Production of GFP and glucoamylase by recombinant Aspergillus niger: Effects of fermentation conditions on fungal morphology and protein secretion

Biotechnology Progress

Volumn 21, Issue 5, 2005, Pages 1389-1400

  Talabardon, Mylene ^a   Yang, Shang Tian ^a  

^a Ohio State University   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

BIOREACTORS; CELL CULTURE; CELL IMMOBILIZATION; CELLS; ENZYMES; FERMENTATION; FLUORESCENCE; GENES; MICROBIOLOGY; MORPHOLOGY; OXYGEN; PROTEINS;

ASPERGILLUS NIGER; GLUCOAMYLASE; PROTEIN SECRETION; ROTATING FIBROUS BEDS (RFB);

FUNGI;

GLUCAN 1,4 ALPHA GLUCOSIDASE; GREEN FLUORESCENT PROTEIN; RECOMBINANT PROTEIN;

ARTICLE; ASPERGILLUS NIGER; BIOFILM; BIOREACTOR; BIOSYNTHESIS; CELL PROLIFERATION; CELL SIZE; CULTURE TECHNIQUE; CYTOLOGY; FERMENTATION; GENETICS; GROWTH, DEVELOPMENT AND AGING; IMMOBILIZED CELL; METABOLISM; METHODOLOGY; MICROBIOLOGY; PHYSIOLOGY; PROTEIN ENGINEERING; PROTEIN SYNTHESIS;

ASPERGILLUS NIGER; BIOFILMS; BIOREACTORS; CELL CULTURE TECHNIQUES; CELL PROLIFERATION; CELL SIZE; CELLS, IMMOBILIZED; FERMENTATION; GLUCAN 1,4-ALPHA-GLUCOSIDASE; GREEN FLUORESCENT PROTEINS; PROTEIN BIOSYNTHESIS; PROTEIN ENGINEERING; RECOMBINANT PROTEINS;

ASPERGILLUS NIGER; FUNGI; GOSSYPIUM HIRSUTUM;

EID: 26644449199     PISSN: 87567938     EISSN: None     Source Type: Journal    
DOI: 10.1021/bp0501064     Document Type: Article

References (63)

1. Meerman, H. J., Kelley, A. S.; Ward, M. Advances in protein expression in filamentous fungi. In Protein Expression Technologies; Baneyx, F., Ed.; Horizon Bioscience, Wymondham, UK, 2004; pp 345-385.
2. Punt, P. J.; van Biezen, N.; Conesa, A.; Albers, A.; Mangnus, J.; van den Hondel, C. Filamentous fungi as cell factories for heterologous protein production. Trends Biotechnol. 2002, 20, 200-206.
3. Gouka, R. J.; Punt, P. J.; Hessing, J. G. M.; van den Hondel, C. A. M. J. J. Analysis of heterologous protein in defined recombinant A. awamori strains. Appl. Environ. Microbiol. 1996, 62, 1951-1957.
4. MacKenzie, D. A.; Jeenes, D. J.; Archer, D. B. Filamentous fungi as expression systems for heterologous proteins. In Mycota, 2nd ed.; Kueck, U., Ed.; Springer-Verlag: New York, 2004; Vol. 2, pp 289-315.
5. Christensen, T.; Woeldike, H.; Boel, E.; Mortensen, S. B.; Hjortshoej, K.; Thim, L.; Hansen, M. T. High level expression of recombinant genes in Aspergillus oryzae. Bio/Technology 1988, 6, 1419-1422.
6. Shibuya, I.; Tsuchiya, K.; Tamura, G.; Ishikawa, T.; Haro, S. Overproduction of an α-amylase/ glucoamylase fusion protein in Aspergillus oryzae using a high expression vector. Biosci. Biotechnol. Biochem. 1992, 56, 1674-1675.
7. Dunn-Coleman, N. S.; Bloebaum, P.; Berka, R. M.; Bodie, E.; Robinson, N.; Armstrong, G.; Ward, M.; Przetak, M.; Carter, G. L.; LaCost, R.; Wilson, L. J.; Kodama, K. H.; Baliu, E. F.; Bower, B.; Lamsa, M.; Heinsohn, H. Commercial levels of chymosin production by Aspergillus. Bio/Technology 1991, 9, 976-981.
8. Tsuchiya, K.; Gomi, K.; Tamura, G. Secretion of calf chymosin from the filamentous fungus Aspergillus oryzae. Appl. Microbiol. Biotechnol. 1993, 40, 327-332.
9. Ward, P. P.; Lo, J. Y.; Duke, M.; May, G. S.; Headon, D. R.; Conelly, O. M. Production of biologically active recombinant human lactoferrin in Aspergillus oryzae. Bio/Technology 1992, 10, 784-789.
10. Ward, P. P.; Piddington, C. S.; Cunningham, G. A.; Zhou, X.; Wyatt, R. D.; Conneely, O. M. A system for production of commercial quantities of human lactoferrin: a broad spectrum natural antibiotic. Bio/Technology 1995, 13, 498-503.
11. Tsuchiya, K.; Tada, S.; Gomi, K.; Kitamoto, K.; Kumagai, C.; Jigami, Y.; Tamura, G. High level expression of the synthetic human lysozyme gene in Aspergillus oryzae. Appl. Microbiol. Biotechnol. 1992, 38, 109-114.
12. Finkelstein, D. B. Improvement of enzyme production in Aspergillus. Antonie van Leeuwenhoek 1987, 53, 349-352.
13. Finkelstein, D. B.; Rambosek, J.; Crawford, M. S.; Soliday, S. L.; McAda, P. C.; Leach, J. Protein secretion in Aspergillus niger. In Genetics and Molecular Biology of Industrial Microorganisms; Hershberger, C. L., Queener, S. W., Hegeman, G., Eds.; American Society for Microbiology: Washington, DC, 1989; pp 295-300.
14. Radzio, R.; Kuch, U. Synthesis of biotechologically relevant heterologous proteins in filamentous fungi. Process Biochem. 1997, 32, 529-539.
15. Ward, M.; Wilson, L. J.; Kodama, K. H.; Rey, M. W.; Berka R. M. improved production of chymosin in Aspergillus by expression as a glucoamylase-chymosin fusion. Bio/Technology 1990, 8, 435-440.
16. Broekhuijsen, M. P.; Matern, I. E.; Contreras, R.; Kinghorn, J. R.; van den Hondel, C. A. M. J. J. Secretion of heterologous proteins by Aspergillus niger: production of active human interleukin-6 in a protease- deficient mutant by Kex2-like processing of a glucoamylase-hil-6 fusion protein. J. Biotechnol. 1993, 32, 135-145.
17. Gouka, R. J.; Punt, P. J.; van den Hondel, C. A. M. J. J. Efficient production of secreted proteins by Aspergillus: progress, limitations and prospects. Appl. Microbiol. Biotechnol. 1997, 47, 1-11.
18. Punt, P. J.; Veldhuisen, G.; van den Hondel, C. Protein targeting and secretion in filamentous fungi - a progress report. Antonie van Leeuwenhoek 1994, 65, 211-216.
19. Bocking, S. P.; Wiebe M. G.; Robson G. D.; Hansen K.; Christiansen L. H.; Trinci A. P. J. Effect of branch frequency in Aspergillus oryzae on protein secretion and culture viscosity. Biotechnol. Bioeng. 1999, 65, 638-648.
20. Wongwicharn, A.; Harvey, L. M.; McNeil, B. Secretion of heterologous and native proteins, growth and morphology in batch cultures of Aspergillus niger B1-D at varying agitation rates. J. Chem. Technol. Biotechnol. 1999, 74, 821-828.
21. Broekhuijsen, M. P.; Matern, I. E.; Contreras, R.; Kinghorn, J. R.; van den Hondel, C. A. M. J. J. Secretion of heterologous proteins by Aspergillus niger: Production of active human interleukin-6 in a protease-deficient mutant by KEX2-like processing of a glucoamylase-hIL-6 fusion protein. J. Biotechnol. 1993, 32, 135-145.
22. McIntyre, M.; Berry, D. R.; McNeil, B. Role of proteases in autolysis of Penicillium chrysogenum chemostat cultures in response to nutrient depletion. Appl. Microbiol. Biotechnol. 2000, 53, 235-242.
23. Berka, R. M.; Hayenga, K. J.; Lawlis, V. B.; Ward, M. Aspartic proteinase-deficient filamentous fungi for improved production of heterologous proteins. U.S. patent 6,509,171, 2003.
24. Wiebe, M. G. Stable production of recombinant proteins in filamentous fungi - problems and improvements. Mycologist 2003, 17, 140-144.
25. Iwashita, K. Recent studies of protein secretion by filamentous fungi. J. Biosci. Bioeng. 2002, 94, 530-535.
26. Thomas, C. R. Shear effects on cells in bioreactors. In Processing of Solid-Liquid Suspensions; Shamlou, P. A., Ed.; Butterworth-Heinemann: Oxford, UK, 1993; pp 158-191.
27. Makagiansar, H. Y.; Shamlou, P. A.; Thomas, C. R.; Lilly, M. D. The influence of mechanical forces on the morphology and penicillin production of Penicillium chrysogenum. Bioprocess Eng. 1993, 9, 83-90.
28. Wang, L. P.; Ridgway, D.; Gu, T. Y.; Moo-young, M. Effects of process parameters on heterologous protein production in Aspergillus niger fermentation. J. Chem. Technol. Biotechnol. 2003, 78, 1259-1266.
29. Bhargava, S.; Nandakumar, M. P.; Roy, A.; Wenger, K. S.; Marten, M. R. Pulsed feeding during fed-batch fungal fermentation leads to reduced viscosity without detrimentally affecting protein expression. Biotechnol. Bioeng. 2003, 81, 341-347.
30. Heydarian, S. M.; Mirjalili, N.; Ison, A. P. Effect of shear on morphology and erythromycin production in Saccharopolyspora erythraea fermentations. Bioprocess Eng. 1999, 21, 31-39.
31. Justen, P.; Paul, G. C.; Nienow, A. W.; Thomas, C. R. Dependence of Penicillium chrysogenum growth, morphology, vacuolation, and productivity in fed-batch fermentations on impeller type and agitation intensity. Biotechnol. Bioeng. 1998, 59, 762-775.
32. Paul, G. C.; Friede, M. A.; Thomas, C. R. Relationship between morphology and citric acid production in submerged Aspergillus niger fermentations. Biochem. Eng. J. 1999, 3, 121-129.
33. Bhargava, Swapnil; Wenger, Kevin S.; Marten, Mark R. Pulsed addition of limiting-carbon during Aspergillus oryzae fermentation leads to improved productivity of a recombinant enzyme. Biotechnol. Bioeng. 2003, 82, 111-117.
34. Kubicek, C. P.; Roehr, M. Aconitase and citric acid fermentation by Aspergillus niger. Appl. Environ. Micobiol. 1985, 50, 1336-1338.
35. Tay A.; Yang S. T. Production of L-(+)-lactic acid from glucose and starch by immobilized cells of Rhizopus oryzae in a rotating fibrous bed bioreactor. Biotechnol. Bioeng. 2002, 80, 1-12.
36. Metwally, M.; el Sayed, M.; Osman, M.; Hanegraaf, P. P. F.; Stouthamer, A. H.; Van Verseveld, H. W. Bioenergetic consequences of glucoamylase production in carbon-limited chemostat cultures of Aspergillus niger. Antonie van Leeuwenhoek 1991, 59, 35-43.
37. Wosten, H. A. B.; Moukha, S. M.; Sietsma, J. H.; Wessels, J. G. H. Localization of growth and secretion of proteins in Aspergillus niger. Gen. Microbiol. 1991, 137, 2017-2023.
38. Lee, I. H.; Walline, R. G.; Plamann, M. Apolar growth of Neurospora crassa leads to increased secretion of extracellular proteins. Mol. Microbiol. 1998, 29, 209-218.
39. Wosten, H. A. B.; Moukha, S. M.; Sietsma, J. H.; Wessels, J. G. H. Localization of growth and secretion of protein in Aspergillus niger, J. Gen. Microbiol. 1991, 137, 2017-2023.
40. Bocking, S. P.; Wiebe, M. G.; Robson, G. D.; Hansen, K.; Christiansen, L. H.; Trinci, A. P. J. Effect of branch frequency in Aspergillus oryzae on protein secretion and culture viscosity. Biotechnol. Bioeng. 1999, 65, 638-648.
41. Chalfie, M.; Tu, Y.; Euskirchen, G. G.; Ward, W. W. and Prasher, D. C. Green fluorescent protein as a marker for gene expression. Science 1994, 263, 725-888.
42. Poeggeler S.; Masloff S.; Hoff B.; Mayrhofer S.; Kueck U. Versatile EGFP reporter plasmids for cellular localization of recombinant gene products in filamentous fungi. Curr. Genet. 2003, 43, 54-61.
43. Heim, R.; Cubitt, A. B.; Tsien, R. Y. Improved green fluorescence. Nature 1995, 373, 663-664.
44. Siedenberg, D.; Mestric, S.; Ganzlin, M.; Schmidt, M.; Punt, P. J.; van den Hondel, C. A. M. J. J.; Rinas, U. GlaA promoter controlled production of a mutant green fluorescent protein (S65T) by recombinant Aspergillus niger during growth on defined medium in batch and fed-batch cultures. Biotechnol. Prog. 1999, 15, 43-50.
45. Xu, J.; Wang, L.; Ridgway, D.; Gu, T.; Moo-Young, M. Increased heterologous protein production in Aspergillus niger fermentation through extracellular proteases inhibition by pelleted growth. Biotechnol. Prog. 2000, 16, 222-227.
46. van Hartingsveldt, W.; Mattern, I. E.; Van Zeijil, C. M. J.; Pouwels, P. H.; van den Hondel, C. A. M. J. J. Development of a homologous transformation system for Aspergillus niger based on the pyrG gene. Mol. Gen. Genet. 1987, 206, 71-75.
47. Withers, J. M.; Swift, R. J.; Wiebe, M. G.; Robson, G. D.; Punt, P. J.; van den Hondel, C. A. M. J. J.; Trinci, A. P. J. Optimization and stability of glucoamylase production by recombinant strains of Aspergillus niger in chemostat culture. Biotechnol. Bioeng. 1998, 59, 407-418.
48. Vogel, H. J. A convenient growth medium for Neurospora (Medium N). Microb. Genet. Bull. 1956, 256, 112-119.
49. Smith, D. C.; Wood, T. M. Xylanase production by Aspergillus awamori. Development of a medium and optimization of the fermentation parameters for the production of extracellular xylanase and β-xylosidase while maintaining low protease production. Biotechnol. Bioeng. 1991, 38, 883-890.
50. Holm, K. A. Automatic spectrometric determination of aminoglucosidase activity using p-nitrophenol-D-glucopyranoside and a flow injection analyzer. Analyst 1986, 111, 927-929.
51. Jimenez-Tobon, G. A; Penninckx, M. J.; Lejeune, R. The relationship between pellet size and production of Mn(II) peroxidase by Phanerochaete chrysosporium in submerged culture. Enzyme Microb. Technol. 1997, 21, 537-542.
52. Liu, H. S.; Jan, M. S.; Chou, C. K.; Chen, P. H.; Ke, N. J. Is green fluorescent protein toxic to the living cells? Biochem. Biophy. Res. Commun. 1999, 260, 712-717.
53. Calik, P.; Calik, G.; Ozdamar, T. H. Oxygen transfer effects in serine alkaline protease fermentation by Bacillus licheniformis: Use of citric acid as the carbon source. Enzyme Microb. Technol. 1998, 23, 451-461.
54. Frankena, J.; Koningstein, G. M.; Verseveld, H. W.; Stouthamer, A. H. Effect of different limitations in chemostat cultures on growth and production of extracellular protease by Bacillus licheniformis. Appl. Microbiol. Biotechnol. 1986, 24, 106-112.
55. Verdoes J. C.; Punt P. J.; van den Hondel C. A. M. J. J. Molecular genetic strain improvement for the overproduction of fungal proteins by filamentous fungi. Appl. Microbiol. Biotechnol. 1995, 43, 195-205.
56. Liu, F.; Li, W.; Ridgway, D.; Gu, T.; Moo-Young, M. Inhibition of extracellular protease secretion by Aspergillus niger using cell immobilization. Biotechnol. Lett. 1998, 20, 539-542.
57. Phillips, G. N. Jr. The three-dimensional structure of green fluorescent protein and its implications for function and design. In Green Fluorescent Protein; Chalfie, M., Steven, K., Eds.; Wiley-Liss: New York, 1998; pp 58-71.
58. Metz, B.; Kossen, N. W. F. Biotechnology review: The growth of molds in the form of pellets - a literature review. Biotechnol. Bioeng. 1977, 19, 781-790.
59. Whitaker, A.; Long, P. A. Fungal pelleting. Process Biochem. 1973, 8, 27-31.
60. Papagianni M.; Moo-Young M. Protease secretion in glucoamylase producer Aspergillus niger cultures: fungal morphology and inoculum effects. Process Biochem. 2002, 37, 1271-1278.
61. Endow, S. A.; Piston, D. W. Methods and protocols. In Green Fluorescent Protein; Chalfie, M., Steven, K., Eds; Wiley-Liss: New York, 1998; p 288.
62. Bai, FW.; Wang, LP.; Huang, HJ.; Xu, JF.; Caesar, J.; Ridgway, D.; Gu, TY.; Moo-Young, M. Oxygen mass-transfer performance of low viscosity gas-liquid-olid system in a split-cylinder airlift bioreactor. Biotechnol. Lett. 2001, 23, 1109-1113.
63. Vats P.; Sahoo D. K.; Banerjee U. C. Production of phytase (myo-inositolhexakisphosphate phosphohydrolase) by Aspergillus niger van Teighem in laboratory-scale fermenter. Biotechnol. Prog. 2004, 20, 737-743.