Skip to main content
SpringerLink
Log in

Morphology and productivity of filamentous fungi

  • Mini-Review
  • Published:
Applied Microbiology and Biotechnology Aims and scope Submit manuscript

Abstract

Cultivation processes involving filamentous fungi have been optimised for decades to obtain high product yields. Several bulk chemicals like citric acid and penicillin are produced this way. A simple adaptation of cultivation parameters for new production processes is not possible though. Models explaining the correlation between process-dependent growth behaviour and productivity are therefore necessary to prevent long-lasting empiric test series. Yet, filamentous growth consists of a complex microscopic differentiation process from conidia to hyphae resulting in various macroscopically visible appearances. Early approaches to model this morphologic development are recapitulated in this review to explain current trends in this area of research. Tailoring morphology by adjusting process parameters is one side of the coin, but an ideal morphology has not even been found. This article reviews several reasons for this fact starting with nutrient supply in a fungal culture and presents recent advances in the investigation of fungal metabolism. It illustrates the challenge to unfold the relationship between morphology and productivity.

This is a preview of subscription content, log in via an institution to check access.

Access this article

Log in via an institution

Price excludes VAT (USA)
Tax calculation will be finalised during checkout.

Instant access to the full article PDF.

Institutional subscriptions

Fig. 1
Fig. 2

Similar content being viewed by others

References

  • Abarca ML, Accensi F, Cano J, Cabañes FJ (2004) Taxonomy and significance of black aspergilli. Antonie Van Leeuwenhoek 86:33–49

    CAS  PubMed  Google Scholar 

  • Adams HL, Thomas CR (1988) The use of image analysis for morphological measurements on filamentous microorganisms. Biotechnol Bioeng 32(5):707–712

    CAS  PubMed  Google Scholar 

  • Allen DG, Robinson CW (1990) Measurement of rheological properties of filamentous fermentation broths. Chem Eng Sci 45:37–48

    CAS  Google Scholar 

  • Alvarez-Vasquez F, Gonzales-Alcon C, Torres NV (2000) Metabolism of citric acid production by Aspergillus niger: model definition, steady state analysis and constrained optimization of citric acid production rate. Biotechnol Bioeng 70:82–108

    CAS  PubMed  Google Scholar 

  • Amanullah A, Christensen LH, Hansen K, Nienow AW, Thomas CR (2002) Dependence of morphology on agitation intensity in fed-batch cultures of Aspergillus oryzae and its implications for recombinant protein production. Biotechnol Bioeng 77(7):815–826

    CAS  PubMed  Google Scholar 

  • Amanullah A, Jüsten P, Davies A, Paul GC, Nienow AW, Thomas CR (2000) Agitation induced mycelial fragmentation of Aspergillus oryzae and Penicillium chrysogenum. Biochem Eng J 5:109–114

    CAS  PubMed  Google Scholar 

  • Amanullah A, Leonildi E, Nienow AW, Thomas CR (2001) Dynamics of mycelia aggregation in cultures of Aspergillus oryzae. Bioprocess Biosyst Eng 24:101–107

    CAS  Google Scholar 

  • Ayazi Shamlou P, Makagiansar HY, Ison AP, Lilliy D, Thomas CR (1994) Turbulent breakage of filamentous microorganisms in submerged culture in mechanically stirred bioreactors. Chem Eng Sci 49(16):2621–2631

    CAS  Google Scholar 

  • Bachewich C, Heath IB (1998) Radial F-actin arrays precede new hypha formation in Saprolegnia: implications for establishing polar growth and regulating tip morphogenesis. J Cell Sci 111:2005–2016

    CAS  PubMed  Google Scholar 

  • Bergter F (1978) Kinetic model of mycelial growth. Z Allg Mikrobiol 18(2):143–145

    CAS  PubMed  Google Scholar 

  • Bocking SP, Wiebe MG, Robson GD, Hansen K, Christiansen LH, Trinci APJ (1999) Effect of branch frequency in Aspergillus oryzae on protein secretion and culture viscosity. Biotechnol Bioeng 65(6):638–648

    CAS  PubMed  Google Scholar 

  • Borchert M, Libra JA (2001) Decolorization of reactive dyes by the white and rot fungus Trametes versicolor in sequencing bath reactors. Biotechnol Bioeng 57:313–321

    Google Scholar 

  • Bowen AR, Chen-Wu JL, Momany M, Young R, Szaniszlo PJ, Robbins PW (1992) Classification of fungal chitin synthases. Proc Natl Acad Sci USA 89(2):519–523

    CAS  PubMed  Google Scholar 

  • Brakhage AA (1998) Molecular regulation of β-lactam biosynthesis in filamentous fungi. Microbiol Mol Biol Rev 62(3):547–585

    CAS  PubMed  PubMed Central  Google Scholar 

  • Brakhage AA, Spröte PQ A-A, Gehrke A, Plattner H, Tüncher A (2004) Regulation of penicillin biosynthesis in filamentous fungi. Adv Biochem Eng Biotechnol 88:45–90

    CAS  PubMed  Google Scholar 

  • Broekhuijsen MP, Mattern IE, Contreras R, Kinghorn JR, van den Hondel CAMJJ (1993) 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-hIL6 fusion protein. J Biotechnol 31:135–145

    CAS  PubMed  Google Scholar 

  • Brown CM, Hugh JS (1965) Elongation of yeast cells in continuous culture. Nature 206(985):676–678

    CAS  PubMed  Google Scholar 

  • Caldwell IY, Trinci APJ (1973) The growth unit of the mould Geotrichum candidum. Arch Mikrobiol 88(1):1–10

    CAS  PubMed  Google Scholar 

  • Carter BLA, Bull AT (1971) The effect of oxygen tension in the medium on the morphology and growth kinetics of Aspergillus nidulans. J Gen Microbiol 65:265–273

    Google Scholar 

  • Charles M (1978) Technical aspects of the rheological properties of microbial cultures. Adv Biochem Eng Biotechnol 8:1–62

    CAS  Google Scholar 

  • Clark DS, Ito K, Horitsu H (1966) Effect of manganese and other heavy metals on submerged citric acid fermentation of molasses. Biotechnol Bioeng 8:465–471

    CAS  Google Scholar 

  • Conesa A, Punt PJ, Luijk Nv, Hondel CAMJJvd (2001) The secretion pathway in filamentous fungi: a biotechnological view. Fungal Genet Biol 33(3):155–171

    CAS  PubMed  Google Scholar 

  • Cox PW, Thomas CR (1992) Classification and measurement of fungal pellets by automated image analysis. Biotechnol Bioeng 39:945–952

    CAS  PubMed  Google Scholar 

  • Cui YQ, Lans RGJMvd, Luyben KCAM (1997) Effect of agitation intensities on fungal morphology of submerged fermentation. Biotechnol Bioeng 55(5):715–726

    CAS  PubMed  Google Scholar 

  • Cui YQ, Lans RGJMvd, Luyben KCAM (1998) Effects of dissolved oxygen tension and mechanical forces on fungal morphology in submerged fermentation. Biotechnol Bioeng 57(4):409–419

    CAS  PubMed  Google Scholar 

  • David H, Akesson M, Nielsen J (2003) Reconstruction of the central carbon metabolism of Aspergillus niger. Eur J Biochem 270(21):4243–4253

    CAS  PubMed  Google Scholar 

  • Dickman MB, Yarden O (1999) Serin/threonine protein kinases and phosphatases in filamentous fungi. Fungal Genet Biol 26(2):99–117

    CAS  PubMed  Google Scholar 

  • Dunn-Coleman NS, Bloebaum P, Berka RM, Bodie E, Robinson N, Armstrong G, Ward M, Przetak M, Carter GL, LaCost R (1991) Commercial levels of chymosin production by Aspergillus. Nat Biotechnol 9(10):976–981

    CAS  Google Scholar 

  • Edwards JS, Palsson BO (2000) The Escherichia coli MG 1655 in silico metabolic genotype: its definition, characteristics, and capabilities. Proc Natl Acad Sci USA 97:5528–5533

    CAS  PubMed  Google Scholar 

  • Elander RP (2003) Industrial production of βlactam antibiotics. Appl Microbiol Biotechnol 61:385–392

    CAS  PubMed  Google Scholar 

  • El-Enshasy HA, Hellmuth K, Rinas U (1999) Fungal morphology in submerged cultures and its relation to glucose oxidase excretion by recombinant Aspergillus niger. Appl Biochem Biotechnol 81(1):1–11

    CAS  PubMed  Google Scholar 

  • Emerson S (1950) The growth phase in Neurospora corresponding to the logarithmic phase in unicellular organisms. J Bacteriol 60(3):221–223

    CAS  PubMed  PubMed Central  Google Scholar 

  • Escamilla Silva EM, Gutierrez GF, Dendooven L, Jiménez IH, Ochoa-Tapia JA (2001) A method to evaluate the isothermal effectiveness factor for dynamic oxygen into mycelial pellets in submerged cultures. Biotechnol Prog 17:95–103

    Google Scholar 

  • Evers ME, Trip H, van den Berg MA, Bovenberg RAL, Driessen AJM (2004) Compartmentalization and transport in β-lactam antibiotics biosynthesis. Adv Biochem Eng Biotechnol 88:111–137

    CAS  PubMed  Google Scholar 

  • Fatile IA (1985) Rheological characteristics of suspensions of Aspergillus niger: correlations of rheological parameters with microbial concentration and shape of the mycelial aggregate. Appl Microbiol Biotechnol 21:60–64

    Google Scholar 

  • Finkelstein DB (1987) Improvement of enzyme production in Aspergillus. Antonie Van Leeuwenhoek 53(5):349–352

    CAS  PubMed  Google Scholar 

  • Förster J, Famili I, Fu P, Palsson BO, Nielsen J (2003) Genome-scale reconstruction of the Saccharomyces cerevisiae metabolic network. Genome Res 13:244–253

    PubMed  PubMed Central  Google Scholar 

  • Fu Y-C, Zhang TC, Bishop PL (1994) Determination of effective oxygen diffusivity in biofilms grown in a completely mixed biodrum reactor. Water Sci Technol 29(10–11):455–462

    CAS  Google Scholar 

  • Fujita M, Iwahori K, S. T, Yamakawa K (1994) Analysis of pellet formation of Aspergillus niger based on shear-stress. J Ferment Bioeng 78(5):368–373

    CAS  Google Scholar 

  • Fujiwara M, Horiuchi H, Ohta A, Takagi M (1997) A novel fungal gene encoding chitin synthase with a myosin motor-like domain. Biochem Biophys Res Comm. 236(1):75–78

    CAS  PubMed  Google Scholar 

  • Ganzlin M (2000) Untersuchungen der induzierten proteinproduktion unter kontrolle des glucoamylasepromotors in Aspergillus niger. Doctoral thesis, Braunschweig: Technische Universität Carolo-Wilhelmina

  • Gerngross TU (2004) Advances in the production of human therapeutic proteins in yeast and filamentous fungi. Nat Biotechnol 22(11):1409–1414

    CAS  PubMed  Google Scholar 

  • Gooday GW (1994) Cell Walls. In: Gow NAR, Gadd GM (eds) The growing fungus. Chapman & Hall, London, p 43–62

    Google Scholar 

  • Grimm LH, Kelly S, Hengstler J, Göbel A, Krull R, Hempel DC (2004) Kinetic studies on the aggregation of Aspergillus niger conidia. Biotechnol Bioeng 87(2):213–218

    CAS  PubMed  Google Scholar 

  • Grimm LH, Kelly S, Völkerding II, Krull R, Hempel DC (in press) Influence of mechanical stress and surface interaction on the aggregation of Aspergillus niger conidia. Biotechnol Bioeng

  • Guebel DV, Darias NVT (2001) Optimization of the citric acid production by Aspergillus niger through a metabolic flux balance model. Electron J Biotechnol 4:1–17

    Google Scholar 

  • Gupta JK, Helding LD, Jorgensen OB (1976) Effect of sugars, hydrogen ion concentration and ammonium nitrate on the formation of citric acid by Aspergillus niger. Acta Microbiol 23:63–67

    CAS  Google Scholar 

  • Habison A, Kubicek CP, Röhr M (1979) Phosphofructokinase as a regulatory enzyme in citric acid producing Aspergillus niger. FEMS Microbiol Lett 5:39–42

    CAS  Google Scholar 

  • Hamanaka T, Higashiyama K, Fujikawa S, Park EY (2001) Mycelial pellet intrastructure and visualization of mycelia and intracellular lipid in a culture of Mortierella alpina. Appl Microbiol Biotechnol 56:233–238

    CAS  PubMed  Google Scholar 

  • Han JR, An CH, Yuan JM (2005) Solid-state fermentation of cornmeal with the basidiomycete Ganoderma lucidum for degrading starch and upgrading nutritional value. J Appl Microbiol 99:910–915

    CAS  PubMed  Google Scholar 

  • Haq IU, Ali S, Qadeer MA, Iqbal J (2002) Effect of copper ions on mould morphology and citric acid productivity by Aspergillus niger using molasses based media. Process Biochem 37:1085–1090

    CAS  Google Scholar 

  • Harris SD, Hamer L, Sharpless KE, Hamer JE (1997) The Aspergillus nidulanssepA gene encodes an FH 1/2 protein involved in cytokinesis and the maintenance of cellular polarity. EMBO J 16(12):3474–3483

    CAS  PubMed  PubMed Central  Google Scholar 

  • Harris SD, Hofman AF, Tedford HW, Lee MP (1999) Identification and characterization of genes required for hyphal morphogenesis in filamentous fungus Aspergillus nidulans. Genetics 151:1015–1025

    CAS  PubMed  PubMed Central  Google Scholar 

  • Hellendoorn L, Mulder H, Heuvel JCvd, Ottengraf SPP (1998) Intrinsic kinetic parameters of the pellet forming fungus Aspergillus awamori. Biotechnol Bioeng 58(5):478–485

    CAS  PubMed  Google Scholar 

  • Hille A, Neu TR, Hempel DC, Horn H (in press) Oxygen profiles and biomass distribution in biopellets of Aspergillus niger. Biotechnol Bioeng

  • Honecker S, Bisping B, Yang Z, Rehm HJ (1989) Influence of sucrose concentration and phosphate limitation on citric acid production by immobilized cells of Aspergillus niger. Appl Microbiol Biotechnol 31:17–24

    CAS  Google Scholar 

  • Howard RJ, Aist JR (1980) Cytoplasmic microtubules and fungal morphogenesis: ultrastructural effects of methyl benzimidazole-2-ylcarbamate determined by freeze-substitution of hyphal tip cells. J Cell Biol 87(1):55–64

    CAS  PubMed  Google Scholar 

  • Huang MY, Bungay HR (1973) Microprobe measurements of oxygen concentrations in mycelial pellets. Biotechnol Bioeng 24:1193–1197

    Google Scholar 

  • Jackson SL, Heath IB (1993) Roles of calcium ions in hyphal tip growth. Microbiol Rev 57(2):367–382

    CAS  PubMed  PubMed Central  Google Scholar 

  • Johansen CL, Coolen L, Hunik JH (1998) Influence of morphology on product formation in Aspergillus awamori during submerged fermentations. Biotechnol Prog 14:233–240

    CAS  PubMed  Google Scholar 

  • Josten V, Lokman C, van den Hondel CAMJJ, Punt PJ (2003) The production of antibody fragments and antibody fusion proteins by yeast and filamentous fungi. Microbial Cell Factories 2(1):1–15

    Google Scholar 

  • Jungebloud A, Bohle K, Goecke Y, Haesner M, Cordes C, Horn H, Hempel DC. (2005) Quantification of product- specific gene expression in biopellets of A niger with real-time PCR. Anal. Chem: submitted

  • Jüsten P, Paul GC, Nienow AW, Thomas CR (1996) Dependence of mycelial morphology on impeller type and agitation intensity. Biotechnol Bioeng 52(6):672–684

    PubMed  Google Scholar 

  • Kaminskyj SGW, Hamer JE (1998) hyp loci control cell pattern formation in the vegetative mycelium of Aspergillus nidulans. Genetics 148:669–680

    CAS  PubMed  PubMed Central  Google Scholar 

  • Kanaly RA, Kim IS, Hur H-G (2005) Biotransformation of 3-methyl-4-nitrophenol, a main product of the insecticide fenitrothion, by Aspergillus niger. J Agric Food Chem 53:6426–6431

    CAS  PubMed  Google Scholar 

  • Kelly S, Grimm LH, Hengstler J, Schultheis E, Krull R, Hempel DC (2004) Agitation effects on submerged growth and product formation of Aspergillus niger. Bioprocess Biosyst Eng 26(5):315–323

    CAS  PubMed  Google Scholar 

  • Kossen NWF (2000) The morphology of filamentous Fungi. Adv Biochem Eng Biotechnol 70:1–34

    CAS  PubMed  Google Scholar 

  • Kristiansen B, Sinclair CG (1979) Production of citric acid in continuous culture. Biotechnol Bioeng 21:297–315

    CAS  Google Scholar 

  • Kubicek CP, Röhr M (1977) Influence of manganese on enzyme synthesis and citric acid accumulation by Aspergillus niger. Eur J Appl Microbiol 4:167–173

    CAS  Google Scholar 

  • Li ZJ, Shukla V, Wenger KS, Fordyce AP, Pedersen AG, Marten MR (2002) Effects of increased impeller power in a production-scale Aspergillus oryzae fermentation. Biotechnol Prog 18(3):437–444

    CAS  PubMed  Google Scholar 

  • Madhani HD, Fink GR (1998) The control of filamentous differentiation and virulence in fungi. Trends Cell Biol 8(9):348–353

    CAS  PubMed  Google Scholar 

  • Maeda H, Yamagata Y, Abe K, Hasegawa F, Machida M, Ishioka R, Gomi K, Nakajima T (2005) Purification and characterization of a biodegradable plastic-degrading enzyme from Aspergillus oryzae. Appl Microbiol Biotechnol 67:778–788

    CAS  PubMed  Google Scholar 

  • Magnuson JK, Lasure LL (2004) Organic acid production by filamentous fungi. In: Tkacz JS, Lange L (eds) Advances in fungal bio/technology for industry, agriculture and medicine. Springer, Berlin Heidelberg New York, p 307–340

    Google Scholar 

  • Makagiansar HY, Ayazi Shamlou P, Thomas CR, Lilliy MD (1993) The influence of mechanical forces on the morphology and penicillin production of Penicillium chrysogenum. Bioprocess Eng 9(2–3):83–90

    CAS  Google Scholar 

  • Maras M, Die Iv, Contreras R, Hondel CAMJJvd (1999) Filamentous fungi as production organisms for glycoproteins of bio-medical interest. Glycoconj J 16(2):99–107

    CAS  PubMed  Google Scholar 

  • McIntyre M, Müller C, Dynesen J, Nielsen J (2001) Metabolic engineering of the morphology of Aspergillus. Adv Biochem Eng Biotechnol 73:103–128

    CAS  PubMed  Google Scholar 

  • Metz B, Bruijn EWd, Suijdam JCv (1981) Method for quantitative representation of the morphology of molds. Biotechnol Bioeng 23:149–162

    Google Scholar 

  • Metz B, Kossen NWF (1977) The growth of molds in the form of pellets—a literature review. Biotechnol Bioeng 14:781–799

    Google Scholar 

  • Metz B, Kossen NWF, Suijdam JCv (1979) The rheology of mould suspensions. Adv Biochem Eng Biotechnol 11:104–56

    Google Scholar 

  • Meyerhoff J, Bellgardt K-H (1995) Two mathematical models for the development of a single microbial pellet, part II. Bioprocess Eng 12:315–322

    CAS  Google Scholar 

  • Meyerhoff J, Tiller V, Bellgardt K-H (1995) Two mathematical models for the development of a single microbial pellet. Part I: detailed morphological model based on the description of individual hyphae. Bioprocess Eng 12:305–313

    CAS  Google Scholar 

  • Momamy M, Taylor I (2000) Landmarks in the early duplication cycles of Aspergillus fumigatus and Aspergillus nidulans: polarity, germ tube emergence and septation. Microbiology 146:3279–3284

    Google Scholar 

  • Morita S, Kuriyama M, Nakatsu M, Kitano K (1994) High level expression of Fusarium alkaline protease gene in Acremonium chrysogenum. Biosci Biotechnol Biochem 58(4):627–630

    CAS  PubMed  Google Scholar 

  • Müller C, McIntyre M, Hansen K, Nielsen J (2002) Metabolic engineering of the morphology of Aspergillus oryzae by altering chitin synthesis. Appl Environ Microbiol 68(4):1827–1836

    PubMed  PubMed Central  Google Scholar 

  • Müller C, Spohr A, Nielsen J (2000) Role of substrate concentration in mitosis and hyphal extension of Aspergillus. Biotechnol Bioeng 67:390–397

    PubMed  Google Scholar 

  • Nielsen J (1993) A simple morphologically structured model describing the growth of filamentous microorganisms. Biotechnol Bioeng 41(7):715–727

    CAS  PubMed  Google Scholar 

  • Nielsen J, Krabben P (1995) Hyphal growth and fragmentation of Penicillium chrysogenum in submerged cultures. Biotech Bioeng 46(6):588–598

    CAS  Google Scholar 

  • Northrop FD, Ljubojevic S, Davies JM (1997) Influence of Na and anions on the dimorphic transition of Candida albicans. Microbiology 143:3757–3765

    CAS  PubMed  Google Scholar 

  • Olsvisk ES, Kristiansen B (1994) Rheology of filamentous fermentations. Biotechnol Adv 12:1–39

    Google Scholar 

  • Papagianni M (2004) Fungal morphology and metabolite production in submerged mycelial processes. Biotechnol Adv 22:189–259

    CAS  PubMed  Google Scholar 

  • Papagianni M, Mattey M, Kristiansen B (1998) Citric acid production and morphology of Aspergillus niger as functions of the mixing intensity in a stirred tank and a tubular loop bioreactor. Biochem Eng J 2(3):197–205

    CAS  Google Scholar 

  • Papagianni M, Mattey M, Kristiansen B (1999) The influence of glucose concentration on citric acid production and morphology of Aspergillus niger in batch and glucostat culture. Enzyme Microb Technol 25:710–717

    CAS  Google Scholar 

  • Papagianni M, Moo-Young M (2002) Protease secretion in glucoamylase producer Aspergillus niger cultures: fungal morphology and inoculum effects. Process Biochem 37:1271–1278

    CAS  Google Scholar 

  • Parton RM, Fischer S, Malhó R, Papasouliotis O, Jelitto TC, Leonard T, Read ND (1997) Pronounced cytoplasmic pH gradients are not required for tip growth in plant and fungal cells. J Cell Sci 110:1187–1198

    CAS  PubMed  Google Scholar 

  • Paul GC, Kent A, Thomas CR (1993) Viability testing and characterization of germination of fungal spores by automatic image analysis. Biotechnol Bioeng 42(1):11–23

    CAS  PubMed  Google Scholar 

  • Paul GC, Thomas CR (1998) Characterisation of mycelial morphology using image analysis. In: Scheper T (ed) Advances in biochemical engineering biotechnology. Springer, Berlin Heidelberg New York, p 2–59

    Google Scholar 

  • Peksel A, Torres NV, Liu J, Juneau G, Kubicek CP (2002) 13C-NMR analysis of glucose metabolism during citric acid production by Aspergillus niger. Appl Microbiol Biotechnol 58:157–163

    CAS  PubMed  Google Scholar 

  • Pons MN, Vivier H (1998) Beyond filamentous species. In: Scheper T (ed) Advances in biochemical engineering biotechnology. Springer, Berlin Heidelberg New York, p 61–93

    Google Scholar 

  • Prosser JI, Trinci APJ (1979) A model of hyphal growth and branching. J Gen Microbiol 111(1):153–164

    CAS  PubMed  Google Scholar 

  • Punt PJ, Biezen vN, Conesa A, Albers A, J. M, Hondel CAvd (2002) Filamentous fungi as cell factories for heterologous protein production. Trends Biotechnol 20:200–206

    CAS  PubMed  Google Scholar 

  • Radzio R, Kück U (1997) Synthesis of biotechnologically relevant heterologous proteins in filamentous fungi. Process Biochem 32(6):529–539

    CAS  Google Scholar 

  • Reissig JL, Kinney SG (1983) Calcium as a branching signal in Neurosporacrassa. J Bacteriol 154(3):1397–1402

    CAS  PubMed  PubMed Central  Google Scholar 

  • Riley GL, Tucker KG, Paul GC, Thomas CR (2000) Effect of biomass concentration and mycelial morphology on fermentation broth rheology. Biotechnol Bioeng 68(2):160–172

    CAS  PubMed  Google Scholar 

  • Rinas U, El-Enshasy HA, Emmler M, Hille A, Hempel DC, Horn H (2005) Model-based prediction of substrate conversion and protein synthesis and excretion in recombinant Aspergillus niger biopellets. Chem Eng Sci 60:2729–2739

    CAS  Google Scholar 

  • Robson GD, Wiebe MG, Trinci APJ (1991) Exogenous cAMP and cGMP modulate branching in Fusarium graminearum. J Gen Microbiol 137(4):963–969

    CAS  PubMed  Google Scholar 

  • Schmidt FR (2004) Recombinant expression systems in the pharmaceutical industry. Appl Microbiol Biotechnol 65:363–372

    CAS  PubMed  Google Scholar 

  • Shu P, Johnson MG (1984) Citric acid production by submerged fermentation with Aspergillus niger. Ind Eng Chem 40(7):1202–1205

    Google Scholar 

  • Smedsgaard J, Nielsen J (2005) Metabolite profiling of fungi and yeast: from phenotype to metabolome by MS and informatics. J Exp Bot 56(410):273–286

    CAS  PubMed  Google Scholar 

  • Sonneborn A, Bockmühl DP, Gerads M, Kurpanek K, Sanglard D, Ernst JF (2000) Protein kinase A encoded by TPK2 regulates dimorphism of Candida albicans. Mol Microbiol 35(2):386–396

    CAS  PubMed  Google Scholar 

  • Spohr A, Dam- Mikkelsen C, Carlsen M, Nielsen J, Villadsen J (1998) On-line study of fungal morphology during submerged growth in a small flow-through cell. Biotechnol Bioeng 58(5):541–543

    CAS  PubMed  Google Scholar 

  • Suijdam JCv, Metz B (1981) Influence of engineering variables upon the morphology of filamentous molds. Biotechnol Bioeng 23(1):111–148

    Google Scholar 

  • Sumathi S, Manju BS (2000) Uptake of reactive textile dyes by Aspergillus foetidus. Enzyme Microb Technol 27:347–355

    CAS  PubMed  Google Scholar 

  • Taylor JW (1995) Making the Deuteromycota redundant: a practical integration of mitosporic and meiosporic fungi. Can J Bot 73:754–759

    Google Scholar 

  • Torralba S, Raudaskoski M, Pedregosa AM, Laborda F (1998) Effect of cytochalasin A on apical growth, action cytoskeleton organization and enzyme secretion in Aspergillus nidulans. Microbiology 144(Pt1):45–53

    CAS  PubMed  Google Scholar 

  • Trinci APJ (1974) A study of the kinetics of hyphal extension and branch initiation of fungal mycelia. J Gen Microbiol 81(1):225–236

    CAS  PubMed  Google Scholar 

  • Tucker KG, Thomas CR (1993) Effect of biomass concentration and morphology on the rheological parameters of Penicillum chrysogenum fermentation broths. Trans Inst Chem Eng 71:111–117

    CAS  Google Scholar 

  • Valkonen M, Ward M, Wang H, Pentttila M, Salonheimo M (2003) Improvenment of foreign-protein production in Aspergillus niger var. awamori by constitutive induction of the unfolded-protein response. Appl Environ Microbiol 69(12):6979–6986

    CAS  PubMed  PubMed Central  Google Scholar 

  • Vanhoutte B, Pons MN, Thomas CR, Louvel L, Vivier H (1995) Characterization of Penicillium chrysogenum physiology in submerged cultures by color and monochrome image analysis. Biotechnol Bioeng 48(1):1–11

    CAS  PubMed  Google Scholar 

  • Ward M, Lin C, Victoria DC, Fox BP, Fox JA, Wong DL, Meerman HJ, Pucci JP, Fong RB, Heng MH et al (2004) Characterization of humanized antibodies secreted by Aspergillus niger. Appl Environ Microbiol 70(5):2567–2576

    CAS  PubMed  PubMed Central  Google Scholar 

  • Wiebe MG, Karandikar A, Robson GD, Trinci APJ, Candia JF, Trapp S, Wallis G, Rinas U, Derkx PMF, Madrid SM et al (2001) Production of tissue plasminogen activator (t-PA) in Aspergillus niger. Biotechnol Bioeng 76(2):164–174

    CAS  PubMed  Google Scholar 

  • Wittler R, Baumgartl H, Lübbers DW, Schügerl K (1986) Investigations of oxygen transfer into Penicillium chrysogenum pellets by microprobe measurements. Biotechnol Bioeng 28:1024–1036

    CAS  Google Scholar 

  • Wongwicharn A, McNeil B, Harvey LM (1999) Effect of oxygen enrichment on morphology, growth, and heterologous protein production in chemostat cultures of Aspergillus niger B1-D. Biotechnol Bioeng 65(4):416–424

    CAS  PubMed  Google Scholar 

  • Wösten HAB, Moukha SM, Sietsma JH, Wessels JGH (1991) Localization of growth and secretion of proteins in Aspergillus niger. J Gen Microbiol 137(1):2017–2023

    PubMed  Google Scholar 

  • Xiang X, Morris NR (1999) Hyphal tip growth and nuclear migration. Curr Opin Microbiol 2(6):636–640

    CAS  PubMed  Google Scholar 

  • Xu DB, Madrid CP, Röhr M, Kubicek CP (1989) The influence of type and concentration of the carbon source on production of citric acid by Aspergillus niger. Appl Microbiol Biotechnol 30:553–558

    CAS  Google Scholar 

  • Yang H, King R, Reichl U, Gilles ED (1992a) Mathematical model for apical growth, septation, and branching of mycelial microorganisms. Biotechnol Bioeng 39(1):49–58

    CAS  PubMed  Google Scholar 

  • Yang H, Reichel U, King R, Gilles ED (1992b) Measurement and simulation of the morphological development of filamentous microorganisms. Biotechnol Bioeng 39(1):44–48

    CAS  PubMed  Google Scholar 

  • Zhang TC, Bishop PL (1994) Evaluation of tortuosity factors and effective diffusivities in biofilms. Water Res 28(11):2279–2287

    CAS  Google Scholar 

Download references

Acknowledgement

Financial support was provided by the German Research Foundation (DFG) through the collaborative research centre SFB 578 - “From gene to product” at the TU Braunschweig.

Author information

Authors and Affiliations

  1. Institute of Biochemical Engineering, Technical University of Braunschweig, Gauβstrasse 17, 38106, Braunschweig, Germany

    L. H. Grimm, S. Kelly, R. Krull & D. C. Hempel

Authors
  1. L. H. Grimm
    View author publications

    You can also search for this author in PubMed Google Scholar

  2. S. Kelly
    View author publications

    You can also search for this author in PubMed Google Scholar

  3. R. Krull
    View author publications

    You can also search for this author in PubMed Google Scholar

  4. D. C. Hempel
    View author publications

    You can also search for this author in PubMed Google Scholar

Corresponding author

Correspondence to D. C. Hempel.

Rights and permissions

Reprints and permissions

About this article

Cite this article

Grimm, L.H., Kelly, S., Krull, R. et al. Morphology and productivity of filamentous fungi. Appl Microbiol Biotechnol 69, 375–384 (2005). https://doi.org/10.1007/s00253-005-0213-5

Download citation

  • Received:

  • Revised:

  • Accepted:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1007/s00253-005-0213-5

Keywords

Search

Navigation