Colonial Growth of Fungi

  • Stefan Olsson
Part of the The Mycota book series (MYCOTA, volume 8)

Abstract

In a previous review in Volume I of this Series, entitled “The Mycelium as an Integrated Entity”, Trinci et al. (1994) treated hyphae and the mycelium from the viewpoint of growing and branching hyphae and linked these and other cellular processes to growth kinetics of the mycelium. The current chapter will focus on this integrated entity — the manifestation of fungal colony growth as the growth of a multicellular integrated organism — and consider how this organism has been studied in different growth systems and how it coordinates activities such as nutrient uptake and reallocation. The discussion revolves around plate cultures of fungi but soil plates more reminiscent of fungi in nature are also examined.

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References

  1. Andrews JH (1998) Bacteria as modular organisms. Annu Rev Microbiol 52:105–126PubMedCrossRefGoogle Scholar
  2. Axelrod DE (1972) Kinetics of differentiation of conidiophores and conidia by colonies of Aspergillus nidulans, J Gen Microbiol 73:181–184PubMedGoogle Scholar
  3. Axelrod DE, Gealt M, Pastushok M (1973) Gene control of developmental competence in Aspergillus nidulans, Dev Biol 34:9–15PubMedCrossRefGoogle Scholar
  4. Bartnicki-Garcia S (1990) Role of vesicles in apical growth and a new mathematical model of hyphal morphogenesis. In: Heath IB (ed) Tip growth in plant and fungal cells. Academic Press, London, pp 211–232Google Scholar
  5. Beadle GW, Tatum EL (1941) Genetic control of biochemical reactions in Neurospora, Proc Natl Acad Sci USA 27:499–506PubMedCrossRefGoogle Scholar
  6. Ben-Jacob E, Cohen I, Gutnick GL (1998) Cooperative organization of bacterial colonies: from genotype to morphotype. Annu Rev Microbiol 52:779–806PubMedCrossRefGoogle Scholar
  7. Bending GD, Read DR (1995) The structure and function of the vegetative mycelium of ectomycorrhizal plants. V. The foraging behavior of ectomycorrhizal mycelium and the translocation of nutrients from exploited organic matter. New Phytol 130:401–409CrossRefGoogle Scholar
  8. Boddy L (1999) Saprotrophic cord-forming fungi: meeting the challenge of heterogeneous environments. Mycologia 91:13–32CrossRefGoogle Scholar
  9. Bolton RG, Boddy L (1993) Characterization of the spatial aspects of foraging mycelial cord systems using fractal geometry. Mycol Res 97:762–768CrossRefGoogle Scholar
  10. Brown AJP, Gow NAR (1999) Regulatory networks controlling Candida albicans morphogenesis. Trends Microbiol 7:333–338PubMedCrossRefGoogle Scholar
  11. Buller AHR (1931) Social organisation in Coprinus sterquilinus and other fungi. In: Researches on Fungi IV Hafner, New York, pp 139–186Google Scholar
  12. Butler GM (1984) Colony ontogeny in basidiomycetes. In: Jennings DH, Rayner ADM (eds) The Ecology and the Physiology of the Fungal Mycelium. Cambridge Univ Press, Cambridge, pp 53–71Google Scholar
  13. Cairney JWG (1992) Translocation of solutes in ectomycorrhizal and saprotrophic rhizomorphs. Mycol Res 96:135–141CrossRefGoogle Scholar
  14. Cairney JWG, Burke RM (1996) Physiological heterogeneity within fungal mycelia: an important concept for a functional understanding of the ectomycorrhizal symbiosis. New Phytol 134:685–695CrossRefGoogle Scholar
  15. Cooper KM, Tinker PB (1981) Translocation and transfer of nutrients in vesicular-arbuscular mycorrhizas. IV. Effect of environmental variables on movement of phosphorus. New Phytol 88:327–339CrossRefGoogle Scholar
  16. Davidson FA (1998) Modelling the qualitative response of fungal mycelia to heterogeneous environments. J Theor Biol 195:281–292PubMedCrossRefGoogle Scholar
  17. Davidson FA, Olsson S (2000) Translocation induced outgrowth of fungi in nutrient-free environments. J Theor Biol 205:73–84PubMedCrossRefGoogle Scholar
  18. Davidson FA, Sleeman BD, Rayner ADM, Crawford JW, Ritz K (1996) Context-dependent macroscopic patterns in growing and interacting mycelial networks. Proc R Soc Lond B Biol Sci 263:873–880CrossRefGoogle Scholar
  19. Dawson CG, Rayner ADM, Boddy L (1988) The form and outcome of mycelial interactions involving cord-forming decomposer basidiomycete in homogeneous and heterogeneous environments. New Phytol 109:423–432CrossRefGoogle Scholar
  20. Donnelly DP, Boddy L (1997) Development of mycelial systems of Stropharia caerulea and Phanaerochaete velutina on soil: effect of temperature and water potential. Mycol Res 101:705–713CrossRefGoogle Scholar
  21. Donnelly DP, Boddy L (1998) Repeated damage results in polarised development of foraging mycelial systems of Phanerochaete velutina, FEMS Microbiol Ecol 26:101–108CrossRefGoogle Scholar
  22. Donnelly DP, Wilkins MF, Boddy L (1995) An integrated image analysis approach for determining biomass, radial extent and box-count fractal dimension in macroscopic mycelial systems. Binary 7:19–28Google Scholar
  23. Donnelly DP, Boddy L, Wilkins MF (1999) Image analysis — a valuable tool for recording and analysing development of mycelial systems. Mycologist 13:120–125CrossRefGoogle Scholar
  24. Finlay RD, Read DJ (1986) The structure and function of the vegetative mycelium of ectomycorrhizal plants. I. Translocation of 14C-labelled carbon between plants interconnected by a common mycelium. New Phytol 103:143–156CrossRefGoogle Scholar
  25. Gealt M, Axelrod AE (1974) Coordinate regulation of enzyme inducibility and developmental competence in Aspergillus nidulans, Dev Biol 41:224–232PubMedCrossRefGoogle Scholar
  26. Gorbushina AA, Krumbein WE, von Ossietzky C (1999) The poikilotrophic micro-organism and its environment. In: Seckbach J (ed) Enigmatic microorganisms and life in extreme environments. Kluwer, Dordrecht, pp 175–185CrossRefGoogle Scholar
  27. Gort AS, Imlay JA (1998) Balance between endogenous superoxide stress and antioxidant defences. J Bacteriol 180:1402–1410PubMedGoogle Scholar
  28. Hansberg W, De-Groot H, Helmut S (1993) Reactive oxygen species associated with cell differentiation in Neurospora crassa, Free Radic Biol Med 14:287–293PubMedCrossRefGoogle Scholar
  29. Hawksworth DL, Kirk PM, Sutton BC, Pegler DN (1995) Ainsworth and Bisby’s dictionary of fungi, 8th edn. CAB International, WallingfordGoogle Scholar
  30. Hughes CL, Boddy L (1994) Translocation of 32P between wood resources recently colonised by mycelial cord systems of Phanaerochaete velutina, FEMS Microbiol Ecol 14:201–212CrossRefGoogle Scholar
  31. Jennings DH (1994) Translocation in mycelia. In: Wessels JGH, Meinhardt F (eds) The Mycota, vol I. Growth, differentiation and sexuality. Springer, Berlin Heidelberg New York, pp 163–173Google Scholar
  32. Kotov V, Reshetnikov S (1990) A stochastic model for early mycelial growth. Mycol Res 94:577–586CrossRefGoogle Scholar
  33. Lilly WW, Higgins SM, Wallweber GJ (1990) Uptake and translocation of 2-aminoisobutyric acid by Schizophyllum-commune, Exp Mycol 14:169–177CrossRefGoogle Scholar
  34. Lilly WW, Wallweber GJ, Higgins SM (1991) Proteolysis and amino acid recycling during nitrogen deprivation in Schizophyllum-commune, Curr Microbiol 23:27–32CrossRefGoogle Scholar
  35. Lindahl BJ, Stenlid J, Olsson S, Finlay R (1999) Translocation of 32P between interacting mycelia of Hypholoma fasciculare and ectomycorrhizal fungi in microcosm systems. New Phytol 144:183–193CrossRefGoogle Scholar
  36. Mihail JD, Obert M, Bruhn JN, Taylor SJ (1995) Fractal geometry of diffuse mycelia and rhizomorphs of Armillaria species. Mycol Res 99:81–88CrossRefGoogle Scholar
  37. Navarro-Bordonaba J, Adams TH (1994) Development of conidia and fruiting bodies in ascomycetes. In: Wessels JGH, Meinhardt F (eds) The Mycota, vol I. Growth, differentiation and sexuality. Springer, Berlin Heidelberg New York, pp 333–350Google Scholar
  38. Obert M (1994) Microbial growth patterns: fractal and kinetic characteristics of patterns generated by a computer model to simulate fungal growth. Fractals 1:354–374CrossRefGoogle Scholar
  39. Obert M, Pfeifer P, Sernetz M (1990) Microbial growth patterns described by fractal geometry. J Bacteriol 172:1180–1185PubMedGoogle Scholar
  40. Olsson S (1994) Uptake of glucose and phosphorus by growing colonies of Fusarium oxysporum as quantified by image analysis. Exp Mycol 18:33–47CrossRefGoogle Scholar
  41. Olsson S (1995) Mycelial density profiles of fungi on heterogeneous media and their interpretation in terms of nutrient reallocation patterns. Mycol Res 99:143–153CrossRefGoogle Scholar
  42. Olsson S (1999) Nutrient translocation and electric signalling in mycelia. In: Gow NAR, Robson GD, Gadd GM (eds) The Fungal Colony. Cambridge Univ Press, Cambridge, pp 25–48CrossRefGoogle Scholar
  43. Olsson S, Gray SN (1998) Patterns and dynamics of 32P-phosphate and labelled 2-aminoisobutyric acid (14C-AIB) translocation in intact basidiomycete mycelia. FEMS Microbiol Ecol 26:109–120CrossRefGoogle Scholar
  44. Olsson S, Jennings DH (1991a) Evidence for diffusion being the mechanism of translocation in the hyphae of three molds. Exp Mycol 15:303–309Google Scholar
  45. Olsson S, Jennings DH (1991b) A glass fiber filter technique for studying nutrient uptake by fungi: the technique used on colonies grown on nutrient gradients of carbon and phosphorus. Exp Mycol 15:292–301CrossRefGoogle Scholar
  46. Olsson S, Nordbring-Hertz B (1986) Microsclerotial germination of Verticillium dahliae as affected by rape rhizosphere. FEMS Microbiol Ecol 31:293–300CrossRefGoogle Scholar
  47. Pastushok M, Axelrod DE (1976) Effect of glucose, ammonium and media maintenance on the time of conidio-phore initiation by surface colonies of Aspergillus nidulans, J Gen Microbiol 94:221–224PubMedGoogle Scholar
  48. Persson C, Olsson S, Jansson H-B (2000) Growth of Arthrobotrys superba from a birch wood resource base into soil determined by radioactive tracing. FEMS Microbiol Ecol 31:47–51PubMedCrossRefGoogle Scholar
  49. Pérez-Martín J, Uría JA, Johnson AD (1999) Phenotypic switching in Candida albicans is controlled by a SIR2 gene. EMBO J 18:2580–2592PubMedCrossRefGoogle Scholar
  50. Pirt SJ (1967) A kinetic study of the mode of growth of surface colonies of bacteria and fungi. J Gen Microbiol 66:137–143Google Scholar
  51. Prosser JI, Trinci APJ (1979) A model for hyphal growth and branching. J Gen Microbiol 111:153–164PubMedGoogle Scholar
  52. Radford DR, Challacombe SJ, Walter JD (1994) A scanning electron microscopy investigation of the structure of colonies of different morphologies produced by phenotypic switching of Candida albicans, J Med Microbiol 40:416–423PubMedCrossRefGoogle Scholar
  53. Ramsdale M (1999) Circadian rhythms in filamentous fungi. In: Gow NAR, Robson GD, Gadd GM (eds) The fungal colony. Cambridge Univ Press, Cambridge, pp 75–107CrossRefGoogle Scholar
  54. Rayner ADM (1991) The challenge of the individualistic mycelium. Mycologia 83:48–71CrossRefGoogle Scholar
  55. Rayner ADM (1996) Interconnectedness and individualism in fungal mycelia. In: Sutton BC (ed) A century of mycology. Cambridge Univ Press, Cambridge, pp 193–232Google Scholar
  56. Rayner ADM, Griffith GS, Ainsworth AM (1995) Mycelial interconnectedness. In: Gow NAR, Gadd GM (eds) The growing fungus. Chapman and Hall, London, pp 21–40CrossRefGoogle Scholar
  57. Regalado CM, Crawford JW, Ritz K, Sleeman BD (1996) The origins of spatial heterogeneity in vegetative mycelia: a reaction-diffusion model. Mycol Res 100:1138–1142CrossRefGoogle Scholar
  58. Ritz K (1995) Growth responses of some soil fungi to spatially heterogeneous nutrients. FEMS Microbiol Ecol 16:269–280CrossRefGoogle Scholar
  59. Ritz K, Crawford JW (1990) Quantification of the fractal nature of colonies of Trichoderma viride, Mycol Res 94:1138–1141CrossRefGoogle Scholar
  60. Ritz K, Crawford JW (1999) Colony development in nutritionally heterogeneous environments. In: Gow NAR, Robson GD, Gadd GM (eds) The Fungal Colony. Cambridge Univ Press, Cambridge, pp 49–74CrossRefGoogle Scholar
  61. Ritz K, Millar SM, Crawford JW (1996) Detailed visualisation of hyphal distribution in fungal mycelia growing in heterogeneous nutritional environments. J Microbiol Methods 25:23–28CrossRefGoogle Scholar
  62. Robson GD, Bell SD, Kuhn PJ, Trinci APJ (1987) Glucose and penicillin concentrations in the medium below fungal colonies. J Gen Microbiol 133:361–367PubMedGoogle Scholar
  63. Robson GD, Kuhn PJ, Trinci APJ (1991) Antagonism by sugars of the effects of validamycin a on growth and morphology of Rhizoctonia cerealis, Mycol Res 95:129–134CrossRefGoogle Scholar
  64. Roze LV, Linz JE (1998) Lovastatin triggers an apoptosis-like cell death process in the fungus Mucor racemosus, Fungal Genet Biol 25:119–133PubMedCrossRefGoogle Scholar
  65. Ryan FJ, Beadle GW, Tatum EL (1943) The tube method of measuring the growth rate of Neurospora, Am J Bot 30:784–799CrossRefGoogle Scholar
  66. Schütte KH (1956) Translocation in the fungi. New Phytol 55:164–182CrossRefGoogle Scholar
  67. Sessom DB, Lilly WW (1986) Derepressible proteolytic activity in homokaryotic hyphae of Schizophyllum commune, Exp Mycol 10:294–300CrossRefGoogle Scholar
  68. Shapiro JA (1998) Thinking about bacterial populations as multicellular organisms. Annu Rev Microbiol 52:81–104PubMedCrossRefGoogle Scholar
  69. Shepherd VA, Orlovich DA, Ashford AE (1993a) A dynamic continuum of pleiomorphic tubules and vacuoles in growing hyphae of a fungus. J Cell Sci 104:495–507Google Scholar
  70. Shepherd VA, Orlovich DA, Ashford AE (1993b) Cell-to-cell transport via motile tubules in growing hyphae of a fungus. J Cell Sci 105:1173–1178PubMedGoogle Scholar
  71. Slutsky B, Buffo J, Soll DR (1985) High-frequency switching of colony morphology in Candida albicans, Science 230:666–669PubMedCrossRefGoogle Scholar
  72. Thrane C, Olsson S, Nielsen TH, SØrensen J (1999) Vital fluorescent stains for detection of fungal stress in Pythium ultimum and Rhizoctonia solani challenged with viscosinamide from Pseudomonas fluorescence DR54. FEMS Microbiol Ecol 30:11–23CrossRefGoogle Scholar
  73. Timonen S, Finlay RD, Olsson S, Söderström B (1996) Dynamics of phosphorus translocation in intact ectomycorrhizal systems: non-destructive monitoring using beta-scanner. FEMS Microbiol Ecol 19:171–180Google Scholar
  74. Toledo VJA, Hansberg W (1994) Enzyme inactivation related to a hyperoxidant state during conidiation of Neurospora crassa, Microbiology 140:2391–2397PubMedCrossRefGoogle Scholar
  75. Toledo VPR, Hansberg W (1995) Redox inbalance at the start of each morphogenetic step of Neurospora crassa conidiation. Arch Biochem Biophys 319:519–524PubMedCrossRefGoogle Scholar
  76. Trinci APJ, Wiebe MG, Robson GD (1994) The mycelium as an integrated entity. In: Wessels JGH, Meinhardt F (eds) The Mycota, vol I. Growth, differentiation and sexuality. Springer, Berlin Heidelberg New York, pp 175–194Google Scholar
  77. Trinci APJ, Bocking S, Swift RJ, Withers JM, Robson GD, Weibe MG (1999) Growth, branching and enzyme production by filamentous fungi in submerged culture. In: Gow NAR, Robson GD, Gadd GM (eds) The Fungal Colony. Cambridge Univ Press, Cambridge, pp 108–125CrossRefGoogle Scholar
  78. Wells JM, Boddy L, Donnelly DP (1998a) Temporary phosphorus partitioning in mycelial systems of the cord-forming basidiomycete Phanerochaete velutina, New Phytol 140:283–293CrossRefGoogle Scholar
  79. Wells JM, Boddy L, Donnelly DP (1998b) Wood decay and phosphorus translocation by the cord-forming basidiomycete Phanaerochaete velutina: the significance of local nutrient supply. New Phytol 138:607–617CrossRefGoogle Scholar
  80. Wiebe MG, Trinci APJ, Cunliffe B, Robson GD, Oliver SG (1991) Appearance of morphological colonial mutants in glucose-limited continuous flow cultures of Fusarium graminearum a3–5. Mycol Res 95:1284–1288CrossRefGoogle Scholar
  81. Wiebe MG, Robson GD, Trinci APJ, Oliver SG (1992) Characterization of morphological mutants generated spontaneously in glucose-limited continuous flow cultures of Fusarium graminearum a3–5. Mycol Res 96:555–562CrossRefGoogle Scholar

Copyright information

© Springer-Verlag Berlin Heidelberg 2001

Authors and Affiliations

  • Stefan Olsson
    • 1
  1. 1.Department of EcologyRoyal Veterinary and Agricultural UniversityFrederiksberg C, CopenhagenDenmark

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