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Ecological Stress: Melanization as a Response in Fungi to Radiation

  • Isabella Grishkan

Introduction

Fungi are known as organisms highly adapted to their environment. Among various extremes they need to cope with when colonizing natural and man-made substrates is a high level of radiation of different kinds – solar (UV) or ionizing. In the last decades, a significant reduction in the stratospheric ozone layer has been registered, with ozone loss between 1979 and 1991 averaged around 4 ± 6% per decade at northern temperate latitudes (Hollandsworth et al. 1995). As a result, the amount of more harmful UV-B radiation (280–315 nm) reaching the Earth’s surface has increased (e.g., Kerr and McElroy 1993). In parallel, contamination of the environment by radionuclides, a source for the ionizing radiation, is also enhanced. All these man-induced environmental changes increase the necessity to withstand high radiation levels, and the protective role of dark pigmentation mainly of melanin nature in surviving and exploiting highly radiated environments is confirmed to be crucial.

Wha...

Keywords

Alternaria Alternata Cladosporium Cladosporioides Early Cretaceous Period Uppermost Soil Layer Fungal Melanin 
These keywords were added by machine and not by the authors. This process is experimental and the keywords may be updated as the learning algorithm improves.

References

  1. Abdullah SK, Al-Khesraji TO, Al-Edany TY (1986) Soil mycoflora of the Southern Desert of Iraq. Sydowia 39:8–16Google Scholar
  2. Bandaranayake W (1998) Mycosporines: are they nature’s sunscreens? Nat Prod Rep 15:159–172PubMedCrossRefGoogle Scholar
  3. Bell AA, Wheller MH (1986) Biosynthesis and function of fungal melanins. Annu Rev Phytopathol 24:411–451CrossRefGoogle Scholar
  4. Boyd-Wilson KSH, Perry JH, Walter M (1998) Persistance and survival of saprophytic fungi antagonistic to Botrytis cinerea on kiwifruit leaves. In: Proceedings of 51st New Zealand plant protection conference, Lincoln, pp 96–101Google Scholar
  5. Bull AT (1970) Inhibition of polysaccharases by melanin: enzyme inhibition in relation to mycolysis. Arch Biochem Biophys 137:345–356PubMedCrossRefGoogle Scholar
  6. Butler MJ, Day AW (1998) Fungal melanins: a review. Can J Microbiol 44:1115–1136CrossRefGoogle Scholar
  7. Christensen M (1981) Species diversity and dominance in fungal community. In: Carroll GW, Wicklow DT (eds) The fungal community, its organization and role in the ecosystem. Marcell Dekker, New York, pp 201–232Google Scholar
  8. Ciccarone C, Rambelli A (1998) A study on micro-fungi in arid areas. Notes on stress-tolerant fungi. Plant Biosystems 132:17–20Google Scholar
  9. Coelho RR, Sacramento DR, Linhares LF (1997) Amino sugars in fungal melanins and soil humic acids. Eur J Soil Sci 48:425–429CrossRefGoogle Scholar
  10. Cuadros SC, Martinez RNM, Rossi A (1999) Identification and linkage mapping of the phsA gene of Aspergillus nidulans, where mutations affects growth and pigmentation of colonies in a temperature and pH-dependent way. FEMS Microbiol Lett 171:103–106PubMedCrossRefGoogle Scholar
  11. Dadachova E, Casadevall A (2008) Ionizing radiation: how fungi cope, adapt, and exploit with the help of melanin. Curr Opin Microbiol 11:525–531PubMedCrossRefGoogle Scholar
  12. Dadachova E, Howell RW, Bryan RA, Frenkel A, Nosanchuk JD, Casadevall A (2004) Susceptibility of the human pathogenic fungi Cryptococcus neoformans and Histoplasma capsulatum to gamma-radiation versus radioimmunotherapy with alpha- and beta-emitting radioisotopes. J Nucl Med 45:313–320PubMedGoogle Scholar
  13. Dadachova E, Bryan RA, Huang X, Moadel T, Scheitzer AD, Aisin P, Nosanchuk J, Casadevall A (2007a) Ionizing radiation changes the electronic properties of melanin and enhances the growth of melanized fungi. PLoS ONE 5:1–13Google Scholar
  14. Dadachova E, Bryan RA, Howell RC, Schweitzer AD, Aisen P, Nosanchuk JD, Casadevall A (2007b) Radioprotective properties of melanin are a function of its chemical composition, free stable radical presence and spatial arrangement. Pigment Cell Melanoma Res 21:192–199CrossRefGoogle Scholar
  15. Diakumaku E, Gorbushina AA, Krumbein WE, Panina L (1995) Black fungi of marble and limestones – an aesthetical, chemical and physical problem for the conservation of monuments. Sci Total Environ 167:295–304CrossRefGoogle Scholar
  16. Durrell LW, Shields LM (1960) Fungi isolated in culture from soils of the Nevada test site. Mycologia 52:636–641CrossRefGoogle Scholar
  17. Ellis MB (1971) Dematiaceous hyphomycetes. Commonwealth Mycological Institute, Kew, SurreyGoogle Scholar
  18. Ellis MB (1976) More dematiaceous hyphomycetes. Commonwealth Mycological Institute, Kew, SurreyGoogle Scholar
  19. Ellis MB, Ellis JP (1997) Microfungi on land plants: an identification handbook. Richmond, SloughGoogle Scholar
  20. English H, Gerhardt F (1946) The effect of ultraviolet radiation on the viability of fungus spores and on the development of decay in sweet cherries. Phytopathology 36:100–111PubMedGoogle Scholar
  21. Fogarty RV, Tobin JM (1996) Fungal melanins and their interactions with metals. Enzyme Microb Technol 19:311–317PubMedCrossRefGoogle Scholar
  22. Gadd GM, Mowll JL (1985) Cooper uptake by yeast-like cells, hyphae, and chlamydospores of Aureobasidium pullulans. Exp Mycol 9:230–240CrossRefGoogle Scholar
  23. Gorbushina A (2003) Microcolonial fungi: survival potential of terrestrial vegetative structures. Astrobiology 3:543–554PubMedCrossRefGoogle Scholar
  24. Gorbushina A, Krumbien W, Volkman M (2002) Rock surface as life indicator: new ways to demonstrate life and traces of former life. Astrobiology 2:203–213PubMedCrossRefGoogle Scholar
  25. Gorbushina A, Whitehead K, Dorniede T, Niesse A, Shulte A, Hedges JI (2003) Black fungal colonies as units of survival: hyphal mycosporines synthesized by rock-dwelling microcolonial fungi. Can J Bot 81:131–138CrossRefGoogle Scholar
  26. Grishkan I, Nevo E, Wasser SP, Beharav A (2003a) Adaptive spatiotemporal distribution of soil microfungi in “Evolution Canyon” II, Lower Nahal Keziv, western Upper Galilee, Israel. Biol J Linn Soc 79:527–539CrossRefGoogle Scholar
  27. Grishkan I, Nevo E, Wasser SP (2003b) Micromycete diversity in the hypersaline Dead Sea coastal area (Israel). Mycol Progr 2(1):19–28CrossRefGoogle Scholar
  28. Grishkan I, Nevo E, Wasser SP (2004) Micromycetes from the saline Arubotaim Cave (Mount Sedom, the Dead Sea southwestern shore, Israel). J Arid Environ 57:431–443CrossRefGoogle Scholar
  29. Grishkan I, Zaady E, Nevo E (2006) Soil crust microfungi along a southward rainfall aridity gradient in the Negev desert, Israel. Eur J Soil Biol 42:33–42CrossRefGoogle Scholar
  30. Grishkan I, Beharav A, Kirzhne V, Nevo E (2007) Adaptive spatiotemporal distribution of soil microfungi in “Evolution Canyon” III, Nahal Shaharut, extreme Southern Negev desert, Israel. Biol J Linn Soc 90:263–277CrossRefGoogle Scholar
  31. Gunde-Cimerman N, Zalar P, Petrovicˇ U, Turk M, Kogej T, de Hoog GS, Plemenitasˇ A (2004) Fungi in the Salterns. In: Ventosa A (ed) Halophilic microorganisms. Springer, Heidelberg, pp 103–113Google Scholar
  32. Halwagy R, Moustafa AF, Kamel S (1982) Ecology of the soil mycoflora in the desert of Kuwait. J Arid Environ 5:109–125Google Scholar
  33. Hameed A, Awad A (2005) Vegetation: a source of air fungal biocontaminant. Aerobiologia 21:53–61CrossRefGoogle Scholar
  34. Hashem AR (1991) Studies on the fungal flora of Saudi Arabian soil. Cryptogam Botany 2(3):179–182Google Scholar
  35. Herrero AD, Ruiz SS, Bustillo MG, Morales PC (2006) Study of airborne fungal spores in Madrid, Spain. Aerobiologia 22:135–142CrossRefGoogle Scholar
  36. Hill ZH (1992) The function of melanin or 6 people examine an elephant. BioEssays 14:49–56PubMedCrossRefGoogle Scholar
  37. Hollandsworth SM, McPeters RD, Flynn LE, Planet W, Miller AJ, Chandra S (1995) Ozone trends deduced from combined Nimbus 7 SBUV and NOAA 11 SBUV/2 data. Geophys Res Lett 22:905–908CrossRefGoogle Scholar
  38. Hughes KA, Lawley B, Newsham K (2003) Solar UV-B radiation inhibits the growth of Antarctic terrestrial fungi. Appl Environ Microbiol 69:1488–1491PubMedCrossRefGoogle Scholar
  39. Hulot G, Gallet Y (2003) Do superchrons occur without any palaeomagnetic warning? Earth Planet Sci Lett 210:191–201CrossRefGoogle Scholar
  40. Johnson D (2003) Response of terrestrial microorganisms to ultraviolet-B radiation in ecosystems. Res Microbiol 154:315–320PubMedCrossRefGoogle Scholar
  41. Kerr JB, McElroy CT (1993) Evidence for large upward trends in ultraviolet-B radiation linked to ozone depletion. Science 262:1032–1034PubMedCrossRefGoogle Scholar
  42. Kul’ko AB, Marfenina OE (2001) The distribution of microscopic fungi along Moscow roads. Microbiology 70:709–713 (Engl. Transl.)PubMedGoogle Scholar
  43. Lamb BC, Helmi S, Roberts S, Adak GK, Simrack D (1992) Interactions of UVsensitivity and photoreactivation with the type and distribution of ascospore pigmentation in wild-type and mutant strains of Ascobolus immersus, Sordaria brevicollis, and Sordaria fimicola. Genet (Life Sci Adv) 11:153–160Google Scholar
  44. Levetin E, Dorsey K (2006) Contribution of leaf surface fungi to the air spora. Aerobiologia 22:3–12CrossRefGoogle Scholar
  45. Lugauskas A, Sveistyte L, Ulevicius V (2003) Concentration and species diversity of airborne fungi near busy streets in Lithuanian urban areas. Ann Agric Environ Med 10:233–239PubMedGoogle Scholar
  46. Mahmoud YA-G (2004) Uptake of radionuclides by some fungi. Mycobiology 32:110–114CrossRefGoogle Scholar
  47. Marfenina OE (1998) Do we have the “microbial risk” problem in urban ecosystems. In: Ecology of cities. Proceedings of the international conference, Rhodes, June 8–12, pp 299–305Google Scholar
  48. Mirchink TG, Kashkina GB, Abaturov ID (1972) Resistance of fungi with different pigments to radiation. Mikrobiologiia 41:83–86PubMedGoogle Scholar
  49. Money NP, Howard RJ (1996) Confirmation of a link between fungal pigmentation, turgor pressure, and pathogenicity using a new method of turgor measurement. Fungal Genet Biol 20:217–227CrossRefGoogle Scholar
  50. Mulder JL, El-Hendawy H (1999) Microfungi under stress in Kuwait’s coastal saline depressions. Kuwait J Sci Eng 26:157–172Google Scholar
  51. Old KM, Robertson WM (1970) Effects of lytic enzymes and natural soil on the fine structure of conidia of Cochliobolus sativus. Trans Br Mycol Soc 54:343–350CrossRefGoogle Scholar
  52. Onofri S, Selbmann L, de Hoog GS, Grube M, Barreca D, Ruisi S, Zucconi L (2007) Evolution and adaptation of fungi at boundaries of life. Adv Space Res 40:1657–1664CrossRefGoogle Scholar
  53. Pavlicek T, Sharon D, Kravchenko V, Saaroni H, Nevo E (2003) Microclimatic interslope differences underlying biodiversity contrasts in “Evolution Canyon”, Mt. Carmel, Israel. Isr J Earth Sci 52:1–9CrossRefGoogle Scholar
  54. Pereira PT, de Carvalho MM, Girio FM, Roseiro JC, Amaral-Collaco MT (2002) Diversity of microfungi in the phylloplane of plants growing in a Mediterranean ecosystem. J Basic Microbiol 42:396–407PubMedCrossRefGoogle Scholar
  55. Perry RS, Engel MH, Botta O, Staley JT (2003) Amino acid analysies of desert varnish fron the Sonoran and Mojave Deserts. Geomicrobiol J 20:427–438CrossRefGoogle Scholar
  56. Prospero JM, Blades E, Mathison G, Naidu R (2005) Interhemispheric transport of viable fungi and bacteria from Africa to the Caribbean with soil dust. Aerobiologia 21:1–19CrossRefGoogle Scholar
  57. Prota G (1992) Melanins and melanogenesis. Academic, San DiegoGoogle Scholar
  58. Ranzoni FV (1968) Fungi isolated in culture from soils of the Sonoran desert. Mycologia 60:356–371PubMedCrossRefGoogle Scholar
  59. Rehnstrom AL, Free SJ (1997) The isolation and characterization of melanin-deficient mutants of Monilinia fructicola. Physiol Mol Plant Pathol 49:321–330CrossRefGoogle Scholar
  60. Rizzo DM, Blanchette RA, Palmer MA (1992) Biosorption of metal ions by Armillaria rhizomorphs. Can J Bot 70:1515–1520CrossRefGoogle Scholar
  61. Rosas AL, Casadevall A (1997) Melanization effect susceptibility of Cryptococcus neoformans to heat and cold. FEMS Microbiol Lett 153:265–272PubMedCrossRefGoogle Scholar
  62. Saleh YG, Mayo MS, Ahearn DG (1988) Resistance of some common fungi to gamma irradiation. Appl Environ Microbiol 54:2134–2135PubMedGoogle Scholar
  63. Selbmann L, de Hoog GS, Mazzaglia A, Friedmann EI, Onofri S (2005) Fungi at the edge of life: cryptoendolithic black fungi from Antarctic desert. Stud Mycol 51:1–32Google Scholar
  64. Sen B, Asan A (2001) Airborne fungi in vegetable growing areas of Edirne, Turkey. Aerobiologia 17:69–75CrossRefGoogle Scholar
  65. Sghaier H, Ghedira K, Benkahla A, Barkallah I (2008) Basal DNA repair machinery is subject to positive selection in ionizingradiation-resistant bacteria. BMC Genomics 9:297–304PubMedCrossRefGoogle Scholar
  66. Shilo M (1978) Strategies of life in extreme environments. Verlag Chemie, WeinheimGoogle Scholar
  67. Singaravelan N, Grishkan I, Beharav A, Wakamatsu K, Ito Sh, Nevo E (2008) Adaptive melanin response of the soil fungus Aspergillus niger to UV radiation stress at “Evolution Canyon”, Mount Carmel, Israel. PLoS ONE 3(8):1–5CrossRefGoogle Scholar
  68. Skujins J (1984) Microbial ecology of desert soils. Adv Microb Ecol 7:49–91CrossRefGoogle Scholar
  69. Staley JT, Palmer F, Adams JB (1982) Microcolonial fungi: common inhabitans on desert rocks? Science 215:1093–1095PubMedCrossRefGoogle Scholar
  70. Sterflinger K, Krumbien WE (1995) Multiple stress factors affecting growth of rock inhabiting black fungi. Bot Acta 108:490–496Google Scholar
  71. Ulevicius V, Peciulyte D, Lugauskas A, Andriejauskiene J (2004) Field study on changes in viability of airborne fungal propagules exposed to UV radiation. Environ Toxicol 19:437–441PubMedCrossRefGoogle Scholar
  72. Urzi C, Wollenzien U, Criseo G, Krumbien WE (1995) Biodiversity of the rock inhabiting microbiota with special reference to black fungi and black yeasts. In: Allsopp D, Hawksworth DL, Colwell RR (eds) Microbial diversity and ecosystem function. Oxford University Press, New York, pp 289–302Google Scholar
  73. Van der Wal A, Bloem J, Christian M, de Boer W (2009) Relative abundance and activity of melanized hyphae in different soil ecosystems. Soil Biol Biochem 41:417–419CrossRefGoogle Scholar
  74. Van Duin D, Casadevall A, Nosanchuk JD (2002) Melanization of Cryptococcus neoformans and Histoplasma capsulatum reduces their susceptibility to amphotericin B and caspofungin. Antimicrob Agents Chemother 46:3394–3400PubMedCrossRefGoogle Scholar
  75. Waisel Y, Ganor E, Glikman M, Epstein V, Brenner S (1997) Airborne fungal spores in the coastal plain of Israel: A preliminary survey. Aerobiologia 13:281–287CrossRefGoogle Scholar
  76. Wang Y, Casadevall A (1994) Susceptibility of melanized and non-melanized Cryptococcus neoformans to nitrogen- and oxygen-derived oxidants. Infect Immun 62:3004–3007PubMedGoogle Scholar
  77. Yanagita T (1990) Natural microbial communities: ecological and physiological features. Springer, TokyoGoogle Scholar
  78. Youngchim S, Moriris-Jones R, Hay RJ, Hamilton AJ (2004) Production of melanin by Aspergillus fumigatus. J Med Microbiol 53:175–181PubMedCrossRefGoogle Scholar
  79. Zak J (2005) Fungal communities of desert ecosystems: links to climate change. In: Dighton J, White JF Jr, Oudemans P (eds) The fungal community, its organization and role in the ecosystem. CRC Press, Boca Raton, pp 659–681CrossRefGoogle Scholar
  80. Zhdanova NN, Pokhodenko VD (1973) The possible participation of a melanin pigment in the protection of fungus cell from desiccation. Microbiology 5:753–757 (Engl. Transl.)Google Scholar
  81. Zhdanova NN, Vasilevskaya AA, Sadnovikov YuS, Artishkova LA (1990) The dynamics of micromycete complexes contaminated with soil radionuclides. Mikologia I Fitopatologia 24:504–512Google Scholar
  82. Zhdanova NN, Zakharchenko VA, Veber VV (2000) Fungi from Chernobyl: mycobiota of the inner regions of the containment structures of the damaged nuclear reactor. Mycol Res 104:1421–1426CrossRefGoogle Scholar
  83. Zhdanova NN, Tugay T, Dighton J, Zheltonozhsky V, McDermott P (2004) Ionizing radiation attracts soil fungi. Mycol Res 108:1089–1096PubMedCrossRefGoogle Scholar
  84. Zhdanova NN, Zakharchenko VA, Haselwandter K (2005) Radionuclides and fungal communities. In: Dighton J, White JF Jr, Oudemans P (eds) The fungal community, its organization and role in the ecosystem. CRC Press, Baton Rouge, pp 759–768Google Scholar
  85. Zoppas BC, Valencia-Barrera RM, Duso SM, Fernandez-Gonzalez D (2006) Fungal spores prevalent in the aerosol of the city Caxias do Sul, Rio Grande do Sul, Brazil, over 2-yaer period (2001–2002). Aerobiologia 22:119–126Google Scholar

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© Springer 2011

Authors and Affiliations

  1. 1.Institute of EvolutionUniversity of HaifaHaifaIsrael

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