Characterization and control of fungal morphology for improved production performance in biotechnology

Journal of Biotechnology

Volumn 163, Issue 2, 2013, Pages 112-123

  Krull, Rainer ^a   Wucherpfennig, Thomas ^a   Esfandabadi, Manely Eslahpazir ^a   Walisko, Robert ^a   Melzer, Guido ^a   Hempel, Dietmar C ^a   Kampen, Ingo ^a   Kwade, Arno ^a   Wittmann, Christoph ^a  

^a TECHNICAL UNIVERSITY OF BRAUNSCHWEIG   (Germany)

Author keywords

Environome; Filamentous microorganisms; Image analysis; Morphology; Mycel and pellet growth; Rheology

Indexed keywords

BIOPROCESSES; ENVIRONOME; FILAMENTOUS FUNGI; FILAMENTOUS MICROORGANISMS; FUNGAL MORPHOLOGY; FUNGAL SPORES; INDUSTRIAL BIOTECHNOLOGY; MICRO-PARTICLES; MORPHOLOGICAL PROPERTIES; OSMOLALITY; PH VALUE; POWER INPUT; PRECISE CONTROL; PROCESS PARAMETERS; PRODUCTION PERFORMANCE; QUANTITATIVE ESTIMATES; SPHERICAL PELLETS; SUBMERGED CULTURES; TOOLS AND TECHNIQUES; TRANSFER CHARACTERISTICS;

BIOTECHNOLOGY; FUNGI; IMAGE ANALYSIS; OPTIMIZATION; PELLETIZING; RHEOLOGY; SURFACE PROPERTIES;

MORPHOLOGY;

ARTICLE; ATOMIC FORCE MICROSCOPY; BIOTECHNOLOGY; CONFOCAL LASER MICROSCOPY; CONTACT ANGLE; DIGITAL IMAGING; FLOW CYTOMETRY; FLOW KINETICS; FLUORESCENCE LIFETIME IMAGING MICROSCOPY; FLUORESCENCE MICROSCOPY; FOCUSED BEAM REFLECTANCE MEASUREMENT; FUNGAL LIFE CYCLE STAGE; FUNGUS; FUNGUS CULTURE; FUNGUS GROWTH; FUNGUS HYPHAE; FUNGUS SPORE; INDUSTRIAL PRODUCTION; LASER DIFFRACTION TECHNIQUE; MICROELECTRODE; MYCELIUM; NONHUMAN; OSMOLALITY; PELLET SLICING; PH MEASUREMENT; PRIORITY JOURNAL; SEDIMENTATION; ZETA POTENTIAL;

BIOENGINEERING; BIOTECHNOLOGY; FUNGI; INDUSTRIAL MICROBIOLOGY; MYCELIUM;

FUNGI;

EID: 84872192827     PISSN: 01681656     EISSN: 18734863     Source Type: Journal    
DOI: 10.1016/j.jbiotec.2012.06.024     Document Type: Article

References (126)

1. Ahamed A., Vermette P. Effect of culture medium composition on Trichoderma reesei's morphology and cellulase production. Bioresource Technology 2009, 100:5979-5987.
2. Amanullah A., Christensen L.H., Hansen K., Nienow A.W., Thomas C.R. Dependence of morphology on agitation intensity in fed-batch cultures of Aspergillus oryzae and its implications for recombinant protein production. Biotechnology and Bioengineering 2002, 77:815-826.
3. Archer D.B. Filamentous fungi as microbial cell factories for food use. Current Opinion in Biotechnology 2000, 11:478-483.
4. Arfsten J., Leupold S., Bradtmöller C., Kampen I., Kwade A. Atomic force microscopy studies on the nanomechanical properties of Saccharomyces cerevisiae. Colloids and Surfaces B: Biointerfaces 2010, 79:284-290.
5. Aynsley M., Ward A.C., Wright A.R. A mathematical model for the growth of mycelial fungi in submerged culture. Biotechnology and Bioengineering 1990, 35:820-830.
6. Barry D.J., Cecilia A.E., Chan A.E., Williams G.A. Morphological quantification of filamentous fungal development using membrane immobilization and automatic image analysis. Journal of Industrial Microbiology and Biotechnology 2009, 36:787-800.
7. Barry D.J., Williams G.A. Microscopic characterisation of filamentous microbes: towards fully automated morphological quantification through image analysis. Journal of Microscopy 2011, 244:1-20.
8. Bizukojc M., Ledakowicz S. Physiological, morphological and kinetic aspects of lovastatin biosynthesis by Aspergillus terreus. Biotechnology Journal 2009, 4:647-664.
9. Bizukojc M., Ledakowicz S. The morphological and physiological evolution of Aspergillus terreus mycelium in the submerged culture and its relation to the formation of secondary metabolites. World Journal of Microbiology and Biotechnology 2010, 26:41-54.
10. Bobowicz-Lassociska T., Grajek W. Changes in protein secretion of Aspergillus niger caused by the reduction of the water activity by potassium chloride. Acta Biotechnologica 1995, 15:277-287.
11. 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. Biotechnology and Bioengineering 1999, 65:638-648.
12. Caldwell I.Y., Trinci A.P. The growth unit of the mould Geotrichum candidum. Archives of Microbiology 1973, 88:1-10.
13. Carlsen M., Spohr A.B., Nielsen J., Villadsen J. Morphology and physiology of an alpha amylase producing strain of Aspergillus oryzae during batch cultivations. Biotechnology and Bioengineering 1996, 49:266-276.
14. Casas López J.L., Sánchez Pérez J.A., Fernández Sevilla J.M., Rodríguez Porcel E.M., Chisti Y. Pellet morphology, culture rheology and lovastatin production in cultures of Aspergillus terreus. Journal of Biotechnology 2005, 116:61-77.
15. Chen C.Y., Seguin-Swartz G. A rapid method for assessing the viability of fungal spores. Canadian Journal of Plant Pathology-Revue Canadienne de Phytopathologie 2002, 24:230-232.
16. Cronenberg C.C.H., Ottengraf S.P.P., van den Heuvel J.C., Pottel F., Sziele D., Schügerl K., Bellgardt K.H. Influence of age and structure of Penicillium chrysogenum pellets on the internal concentration profiles. Bioprocess Engineering 1994, 10:209-216.
17. Cui Y.Q., van der Lans R.G.J.M., Luyben K.C.A.M. Effects of dissolved oxygen tension and mechanical forces on fungal morphology in submerged fermentation. Biotechnology and Bioengineering 1998, 57:409-419.
18. Dague E., Alsteens D., Latgé J.P., Verbelen C., Raze D., Baulard A.R., Dufrêne Y.F. Chemical force microscopy of single live cells. Nano Letters 2007, 7:3026-3030.
19. Dague E., Alsteens D., Latgé J.P., Dufrêne Y.F. High-resolution cell surface dynamics of germinating Aspergillus fumigatus conidia. Biophysical Journal 2008, 94:656-660.
20. de Bekker C., van Veluw G.J., Vinck A., Wiebenga L.A., Wösten H.A.B. Heterogeneity of Aspergillus niger microcolonies in liquid shaken cultures. Applied and Environment Microbiology 2011, 77:1263-1267.
21. Deckwer W.D., Jahn D., Hempel D.C., Zeng A.P. System biology approach to bioprocess development. Life Science Engineering 2006, 6:455-469.
22. Driouch H., Sommer B., Wittmann C. Morphology engineering of Aspergillus niger for improved enzyme production. Biotechnology and Bioengineering 2010, 105:1058-1068.
23. Driouch H., Roth A., Dersch P., Wittmann C. Optimized bioprocess for production of fructofuranosidase by recombinant Aspergillus niger. Applied Microbiology and Biotechnology 2010, 87:2011-2024.
24. Driouch H., Roth A., Dersch P., Wittmann C. Filamentous fungi in good shape: microparticles for tailor-made fungal morphology and enhanced enzyme production. Bioengineered Bugs 2011, 2:100-104.
25. Driouch H., Hänsch R., Wucherpfennig T., Krull R., Wittmann C. Improved enzyme production by superior bio-pellets of Aspergillus niger - targeted morphology engineering using titanate micro particles. Biotechnology and Bioengineering 2012, 109:462-471.
26. Dufrêne Y.F. Atomic force microscopy of fungal cell walls: an update. Yeast 2010, 27:465-471.
27. Dynesen J., Nielsen J. Surface hydrophobicity of Aspergillus nidulans conidiospores and its role in pellet formation. Biotechnology Progress 2003, 19:1049-1052.
28. Emerson S. The growth phase in Neurospora corresponding to the logarithmic phase in unicellular organisms. Journal of Bacteriology 1950, 60:221-223.
29. Eslahpazir M., Wittmann C., Krull R. Computational fluid dynamics. Comprehensive Biotechnology 2011, vol. 2:1027-1038. Elsevier. second ed.
30. Fang T.H., Kang S.H., Hong Z.H., Wu C.D. Elasticity and nanomechanical response of Aspergillus niger spores using atomic force microscopy. Micron 2012, 43:407-411.
31. Fiedurek J. Effect of osmotic stress on glucose oxidase production and secretion by Aspergillus niger. Journal of Basic Microbiology 1998, 38:107-112.
32. Fujita M., Iwahori K., Tatsuta S., Yamakawa K. Analysis of pellet formation of Aspergillus niger based on shear stress. Journal of Fermentation and Bioengineering 1994, 78:368-373.
33. Galbraith J.C., Smith J.E. Filamentous growth of Aspergillus niger in submerged shake culture. Transactions of the British Mycological Society 1969, 52:237-246.
34. Gallardo-Moreno A.M., Gonzalez-Martin M.L., Perez-Giraldo C., Garduno E., Bruque J.M., Gomez-Garcia A.C. Thermodynamic analysis of growth temperature dependence in the adhesion of Candida parapsilosis to polystyrene. Applied and Environment Microbiology 2002, 68:2610-2613.
35. Gibbs P.A., Seviour R.J., Schmid F. Growth of filamentous fungi in submerged culture: problems and possible solutions. Critical Reviews in Biotechnology 2000, 20:17-48.
36. Grimm L.H., Kelly S., Hengstler J., Göbel A., Krull R., Hempel D.C. Kinetic studies on the aggregation of Aspergillus niger conidia. Biotechnology and Bioengineering 2004, 87:213-218.
37. Grimm L.H., Kelly S., Völkerding I.I., Krull R., Hempel D.C. Influence of process parameters on the aggregation of Aspergillus niger conidia. Biotechnology and Bioengineering 2005, 92:879-888.
38. Grimm L.H., Kelly S., Krull R., Hempel D.C. Morphology and productivity of filamentous fungi. Applied Microbiology and Biotechnology 2005, 49:375-384.
39. Gupta K., Mishra P., Srivastava P. A correlative evaluation of morphology and rheology of Aspergillus terreus during lovastatin fermentation. Biotechnology and Bioprocess Engineering 2007, 12:140-146.
40. Heffels C., Polke R., Radle M., Sachweh B., Schafer M., Scholz N. Control of particulate processes by optical measurement techniques. Particle and Particle Systems Characterization 1998, 15:211-218.
41. Henzler H.-J. Particle stress in bioreactors. Influence on Stress on Cell Growth and Product Formation, Series: Advances in Biochemical Engineering/Biotechnology 2000, 67:35-82. Springer-Verlag, Berlin Heidelberg, 2010.
42. Herbrich S., Gehder M., Krull R., Gericke K.H. Label-free spatial analysis of free and enzyme-bound NAD(P)H in the presence of high concentrations of melanin. Journal of Fluorescence 2012, 22:349-355.
43. Hille A., Neu T.R., Hempel D.C., Horn H. Oxygen profiles and biomass distribution in biopellets of Aspergillus niger. Biotechnology and Bioengineering 2005, 92:614-623.
44. Hille A., Neu T.R., Hempel D.C., Horn H. Einfluss der Morphologie auf Stofftransport und -umsatz in Aspergillus niger - pellets. Chemie Ingenieur Technik 2006, 78:627-632.
45. Hille A., Neu T.R., Hempel D.C., Horn H. Effect diffusivities and mass fluxes in fungal biopellets. Biotechnology and Bioengineering 2009, 103:1202-1213.
46. Hopfner T., Bluma A., Rudolph G., Lindner P., Scheper T. A review of non-invasive optical-based image analysis systems for continuous bioprocess monitoring. Bioprocess and Biosystems Engineering 2010, 33:247-256.
47. Hwang H.J., Kim S.W., Xu C.P., Choi J.W., Yun J.W. Morphological and rheological properties of the three different species of basidiomycetes Phellinus in submerged cultures. Journal of Applied Microbiology 2004, 96:1296-1305.
48. Johansen C.L., Coolen L., Hunik J.H. Influence of morphology on product formation in Aspergillus awamori during submerged fermentations. Biotechnology Progress 1998, 14:233-240.
49. Kailas L., Ratcliffe E.C., Hayhurst E.J., Walker M.G., Foster S.J., Hobbs J.K. Immobilizing live bacteria for AFM imaging of cellular processes. Ultramicroscopy 2009, 109:775-780.
50. Kaup B.A., Ehrich K., Pescheck M., Schrader J. Microparticle-enhanced cultivation of filamentous microorganisms: increased chloroperoxidase formation by Caldariomyces fumago as an example. Biotechnology and Bioengineering 2008, 99:491-498.
51. Kelly S., Grimm L.H., Hengstler J., Schultheis E., Krull R., Hempel D.C. Agitation effects on submerged growth and product formation of Aspergillus niger. Bioprocess and Biosystems Engineering 2004, 26:315-323.
52. Kelly S., Grimm L.H., Jonas R., Hempel D.C., Krull R. Effects of fluid dynamic induced shear stress on fungal growth and morphology. Process Biochemistry 2006, 41:2113-2117.
53. Kelly S., Grimm L.H., Jonas R., Hempel D.C., Krull R. Investigations of the morphogenesis of filamentous microorganisms. Engineering in Life Sciences 2006, 6:475-480.
54. Kilonzo P.M., Margaritis A. The effects of non-Newtonian fermentation broth viscosity and small bubble segregation on oxygen mass transfer in gas-lift bioreactors: a critical review. Biochemical Engineering Journal 2004, 17:27-40.
55. Krull R., Cordes C., Horn H., Kampen I., Kwade A., Neu T.R., Nörtemann B. Morphology of filamentous fungi - linking cellular biology to process engineering using Aspergillus niger. Advances in Biochemical Engineering/Biotechnology 2010, vol. 121:1-21.
56. Kües U., Rühl M. Automated image analysis to observe pellet morphology in liquid cultures of filamentous fungi such as the basidiomycete Coprinopsis cinerea. Current Trends in Biotechnology and Pharmacy 2009, 3:241-253.
57. Laflamme C., Verreault D., Lavigne S., Trudel L., Ho J., Duchaine C. Autofluorescence as a viability marker for detection of bacterial spores. Frontiers in Bioscience 2005, 10:1647-1653.
58. Lapin A., Schmid J., Reuss M. Modeling the dynamics of E. coli populations in the three-dimensional turbulent field of a stirred-tank bioreactor - a structured-segregated approach. Chemical Engineering Science 2006, 61:4783-4797.
59. Leckband D., Israelachvili J. Intermolecular forces in biology. Quarterly Reviews of Biophysics 2001, 34:105.
60. Lejeune R., Baron G.V. Effect of agitation on growth and enzyme production of Trichoderm reesei in batch fermentation. Applied Microbiology and Biotechnology 1995, 43:249-258.
61. Ley I. Assessing resolution and sensitivity in a laser diffraction particle size analyser. American Laboratory 2000, 32:33-38.
62. Li Q., Harvey L.M., McNeil B. Oxygen enrichment effects on protein oxidation, proteolytic activity and the energy status of submerged batch cultures of Aspergillus niger B1-D. Process Biochemistry 2008, 43:238-243.
63. Lin P.J., Grimm L.H., Wulkow M., Hempel D.C., Krull R. Population balance modeling of the conidial agglomeration of Aspergillus niger. Biotechnology and Bioengineering 2008, 99:341-350.
64. Lin P.J., Scholz A., Krull R. Effect of volumetric power input by aeration and agitation on pellet morphology and product formation of Aspergillus niger. Biochemical Engineering Journal 2010, 49:213-220.
65. Liu Y., Liao W., Chenet S. Study of pellet formation of filamentous fungi Rhizopus oryzae using a multiple logistic regression model. Biotechnology and Bioengineering 2008, 99:117-128.
66. Lubertozzi D., Keasling J.D. Developing Aspergillus as a host for heterologous expression. Biotechnology Advances 2009, 27:53-75.
67. Lyklema J. Electrokinetics after Smoluchowski. Colloids and Surfaces A 2003, 222:5-14.
68. Mahnke E.U., Büscher K., Hempel D.C. A novel approach for the determination of mechanical stresses in gas-liquid reactors. Chemical Engineering and Technology 2000, 23:509-513.
69. Mainwaring D.O., Wiebe M.G., Robson G.D., Goldrick M., Jeenes D.J., Archer D.B., Trinci A.P.J. Effect of pH on hen egg white lysozyme production and evolution of a recombinant strain of Aspergillus niger. Journal of Biotechnology 1999, 75:1-10.
70. Maruyama J., Kitamoto K. Differential distribution of the endoplasmic reticulum network in filamentous fungi. FEMS Microbiology Letters 2007, 272:1-7.
71. McIntyre M., Dynesen J., Nielsen J. Morphological characterization of Aspergillus nidulans: growth, septation and fragmentation. Microbiology 2001, 147:239-246.
72. Metz B., Kossen N.W.F. The growth of molds in the form of pellets - a literature review. Biotechnology and Bioengineering 1977, 19:781-799.
73. Metz B., De Bruijn E.W., van Suijdam J.C. Methods for quantitative representation of the morphology of molds. Biotechnology and Bioengineering 1981, 23:149-162.
74. Meyer V. Genetic engineering of filamentous fungi - progress, obstacles and future trends. Biotechnology Advances 2008, 26:177-185.
75. Mitard A., Riba J.P. Rheological properties of Aspergillus niger pellet suspensions. Applied Microbiology and Biotechnology 1986, 25:245-249.
76. Müller C., Hansen K., Szabo P., Nielsen J. Effect of deletion of chitin synthase genes on mycelial morphology and culture viscosity in Aspergillus oryzae. Biotechnology and Bioengineering 2003, 81:525-534.
77. Nielsen J., Krabben P. Hyphal growth and fragmentation of Penicillium chrysogenum in submerged cultures. Biotechnology and Bioengineering 1995, 46:588-598.
78. Nielsen J. Modeling the morphology of filamentous microorganisms. Trends in Biotechnology 1996, 14:438-443.
79. Nielsen J., Johansen C.L., Jacobsen M., Krabben P., Villadsen J. Pellet formation and fragmentation in submerged cultures of Penicillium chrysogenum and its relation to penicillin production. Biotechnology Progress 1995, 11:93-98.
80. Olsvik E.S., Kristiansen B. On-line rheological measurements and control in fungal fermentations. Biotechnology and Bioengineering 1992, 40:375-387.
81. Olsvik E., Kristiansen B. Rheology of filamentous fermentations. Biotechnology Advances 1994, 12:1-39.
82. Oncu S., Tari C., Unluturk S. Effect of various process parameters on morphology, rheology, and polygalacturonase production by Aspergillus sojae in a batch bioreactor. Biotechnology Progress 2007, 23:836-845.
83. Oolman T., Blanch H.W., Erickson L.E. Non-Newtonian fermentation systems. Critical Reviews in Biotechnology 1986, 4:133-184.
84. Osherov N., May G.S. The molecular mechanisms of conidial germination. FEMS Microbiology Letters 2001, 199:153-160.
85. Packer H.L., Thomas C.R. Morphological measurements on filamentous microorganisms by fully automatic image analysis. Biotechnology and Bioengineering 1990, 35:870-881.
86. Papagianni M., Mattey M., Kristiansen B. Citric acid production and morphology of Aspergillus niger as functions of the mixing intensity in a stirred tank and a tubular loop bioreactor. Biochemical Engineering Journal 1998, 2:197-205.
87. Papagianni M. Fungal morphology and metabolite production in submerged mycelial processes. Biotechnology Advances 2004, 22:189-259.
88. Papagianni M., Mattey M. Physiological aspects of free and immobilized Aspergillus niger cultures producing citric acid under various glucose concentrations. Process Biochemistry 2004, 39:1963-1970.
89. Park E.Y., Koizumi K., Higashiyama K. Analysis of morphological relationship between micro- and macromorphology of Mortierella species using a flow-through chamber coupled with image analysis. Journal of Eukaryotic Microbiology 2006, 53:199-203.
90. Pazouki M., Panda T. Understanding the morphology of fungi. Bioprocess and Biosystems Engineering 2000, 22:127-143.
91. Petersen N., Stocks S., Gernaey K.V. Multivariate models for prediction of rheological characteristics of filamentous fermentation broth from the size distribution. Biotechnology and Bioengineering 2008, 100:61-71.
92. Pilz R.D., Hempel D.C. Mechanical stress on suspended particles in two- and three-phase airlift loopreactors and bubble columns. Chemical Engineering Science 2005, 60:6004-6012.
93. Priegnitz B.E., Wargenau A., Brandt U., Rohde M., Dietrich S., Kwade A., Krull R., Fleissner A. The role of initial spore adhesion in pellet and biofilm formation in Aspergillus niger. Fungal Genetics and Biology 2012, 49:30-38.
94. Prosser J.I., Trinci A.P.J. A model for hyphal growth and branching. Journal of General Microbiology 1979, 111:153-164.
95. Ramkrishna D. Population Balances. Chemical Engineering 2000, vol. 1. Academic Press, San Diego.
96. Reynaga-Pena C.G., Bartnicki-Garcia S. Apical branching in a temperature sensitive mutant of Aspergillus niger. Fungal Genetics and Biology 1997, 22:153-167.
97. Riley G.L., Tucker K.G., Paul G.C., Thomas C.R. Effect of biomass concentration and mycelial morphology on fermentation broth rheology. Biotechnology and Bioengineering 2000, 68:160-172.
98. Rodri{dotless}guez Porcel E.M., Casas Lopez J.L., Sanchez Perez J.A., Fernandez Sevilla J.M., Chisti Y. Effects of pellet morphology on broth rheology in fermentations of Aspergillus terreus. Biochemical Engineering Journal 2005, 26:139-144.
99. Ryoo D., Choi C.S. Surface thermodynamics of pellet formation in Aspergillus niger. Biotechnology Letters 1999, 21:97-100.
100. Shrig P., Wissler P. Monitoring and optimisation of cooling crystallisation of vitamin C with Lasentec FBRM inline particle measurement probe. Chemie Ingenieur Technik 2001, 73:377-381.
101. Smith A.E., Moxham K.E., Middelberg A.P.J. On uniquely determining cell-wall material properties with the compression experiment. Chemical Engineering Science 1998, 53:3913-3922.
102. Spohr A., Dam-Mikkelsen C., Carlsen M., Nielsen J., Villadsen J. On-line study of fungal morphology during submerged growth in a small flowthrough cell. Biotechnology and Bioengineering 1998, 58:541-553.
103. Stintzing A., Pilz R.D., Hempel D.C., Krull R. Mechanische Beanspruchungen in Mehrphasenreaktoren. Chemie Ingenieur Technik 2008, 80:1837-1842.
104. Stocks S.M., Thomas C.R. Strength of mid-logarithmic and stationary phase Saccharopolyspora erythraea hyphae during a batch fermentation in defined nitrate-limited medium. Biotechnology and Bioengineering 2001, 73:370-378.
105. Sullivan C.J., Venkataraman S., Retterer S.T., Allison D.P., Doktycz M.J. Comparison of the indentation and elasticity of E. coli and its spheroplasts by AFM. Ultramicroscopy 2007, 107:342-934.
106. Touhami A., Jericho M.H., Beveridge T.J. Atomic force microscopy of cell growth and division in Staphylococcus aureus. Journal of Bacteriology 2004, 186:3286-3295.
107. Trinci A.P. A study of the kinetics of hyphal extension and branch initiation of fungal mycelia. Journal of General Microbiology 1974, 81:225-236.
108. Tucker K.G., Kelly T., Delgrazia P., Thomas C.R. Fully-automatic measurement of mycelial morphology by image analysis. Biotechnology Progress 1992, 8:353-359.
109. Tung J.W., Heydari K., Tirouvanziam R., Sahaf B., Parks D.R., Herzenberg L.A., Herzenberg L.A. Modern flow cytometry: a practical approach. Clinics in Laboratory Medicine 2007, 27:453-468.
110. Vadillo-Rodriguez V., Beveridge T.J., Dutcher J.R. Surface viscoelasticity of individual gram-negative bacterial cells measured using atomic force microscopy. Journal of Bacteriology 2008, 190:4225-4232.
111. Vecht-Lifshitz S.E., Magdassi S., Braun S. Pellet formation and cellular aggregation in Streptomyces tendae. Biotechnology and Bioengineering 1990, 35:890-896.
112. Villena G.K., Fujikawa T., Tsuyumu S., Gutiérrez-Correa M. Structural analysis of biofilms and pellets of Aspergillus niger by confocal laser scanning microscopy and cryo scanning electron microscopy. Bioresource Technology 2010, 101:1920-1926.
113. Wang L., Ridgway D., Gu T., Moo-Young M. Effects of process parameters on heterologous protein production in Aspergillus niger fermentation. Journal of Chemical Technology and Biotechnology 2003, 78:1259-1266.
114. Wargenau A., Kwade A. Determination of adhesion between single Aspergillus niger spores in aqueous solutions using an atomic force microscope. Langmuir 2010, 26:11071-11076.
115. Wargenau A., Fleissner A., Bolten C.J., Rohde M., Kampen I., Kwade A. On the origin of the electrostatic surface potential of Aspergillus niger spores in acidic environments. Research in Microbiology 2011, 162:1011-1017.
116. White S., et al. The autolysis of industrial filamentous fungi. Critical Reviews in Biotechnology 2002, 22:1-14.
117. Wittler R., BaumgartI H., Lübbers D.W., Schügerl K. Investigations of oxygen transfer into Penicillium chrysogenum pellets by microprobe measurements. Biotechnology and Bioengineering 1986, 28:1024-1036.
118. Wright C.J., Armstrong I.A. The application of atomic force microscopy force measurements to the characterisation of microbial surfaces. Surface and Interface Analysis 2006, 38:1419-1428.
119. Wright C.J., Shah M.K., Powell L.C., Armstrong I. Application of AFM from microbial cell to biofilm. Scanning 2010, 32:134-149.
120. Wucherpfennig T., Kiep K.A., Driouch H., Wittmann C., Krull R. Morphology and rheology in filamentous cultivations. Advances in Applied Microbiology 2010, 72:89-133.
121. Wucherpfennig T., Hestler T., Krull R. Morphology engineering - osmolality and its effect on Aspergillus niger morphology and productivity. Microbial Cell Factories 2011, 11. http://dx.doi.org/10.1186/1475-2859-10-58.
122. Xia J.Y., Wang Y., Zhang S., Chen N., Yin P., Zhuang Y., Chu J. Fluid dynamics investigation of variant impeller combinations by simulation and fermentation experiment. Biochemical Engineering Journal 2009, 43:252-260.
123. Yang S., Lewandowski Z. Measurement of local mass transfer coefficient in biofilms. Biotechnology and Bioengineering 1995, 48:737-744.
124. Zhang Z.Y., Jin B., Kelly J.M. Effects of cultivation parameters on the morphology of Rhizopus arrhizus and the lactic acid production in a bubble column reactor. Engineering for Life Sciences 2007, 7:490-496.
125. Zhao L., Schaefer D., Marten M.R. Assessment of elasticity and topography of Aspergillus nidulans spores via atomic force microscopy. Applied and Environment Microbiology 2005, 71:955-960.
126. Znidarsic P., Pavko A. The morphology of filamentous fungi in submerged cultivations as a bioprocess parameter. Food Technology and Biotechnology 2001, 39:237-252.