Polyextremotolerant black fungi: Oligotrophism, adaptive potential, and a link to lichen symbioses

Frontiers in Microbiology

Volumn 3, Issue NOV, 2012, Pages

  Gostinĉar, Cene ^a,b   Muggia, Lucia ^c,d   Grube, Martin ^a,c  

^a UNIVERSITY OF LJUBLJANA   (Slovenia)

^b Centre of Excellence for Integrated Approaches in Chemistry and Biology of Proteins   (Slovenia)

^c UNIVERSITY OF GRAZ   (Austria)

^d UNIVERSITY OF TRIESTE   (Italy)

Author keywords

Melanin; Oligotrophism; Protective molecules; Secondary metabolites; Stress

Indexed keywords

EID: 84875871743     PISSN: None     EISSN: 1664302X     Source Type: Journal    
DOI: 10.3389/fmicb.2012.00390     Document Type: Article

References (59)

1. Bar-Even, A., Noor, E., and Milo, R. (2012). A survey of carbon fixation pathways through a quantitative lens.J. Exp. Bot. 63, 2325-2342.
2. Blomberg, A., and Adler, L. (1992). Physiology of osmotolerance in fungi. Adv. Microb. Physiol. 33, 145-212.
3. Boustie, J., Tomasi, S., and Grube, M. (2011). Bioactive lichen metabolites: alpine habitats as an untapped source. Phytochem. Rev. 10, 287-307.
4. Brunauer, G., Blaha, J., Hager, A., Türk, R., Stocker-Wörgötter, E., and Grube, M. (2007). Lichenoid structures in vitro of a cultured lichenicolous fungus. Symbiosis 44, 127-136.
5. Bryan, R., Jiang, Z., Friedman, M., and Dadachova, E. (2011). The effects of gamma radiation, UV and visible light on ATP levels in yeast cells depend on cellular melaniza-tion. Fungal Biol. 115,945-949.
6. Butler, M. J., and Day, A. W. (1998). Fungal melanins: a review. Can. J. Microbiol. 44, 1115-1136.
7. Dadachova, E., and Casadevall, A. (2008). Ionizing radiation: how fungi cope, adapt, and exploit with the help of melanin. Curr. Opin. Microbiol. 11,525-531.
8. Dadachova, E., Bryan, R. A., Huang, X., Moadel, T., Schweitzer, A. D., Aisen, P., et al. (2007). Ionizing radiation changes the electronic properties of melanin and enhances the growth of melanized fungi. PLoS ONE 2:e457. doi: 10.1371/journal.pone.0000457
9. Daly, M. J. (2012). Death by protein damage in irradiated cells. DNA Repair 11, 12-21.
10. Daly, M. J., Gaidamakova, E. K., Matrosova, V. Y., Kiang, J. G., Fukumoto, R., Lee, D. Y., et al. (2010). Small-molecule antioxidant proteome-shields in Deinococcus radiodurans. Plos ONE 5:e12570. doi: 10.1371/journal.pone.0012570
11. Fan, Y., Solomon, P., Oliver, R. P., and Brown, L. S. (2011). Photochemical characterization of a novel fungal rhodopsin from Phaeosphaeria nodorum. Biochim. Biophys. Acta 1807,1457-1466.
12. Friedl, T., and Büdel, B. (2008). "Photobionts," in Lichen Biology, ed T. H. Nash 3rd. (Cambridge: Cambridge University Press), 9-26.
13. Fuchs, G. (2011). Alternative pathways of carbon dioxide fixation: insights into the early evolutions of life. Ann. Rev. Microbiol. 65, 631-658.
14. Gadd, G. M., and de Rome, L. (1988). Biosorption of copper by fungal melanin. Appl Microbiol. Biotechnol. 29, 610-617.
15. 2+-Peptide complex from Deinococcus. Cell Host Microbe 12, 117-124.
16. Gorbushina, A. A., Beck, A., and Schulte, A. (2005). Microcolonial rock inhabiting fungi and lichen photobionts: evidence for mutualistic interactions. Mycol Res. 109, 1288-1296.
17. Gorbushina, A. A., and Broughton, W. J. (2009). Microbiology of the atmosphere-rock interface: how biological interactions and physical stresses modulate a sophisticated microbial ecosystem. Ann. Rev. Microbiol. 63,431-450.
18. Gorbushina, A. A., Whitehead, K., Dornieden, T., Niesse, A., Schulte, A., and Hedges, J. (2003). Black fungal colonies as units of survival: hyphal mycosporines synthesized by rock dwelling micro-colonial fungi. Can. J. Bot. 2, 131-138.
19. Gostincar, C., Grube, M., de Hoog, S., Zalar, P., and Gunde-Cimerman, N. (2010). Extremotolerance in fungi: evolution on the edge. FEMS Microbiol. Ecol. 71,2-11.
20. Gostincar, C., Grube, M., and Gunde-Cimerman, N. (2011). Evolution of fungal pathogens in domestic environments? Fungal Biol. 115, 1008-1018.
21. Gostincar, C., Lenassi, M., Gunde-Cimerman, N., Plemenitaš, A. (2011). Fungal adaptation to extremely high salt concentrations. Adv. Appl. Microbiol. 77, 71-96.
22. Grote, M., O'Malley, M. A. (2011). Enlightening the life sciences: the history of halobacterial andmi-crobial rhodopsin research. FEMS Microbiol. Rev. 35, 1082-1099.
23. Gueidan, C., Ruibal, C., de Hoog, G. S., and Schneider, H. (2011). Rock-inhabiting fungi originated during periods of dry climate in the late Devonian and middle Triassic. Fungal Biol. 115, 987-996.
24. Gueidan, C., Ruibal, C., de Hoog, G. S., Gorbushina, A. A., Untereiner, W. A., and Lutzoni, F. (2008). A rock-inhabiting ancestor for mutualistic and pathogen-rich fungal lineages. Stud. Mycol. 61, 111-119.
25. Gunde-Cimerman, N., Zalar, P., de Hoog, S., and Plemenitaš, A. (2000). Hypersaline waters in salterns - natural ecological niches for halophilic black yeasts. FEMS Microbiol. Ecol. 32, 235-240.
26. Hallmann, C, Riidrich, J., Enseleit, M., Friedl, T., and Hoppert, M. (2011). Microbial diversity on a marble monument: a case study. Environ. Earth Sci. 63, 1701-1711.
27. Harutyunyan, S., Muggia, L., and Grube, M. (2008). Black fungi in lichens from seasonally arid habitats. Stud. Mycol. 61, 83-90.
28. Jürgensen, C. W., Jacobsen, N. R., Emri, T., Eriksen, S. H., and Pócsi, I. (2001). Glutathione metabolism and dimorphism in Aureobasidium pullulans. J. Basic Microbiol. 41, 131-137.
29. Kogej, T., Gostincar, C., Volkmann, M., Gorbushina, A. A., and Gunde-Cimerman, N. (2006). Mycosporines in extremophilic fungi-novel complementary osmolytes? Environ. Chem. 3, 105-110.
30. Kohlmeyer, J., Hawksworth, D., and Volkmann-Kohlmeyer, B. (2004). Observations on two marine and maritime "borderline" lichens: Mastodia tessellata and Collemopsidium pelvetiae. Mycol. Prog. 3,51-56.
31. Kranner, I., Cram, W. J., Zorn, M., Wornik, S., Yoshimura, I., Stabentheiner, E., et al. (2005). Antioxidants and photoprotec-tion in a lichen as compared with its isolated symbiotic partners. Proc. Natl. Acad. Sci. U.S.A. 102, 3141-3146.
32. Lapinskas, P. J., Cunningham, K. W., Liu, X. F., Fink, G. R., and Culotta, V. C. (1995). Mutations in PMR1 suppress oxidative damage in yeast cells lacking superoxide dismutase. Mol. Cell. Biol. 15, 1382-1388.
33. Madhour, A., Anke, H., Mucci, A., Davoli, P., and Weber, R. W. (2005). Biosynthesis of the xanthophyll plectaniaxanthin as a stress response in the red yeast Dioszegia (Tremellales, Heterobasidiomycetes, Fungi). Phytochemistry 66, 2617-2626.
34. Miller, A. Z., Sanmartín, P., Pereira-Pardo, L., Dionísio, A., Saiz-Jimenez, C., Macedo, M. F., et al. (2012). Bioreceptivity of building stones: a review. Sci. Total Environ. 426, 1-12.
35. Muggia, L., Hafellner, J., Wirtz, N., Hawksworth, D. L., and Grube, M. (2008). The sterile microfila-mentous lichens Cystocoleus ebeneus and Racodium rupestre are relatives of clinically important doth-idealean fungi. Mycol. Res. 112, 50-56.
36. Nelsen, M. P., Lücking, R., Grube, M., Mbatchou, J. S., Muggia, L., Rivas Plata, E., et al. (2009). Unravelling the phylogenetic relationships of lichenised fungi in Dothideomyceta. Stud. Mycol. 64, 135-144.
37. Ocon, A., Hampp, R., and Requena, N. (2007). Trehalose turnover during abiotic stress in arbuscular myc-orrhizal fungi. New Phytol. 174, 879-891.
38. Onofri, S., Barreca, D., Selbmann, L., Isola, D., Rabbow, E., Horneck, G., et al. (2008). Resistance of Antarctic black fungi and cryptoendolithic communities to simulated space and Martian conditions. Stud. Mycol. 61, 99-109.
39. Onofri, S., Selbmann, L., de Hoog, G. S., Grube, M., Barreca, D., Ruisi, S., et al. (2007). Evolution of fungi at boundaries of life. Adv. Space Res. 40, 1657-1664.
40. Oren, A., and Gunde-Cimerman, N. (2007). Mycosporines and mycosporine-like amino acids: UV protectants or multipurpose secondary metabolites? FEMS Microbiol. Lett. 269, 1-10.
41. Palmer, R. J., and Friedman, E. I. (1988). Incorporation of inorganic carbon by Antarctic cryptoendolithic fungi. Polarforschung 58, 189-191.
42. Parkinson, S. M., Killham, K., and Wainwright, M. (1990). Assimilation of 14CO2 by Fusarium oxysporum grown under olig-otrophic conditions. Mycol. Res. 94, 959.
43. Parkinson, S. M., Wainwright, M., and Killham, K. (1989). Observations on oligotrophic growth of fungi on silica gel. Mycol. Res. 93, 529.
44. Paudel, B., Bhattarai, H. D., Koh, H. Y., Lee, S. G., Han, S. J., Lee, H. K., et al. (2011). Ramalin, a novel nontoxic antioxidant compound from the Antarctic lichen Ramalina terebrata. Phytomedicine 18, 1285-1290.
45. Prenafeta-Boldu, F. X., Summerbell, R., and de Hoog, G. S. (2006). Fungi growing on aromatic hydrocarbons: biotechnology's unexpected encounter with bio-hazard? FEMS Microbiol. Rev. 30, 109-130.
46. Rastogi, R. P., Richa, Sinha, R. P., Singh, S. P., and Häder, D. P. (2010). Photoprotective compounds from marine organisms. J. Ind. Microbiol. Biotechnol. 37, 537-558.
47. Rezanka, T., Temina, M., Tolstikov, A. G., and Dembitsky, V. M. (2004). Natural microbial UV radiation filters - mycosporine-like amino acids. Folia Microbiol. 49, 339-352.
48. Roullier, C., Chollet-Krugler, M., Bernard, A., and Boustie, J. (2009). Multiple dual-mode centrifugal partition chromatography as an efficient method for the purification of a mycosporine from a crude methanolic extract of Lichina pygmaea. J. Chromatogr. B Analyt. Technol. Biomed. Life Sci. 877, 2067-2073.
49. Roullier, C., Chollet-Krugler, M., Pferschy-Wenzig, E. M., Maillard, A., Rechberger, G. N., Legouin-Gargadennec, B., et al. (2011). Characterization and identification of mycosporines-like compounds in cyanolichens. Isolation of mycosporine hydrox-yglutamicol from Nephroma laevigatum. Ach. Phytochemistry 72, 1348-1357.
50. Ruibal, C., Gueidan, C., Selbmann, L., Gorbushina, A. A., Crous, P. W., Groenewald, J. Z., et al. (2009). Phylogeny of rock-inhabiting fungi related to Dothideomycetes. Stud. Mycol. 64, 123-133.
51. Schweitzer, A. D., Revsjkaya, E., Chu, P., Pazo, V., Friedman, M., Nosanchuk, J. D., et al. (2010). Melanin-covered nanoparticles for protection of bone marrow during radiation therapy of cancer. Int. J. Radiat. Oncol. Biol. Phys. 78, 1494-1502.
52. Scott, J. A., Untereiner, W A., Ewaze, J. O., Wong, B., and Doyle, D. (2007). Baudoinia, a new genus to accommodate Torula compniacensis. Mycologia 99, 592-601.
53. Shima, J., and Takagi, H. (2009). Stress-tolerance of baker's-yeast (Saccharomyces cerevisiae) cells: stress-protective molecules and genes involved in stress tolerance. Biotechnol. Appl. Biochem. 53, 155-164.
54. Slepecky, R. A., and Starmer, W. T. (2009). Phenotypic plasticity in fungi: a review with observations on Aureobasidium pullulans. Mycologia 101, 823-832.
55. Sterflinger, K., Tesei, D., and Zakharova, K. (2012). Fungi in hot and cold deserts with particular reference to micro-colonial fungi. Fungal Ecol. 5, 453-462.
56. Takagi, H. (2008). Proline as a stress protectant in yeast: physiological functions, metabolic regulations, and biotechnological applications. Appl. Microbiol. Biotechnol. 81, 211-223.
57. Turick, C. E., Ekechukwu, A. A., Milliken, C. E., Casadevall, A., and Dadachova, E. (2011). Gamma radiation interacts with melanin to alter its oxidation-reduction potential and results in electric current production. Bioelectrochemistry 82, 69-73.
58. Waschuk, S. A., Bezerra, A. G., Shi, L., and Brown, L. S. (2005). Leptosphaeria rhodopsin: bacteriorhodopsin-like proton pump from a eukaryote. Proc. Natl. Acad. Sci. U.S.A. 102, 6879-6883.
59. Zhdanova, N. N., Zakharchenko, V. A., Vember, V. V., and Nakonechnaya, L. T. (2000). Fungi from Chernobyl: mycobiota of the inner regions of the containment structures of the damaged nuclear reactor. Mycol. Res. 104, 1421-1426.