Microbial Ecology

, Volume 57, Issue 4, pp 757–765 | Cite as

Growth and Mating of Cryptococcus neoformans var. grubii on Woody Debris

  • A. Botes
  • T. Boekhout
  • F. Hagen
  • H. Vismer
  • J. Swart
  • A. Botha
Original Article

Abstract

A total of 36 Cryptococcus neoformans strains originating from South Africa were screened for wood degrading enzymes. All strains tested positive for cellulase activity while none where capable of xylan degradation. Three C. neoformans var. grubii strains, originating from clinical and environmental samples, representing the same genotype (VNI/AFLP1—C. neoformans var. grubii) and MATα, were evaluated for growth on debris of two common tree species in South Africa: Acacia mearnsii and Eucalyptus camaldulensis. The mating capability of all the C. neoformans strains was evaluated on similar debris. Strains grown on A. mearnsii yielded substantially greater yeast populations. A total of 26%, 6%, 46%, and 80% of the 36 C. neoformans strains tested were either able to mate or develop filaments when crossed on A. mearnsii and E. camaldulensis debris, V8 juice, and yeast carbon base (YCB) agar, respectively. Filamentation and monokaryotic fruiting was observed in 3% of strains when C. neoformans was cultured on either A. mearnsii, E. camaldulensis debris, or YCB. The results indicate that this fungus is capable of completing its life cycle and can produce basidiospores on woody debris. In the future, these findings should be considered when studying the epidemiology, microbial ecology, and proposed infection process of this global pathogen.

References

  1. 1.
    Abbott TS (ed) (1985) In: Soil testing service: methods and interpretation. NSW Department of Agriculture, SydneyGoogle Scholar
  2. 2.
    Beyers CP, Coetzer FJ (1971) Effect of concentration, pH and time on the properties of di-ammonium EDTA as a multiple soil extractant. Agrochemophysica 3:49–54Google Scholar
  3. 3.
    Blackburn TH (1983) The microbial nitrogen cycle. In: Krumbein CWE (ed) Microbial geochemistry. Blackwell, Oxford, UK, pp 63–89Google Scholar
  4. 4.
    Boekhout T, van Belkum A, Leenders ACAP, Verbrugh H, Mukamurangwa P, Swinne D, Scheffers WA (1997) Molecular typing of Cryptococcus neoformans: taxonomic and epidemiological aspects. Int J Syst Bacteriol 47:432–442PubMedCrossRefGoogle Scholar
  5. 5.
    Boekhout T, Bandoni RJ, Fell JW, Kwon-Chung KJ (1998) Discussion of teleomorphic and anamorphic genera of the heterobasidiomycetous yeasts. In: Kurtzman CP, Fell JW (eds) The yeasts, a taxonomic study. Elsevier, Amsterdam, The Netherlands, pp 609–625CrossRefGoogle Scholar
  6. 6.
    Boekhout T, Theelen B, Diaz M, Fell JW, Hop WCJ, Abeln ECA, Dromer F, Meyer W (2001) Hybrid genotypes in the pathogenic yeast Cryptococcus neoformans. Microbiol 147:891–907Google Scholar
  7. 7.
    British Columbia, Ministry of Agriculture, Food and Fisheries. Resource Management Branch (2002) Soil water storage capacity and available soil moisture. Water Conservation Factsheet (http://www.agf.gov.bc.ca/resmgmt/publist/600series/619000–1.pdf)
  8. 8.
    Bui T, Lin X, Malik R, Heitman J, Carter D (2008) Isolates of Cryptococcus neoformans from infected animals reveal genetic exchange in unisexual, α-mating type populations. Eukaryot Cell (in press)Google Scholar
  9. 9.
    Casadevall A, Steenbergen J, Nosanchuk J (2003) ‘Ready made’ virulence and ‘dual use’ virulence factors in pathogenic environment—the Cryptococcus neoformans paradigm. Curr Opinion Microbiol 6:332–337CrossRefGoogle Scholar
  10. 10.
    Chuck SL, Sande MA (1989) Infections with Cryptococcus neoformans in the acquired immunodeficiency syndrome. N Engl J Med 321:794–799PubMedGoogle Scholar
  11. 11.
    Cogliati M, Esposto MC, Clarke DL, Wickes BL, Viviani MA (2001) Origin of Cryptococcus neoformans var. neoformans diploid strains. J Clin Microbiol 39:3889–3894PubMedCrossRefGoogle Scholar
  12. 12.
    De Koker TH, Zhao J, Allsop SF, Janse BJH (2000) Isolation and enzymatic characterization of South African white rot fungi. Mycol Res 104:820–824CrossRefGoogle Scholar
  13. 13.
    Doll EC, Lucas RE (1973) Testing soils for potassium, calcium and magnesium. In: Walsh LM, Beatons JD (eds) Soil testing and plant analysis. Soil Science Society of America, Madison, WI, USA, pp 133–152Google Scholar
  14. 14.
    Ellis DH, Pfeiffer TJ (1990) Natural habitat of Cryptococcus neoformans var. gattii. J Clin Microbiol 28:1642–1644PubMedGoogle Scholar
  15. 15.
    Ellis DH, Pfeiffer TJ (1990) Ecology, life cycle and infectious propagule of Cryptococcus neoformans. Lancet 336:923–925PubMedCrossRefGoogle Scholar
  16. 16.
    Farkas VM, Liskova M, Bielly P (1985) Novel media for detection of microbial producers of cellulase and xylanase. FEMS Microbiol Lett 28:137–140CrossRefGoogle Scholar
  17. 17.
    Fertilizer Society of South Africa. (1974) Manual of soil analysis methods. FSSA publication no. 37, Fertilizer Society of South Africa, Lynnewood Ridge, Pretoria, South AfricaGoogle Scholar
  18. 18.
    Forrester DI, Schortemeyer M, Stock WD, Bauhus J, Khanna PK, Cowie AL (2007) Assessing nitrogen fixation in mixed- and single-species plantations of Eucalyptus globulus and Acacia mearnsii. Tree Physiol 27:1319–1328PubMedGoogle Scholar
  19. 19.
    Franzot SP, Fries BC, Cleare W, Casadevall A (1998) Genetic relationship between Cryptococcus neoformans var. neoformans strains of serotypes A and D. J Clin Microbiol 36:2200–2204PubMedGoogle Scholar
  20. 20.
    Fraser JA, Giles SS, Wenink EC, Geunnes-Boyer SG, Wright JR, Diezmann S, Allen A, Stajichl JE, Dietrichl FS, Perfect JR, Heitman J (2005) Same-sex mating and the origin of the Vancouver Island Cryptococcus gattii outbreak. Nature 437:1360–1364PubMedCrossRefGoogle Scholar
  21. 21.
    Halliday C, Bui T, Krockenberger M, Malik R, Ellis D, Carter D (1999) Presence of α and a mating types in environmental and clinical isolates of Cryptococcus neoformans var. gatti strains from Australia. J Clin Microbiol 37:2920–2926PubMedGoogle Scholar
  22. 22.
    Halliday CL, Carter DA (2003) Clonal reproduction and limited dispersal in an environmental population of Cryptococcus neoformans var. gattii isolates from Australia. J Clin Microbiol 41:703–711PubMedCrossRefGoogle Scholar
  23. 23.
    Hiremath SS, Chowdhary A, Kowshik T, Randhawa HS, Sun S, Xu J (2008) Long-distance dispersal and recombination in environmental populations of Cryptococcus neoformans var. grubii from India. Microbiol 154:1513–1524CrossRefGoogle Scholar
  24. 24.
    Kwon-Chung KJ (1975) A new genus, Filobasidiella, the perfect state of Cryptococcus neoformans. Mycologia 61:1197–1200CrossRefGoogle Scholar
  25. 25.
    Kwon-Chung KJ (1998) Filobasidiella Kwon-Chung. In: Kurtzman CP, Fell JW (eds) The yeasts, a taxonomic study. Elsevier, Amsterdam, The Netherlands, pp 656–662CrossRefGoogle Scholar
  26. 26.
    Kwon-Chung KJ, Bennett JE (1984) Epidemiologic differences between the two varieties of Cryptococcus neoformans. Am J Epidemiol 120:123–130PubMedGoogle Scholar
  27. 27.
    Lazéra MS, Pires FDA, Camillo-Coura L, Nishikawa MM, Bezerra CCF, Trilles L, Wanke B (1996) Natural habitat of Cryptococcus neoformans var. neoformans in decaying wood forming hollows in living trees. J Med Vet Mycol 34:127–131PubMedCrossRefGoogle Scholar
  28. 28.
    Lengeler KB, Cox GM, Heitman J (2001) Serotype AD strains of Cryptococcus neoformans are diploid or aneuploid and are heterozygous at the mating-type locus. Infect Immun 69:115–122PubMedCrossRefGoogle Scholar
  29. 29.
    Lin X, Hull CM, Heitman J (2005) Sexual reproduction between partners of the same mating type in Cryptococcus neoformans. Nature 434:1017–1021PubMedCrossRefGoogle Scholar
  30. 30.
    Litvinseva AP, Thakur R, Vilgalys R, Mitchell TG (2006) Multilocus sequence typing reveals three genetic subpopulations of Cryptococcus neoformans var. grubii (Serotype A), including a unique population in Botswana. Genetics 172:2223–2238CrossRefGoogle Scholar
  31. 31.
    Loftus BJ, Fung E, Roncaglia P, Rowley D, Amedeo P, Bruno D, Vamathevan J, Miranda M, Anderson IJ, Fraser JA, Allen JE, Bosdet IE, Brent MR, Chiu R, Doering TL, Donlin MJ, D’Souza CA, Fox DS, Grinberg V, Fu J, Fukushima M, Haas BJ, Huang JC, Janbon G, Jones SJ, Koo HL, Krzywinski MI, Kwon-Chung JK, Lengeler KB, Maiti R, Marra MA, Marra RE, Mathewson CA, Mitchell TG, Pertea M, Riggs FR, Salzberg SL, Schein JE, Shvartsbeyn A, Shin H, Shumway M, Specht CA, Suh BB, Tenney A, Utterback TR, Wickes BL, Wortman JR, Wye NH, Kronstad JW, Lodge JK, Heitman J, Davis RW, Fraser CM, Hyman RW (2005) The genome of the basidiomycetous yeast and human pathogen Cryptococcus neoformans. Science 307:1321–1324PubMedCrossRefGoogle Scholar
  32. 32.
    McClelland CM, Chang YC, Varma A, Kwon-Chung KJ (2003) Uniqueness of the mating system in Cryptococcus neoformans. Trends in Microbiol 12:208–212CrossRefGoogle Scholar
  33. 33.
    Min KL, Kim YH, Kim YW, Jung HS, Hah YC (2001) Characterization of a novel laccase produced by the wood-rotting fungus Phellinus ribis. Arch Biochem Biophys 392:279–286PubMedCrossRefGoogle Scholar
  34. 34.
    Mitchell TG, Perfect JR (1995) Cryptococcosis in the era of AIDS—100 years after the discovery of Cryptococcus neoformans. Clin Microbiol Rev 8:515–548PubMedGoogle Scholar
  35. 35.
    Nathan SS (2006) The use of Eucalyptus tereticornis Sm. (Myrtaceae) oil (leaf extract) as a natural larvicidal agent against the malaria vector Anopheles stephensi Liston (Diptera: Culicidae). Bioresour Tech 98:1856–1860Google Scholar
  36. 36.
    Neilson JB, Fromtling RA, Bulmer GS (1977) Cryptococcus neoformans: size range of infectious particles from aerosolized soil. Infect Immun 17:634–638PubMedGoogle Scholar
  37. 37.
    Nelson DW, Sommers LE (1982) Total carbon, organic carbon and organic matter. In: Page AL (ed) Methods of soil analysis, part 2. American Society of Agronomy, Madison, WI, USA, p 199Google Scholar
  38. 38.
    Nielsen K, De Obaldia AL, Heitman J (2007) Cryptococcus neoformans mates on pigeon guano: implications for the realized ecological niche and globalization. Eukaryot Cell 6:949–959PubMedCrossRefGoogle Scholar
  39. 39.
    Randhawa HS, Mussa AY, Khan ZU (2000) Decaying wood in tree trunk hollows as a natural substrate for Cryptococcus neoformans and other yeast-like fungi of clinical importance. Mycopathologia 151:63–69CrossRefGoogle Scholar
  40. 40.
    Ren P, Springer DJ, Behr MJ, Samsonoff WA, Chaturvedi S, Chaturvedi V (2006) Transcription factor STE12α has distinct roles in morphogenesis, virulence, and ecological fitness of the primary pathogenic yeast Cryptococcus gattii. Eukaryot Cell 6:1065–1080CrossRefGoogle Scholar
  41. 41.
    Saul N, Krockenberger M, Carter D (2008) Evidence of recombination in mixed-mating-type and α-only populations of Cryptococcus gattii sourced from single eucalyptus tree hollows. Eukaryot Cell 7:727–734PubMedCrossRefGoogle Scholar
  42. 42.
    Smith AH, Imlay JA, Mackie RI (2003) Increasing the oxidative stress response allows Escherichia coli to overcome inhibitory effects of condensed tannins. Appl Environ Microbiol 69:3406–3411PubMedCrossRefGoogle Scholar
  43. 43.
    Sorrell T, Ellis D (1997) Ecology of Cryptococcus neoformans. Rev Iberoam Microbiol 14:42–43Google Scholar
  44. 44.
    Thomas GW, Peaslee DE (1973) Testing for soil phosphorus. In: Walsh LM, Beatons JD (eds) Soil testing and plant analysis. Soil Science Society of America, Madison, WI, USA, pp 15–122Google Scholar
  45. 45.
    Trilles L, Lazéra M, Wanke B, Theelen B, Boekhout T (2003) Genetic characterization of environmental isolates of the Cryptococcus neoformans species complex from Brazil. Med Mycol 41:383–390PubMedCrossRefGoogle Scholar
  46. 46.
    Tscharke RL, Lazéra M, Chang YC, Wickes BL, Kwon-Chung KJ (2003) Haploid fruiting in Cryptococcus neoformans is not mating type α-specific. Fung Gen Biol 39:230–237CrossRefGoogle Scholar
  47. 47.
    Wickes BL, Mayorga ME, Edman U, Edman JC (1996) Dimorphism and haploid fruiting in Cryptococcus neoformans: association with the α-mating type. Prot Natl Acad Sci U S A 93:7327–7331CrossRefGoogle Scholar
  48. 48.
    Xue C, Tada Y, Dong X, Heitman J (2007) The human fungal pathogen Cryptococcus can complete its sexual cycle during a pathogenic association with plants. Cell Host Microbe 1:246–248CrossRefGoogle Scholar
  49. 49.
    Yarrow D (1998) Methods for isolation, maintenance and identification of yeasts. In: Kurtzman CP, Fell JW (eds) The yeasts, a taxonomic study. Elsevier, Amsterdam, The Netherlands, pp 77–98CrossRefGoogle Scholar
  50. 50.
    Zhu X, Gibbons J, Garcia-Rivera J, Casadevall A, Williamson PR (2001) Laccase of Cryptococcus neoformans is a cell wall-associated virulence factor. Infect Immun 69:5589–5596PubMedGoogle Scholar

Copyright information

© Springer Science+Business Media, LLC 2008

Authors and Affiliations

  • A. Botes
    • 1
  • T. Boekhout
    • 2
  • F. Hagen
    • 2
  • H. Vismer
    • 3
  • J. Swart
    • 4
  • A. Botha
    • 1
  1. 1.Department of MicrobiologyStellenbosch UniversityStellenboschSouth Africa
  2. 2.Centraalbureau voor SchimmelculturesUtrechtThe Netherlands
  3. 3.Medical Research CouncilPROMEC UnitTygerbergSouth Africa
  4. 4.Department of Forest and Wood ScienceStellenbosch UniversityStellenboschSouth Africa

Personalised recommendations