant selection markers and expression of an Escherichia coli lacZ fusion gene. Gene 1988.
36. Kovalchuk A., Weber S.S., Nijland J.G., Bovenberg R.A.L., Driessen A.J.M. Fungal ABC transporter deletion and localization analysis. Methods Mol. Biol. 2012, 835:1-16.
37. Marx F., Haas H., Reindl M., Stöffler G., Lottspeich F., Redl B. Cloning, structural organization and regulation of expression of the Penicillium chrysogenum paf gene encoding an abundantly secreted protein with antifungal activity. Gene 1995, 167:167-171.
38. Marx F. Small, basic antifungal proteins secreted from filamentous ascomycetes: a comparative study regarding expression, structure, function and potential application. Appl. Microbiol. Biotechnol. 2004, 65:133-142.
39. Meyer V., Wedde M., Stahl U. Transcriptional regulation of the antifungal protein in Aspergillus giganteus. Mol. Genet. Genomics 2002, 266:747-757.
40. Menne S., Walz M., Kück U. Expression studies with the bidirectional pcbAB-pcbC promoter region from Acremonium chrysogenum using reporter gene fusions. Appl. Microbiol. Biotechnol. 1994, 42:57-66.
41. Nevalainen K.M.H., Te'o V.S.J., Bergquist P.L. Heterologous protein expression in filamentous fungi. Trends Biotechnol. 2005, 23:468-474.
42. Nielsen M.L., De Jongh W.A., Meijer S.L., Nielsen J., Mortensen U.H. Transient marker system for iterative gene targeting of a prototrophic fungus. Appl. Environ. Microbiol. 2007, 73:7240-7245.
43. Nijkamp J.F., van den Broek M., Datema E., de Kok S., Bosman L., Luttik M.A., Daran-Lapujade P., Vongsangnak W., Nielsen J., Heijne W.H., Klaassen P., Paddon C.J., Platt D., Kötter P., van Ham R.C., Reinders M.J., Pronk J.T., de Ridder D., Daran J.M. De novo sequencing, assembly and analysis of the genome of the laboratory strain Saccharomyces cerevisiae CEN.PK113-7D, a model for modern industrial biotechnology. Microb. Cell Fact. 2012, 11:36.
44. Nijland J.G., Ebbendorf B., Woszczynska M., Boer R., Bovenberg R.A.L., Driessen A.J.M. Nonlinear biosynthetic gene cluster dose effect on penicillin production by Penicillium chrysogenum. Appl. Environ. Microbiol. 2010, 76:7109-7115.
45. Nijland J.G., Kovalchuk A., van den Berg M.A., Bovenberg R.A.L., Driessen A.J.M. Expression of the transporter encoded by the cefT gene of Acremonium chrysogenum increases cephalosporin production in Penicillium chrysogenum. Fungal Genet. Biol. 2008, 45:1415-1421.
46. Oldenburg K.R., Vo K.T., Michaelis S., Paddon C. Recombination-mediated PCR-directed plasmid construction in vivo in yeast. Nucl. Acids Res. 1997, 25:451-452.
47. Papagianni M. Fungal morphology and metabolite production in submerged mycelial processes. Biotechnol. Adv. 2004, 22:189-259.
48. Poulsen R.B., Nøhr J., Douthwaite S., Hansen L.V., Iversen J.J., Visser J., Ruijter G.J. Increased NADPH concentration obtained by metabolic engineering of the pentose phosphate pathway in Aspergillus niger. FEBS J. 2005, 272:1313-1325.
49. Raymond C.K., Pownder T.A., Sexson S.L. General method for plasmid construction using homologous recombination. Biotechniques 1999, 26(134-8):140-141.
50. Samorski M., Müller-Newen G., Büchs J. Quasi-continuous combined scattered light and fluorescence measurements: a novel measurement technique for shaken microtiter plates. Biotechnol. Bioeng. 2005, 92:61-68.
51. Saunders G., Picknett T.M., Tuite M.F., Ward M. Heterologous gene expression in filamentous fungi. Trends Biotechnol. 1989, 7:283-287.
52. Sikorski R.S., Hieter P. A system of shuttle vectors and yeast host strains designed for efficient manipulation of DNA in Saccharomyces cerevisiae. Genetics 1989, 122:19-27.
53. Smith T.L., Gaskell J., Berka R.M., Yang M., Henner D.J., Cullen D. The promoter of the glucoamylase-encoding gene of Aspergillus niger functions in Ustilago maydis. Gene 1990, 88:259-262.
54. Snoek I.S.I., van der Krogt Z.A., Touw H., Kerkman R., Pronk J.T., Bovenberg R.A.L., van den Berg M.A., Daran J.M. 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. 2009, 46:418-426.
55. Su X., Schmitz G., Zhang M., Mackie R.I., Cann I.K.O. Heterologous gene expression in filamentous fungi. Adv. Appl. Microbiol. 2012, 81:1-61.
56. Takata M., Sasaki M.S., Sonoda E., Morrison C., Hashimoto M., Utsumi H., Yamaguchi-Iwai Y., Shinohara A., Takeda S. Homologous recombination and non-homologous end-joining pathways of DNA double-strand break repair have overlapping roles in the maintenance of chromosomal integrity in vertebrate cells. EMBO J. 1998, 17:5497-5508.
57. Van den Berg M.A., Albang R., Albermann K., Badger J.H., Daran J.-M., Driessen A.J.M., Garcia-Estrada C., Fedorova N.D., Harris D.M., Heijne W.H.M., Joardar V., Kiel J.A.K.W., Kovalchuk A., Martín J.F., Nierman W.C., Nijland J.G., Pronk J.T., Roubos J.A., van der Klei I.J., van Peij N.N.M.E., Veenhuis M., von Döhren H., Wagner C., Wortman J., Bovenberg R.A.L. Genome sequencing and analysis of the filamentous fungus Penicillium chrysogenum. Nat. Biotechnol. 2008, 26:1161-1168.
58. van den Hondel C.A.M.J.J., Punt P.J., van Gorcom R.F.M. Heterologous gene expression in filamentous fungi. More Gene Manipulations in Fungi 1991, 396-428. Academic Press Inc., San Diego, Calif. J.W. Bennett, L.L. Lasure (Eds.).
59. Varadarajalu L.P., Punekar N.S. Cloning and use of sC as homologous marker for Aspergillus niger transformation. J. Microbiol. Methods 2005, 61:219-224.
60. Veiga T., Gombert A.K., Landes N., Verhoeven M.D., Kiel J.A.K.W., Krikken A.M., Nijland J.G., Touw H., Luttik M.A.H., van der Toorn J.C., Driessen A.J.M., Bovenberg R.A.L., van den Berg M.A., van der Klei I.J., Pronk J.T., Daran J.-M. Metabolic engineering of β-oxidation in Penicillium chrysogenum for improved semi-synthetic cephalosporin biosynthesis. Metab. Eng. 2012, 14:437-448.
61. Vinetsky Y.P., Rozhkova A.M., Chulkin A.M., Satrutdinov A.D., Sinitsyna O.A., Fedorova E.A., Bekkarevich A.O., Okunev O.N., Sinitsyn A.P. Regulatory activity of heterologous gene-activator xlnR of Aspergillus niger in Penicillium canescens. Biochem. Biokhimiia 2009, 74:882-887.
62. Ward M., Turner G. The ATP synthase subunit 9 gene of Aspergillus nidulans: sequence and transcription. Mol. Gen. Genet. 1986, 205:331-338.
63. Weber S.S., Polli F., Boer R., Bovenberg R.A.L., Driessen A.J.M. Increased penicillin production in Penicillium chrysogenum production strains via balanced overexpression of Isopenicillin N Acyltransferase. Appl. Environ. Microbiol. 2012, 78:7107-7113.
64. Wnendt S., Felske-Zech H., Henze P.P.C., Ulbrich N., Stahl U. Characterization of the gene encoding alpha-sarcin, a ribosome inactivating protein secreted by Aspergillus giganteus. Gene 1993, 124:239-244.
65. 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.