Black fungal extremes - CBS

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Ce l l u l a r r e s p o n s e s t o d e s i c c at i o nCONCLUSIONSDuring desiccation-induced mycostasis (dormancy), MCF employ abroad range of unspecific stress response mechanisms including:• cell wall re-encrustation with irradiation-protective andantioxidant melanins (Gorbushina et al. 1993, 2003);• layers of EPS containing lipids, polysaccharides, and proteinsact as an additional irradiation filter and may have propertiessimilar to those described for glass-forming polymers (Hill etal. 1997);• presence of diverse carotenoids that are known to stabilisecell membranes;• presence of intracellular mycosporines (typical of fungalsurvival structures such as spores, fruit bodies and sclerotia)that act as UV-filters, antioxidants and minor osmolytes(Gorbushina et al. 2003, Volkmann et al. 2003, Kogej et al.2006, Kogej et al. 2007), and;• as witnessed by a high proportion of unsaturated fatty acidsand normal levels of membrane lipids (phosphatidylcholine,phosphatidylethanolamine), membranes in dormant desiccatedMCF are maintained in a stable physiological state.ACKNOWLEDGEMENTSThis work was financially supported by a grant of DFG (Go 897/2) as well as by theMinistry of Science and Culture of Lower Saxony (Dorothea-Erxleben-Programm).Technical help of Anette Schulte, Daria Morozova and Renate Kort is deeplyappreciated. William J. Broughton is gratefully acknowledged for his valued help inediting our English text.REFERENCESArzanlou M, Groenewald JZ, Gams W, Braun U, Shin H-D, Crous PW (2007).Phylogenetic and morphotaxonomic revision of Ramichloridium and alliedgenera. Studies in Mycology 58: 57-93.Billi D, Potts M (2002). Life and death of dried prokaryotes. Research in Microbiology153: 7–12.Bligh EG, Dyer WJ (1959). A rapid method of total lipid extraction and purification.Canadian Journal of Biochemistry and Physiology 37: 911–915.Britton G (1995). UV/visible spectroscopy. Carotenoids 1B: Spectroscopy,Basel: Birkhauser, 13–62.Butler MJ, Day AW (1998). Fungal melanins: a review. Canadian Journal ofMicrobiology 44: 1115–1136.Davoli P, Mierau V, Weber RWS (2004). Carotenoids and fatty acids in red yeastsSporobolomyces roseus and Rhodotorula glutinis. Applied Biochemistry andMicrobiology 40: 392–397.Davoli P, Weber RWS (2002). Identification and quantification of carotenoid pigmentsin aeciospores of the daisy rust fungus, Puccinia distincta. Phytochemistry 60:309–313.Gorbushina AA, Krumbein, WE, Hamann, CH, Panina, LK, Soukharzhevski, S,Wollenzien, U. (1993). Role of black fungi in color-change and biodeteriorationof antique marbles. Geomicrobiological Journal 11: 205–221.Gorbushina AA (2003). Microcolonial fungi: survival potential of terrestrial vegetativestructures. Astrobiology 3: 543–554.Gorbushina AA (2007). Life on the Rocks. Environmental Microbiology 9: 1613–1631.Gorbushina AA, Krumbein WE (2000). Subaerial microbial mats and their effects onsoil and rock. In: Microbial Sediments (Riding R & Awramik S, eds). Springer.Berlin: 161–170Gorbushina AA, Whitehead K, Dornieden Th, Niesse A, Schulte A, Hedges JI (2003).Black fungal colonies as units of survival: hyphal mycosporines synthesised byrock dwelling microcolonial fungi. Canadian Journal of Botany 81: 131–138.Hill DR, Keenan TW, Helm RF, Potts M, Crowe LM, Crowe JH (1997). Extracellularpolysaccharide of Nostoc commune (Cyanobacteria) inhibits fusion ofmembrane vesicles during desiccation. Journal of Applied Phycology 9: 237–248.Kabara JJ, Chen JS (1976). Microdetermination of lipid classes of thin-layerchromatography. Analytical Chemistry 48: 814–817.Kates M (1972). Techniques of lipidology. Elsevier, Amsterdam.Kogej T, Gostincar C, Volkmann M, Gorbushina AA, Gunde-Cimerman N (2006).Screening of halophilic and psychrophilic fungi for mycosporines – could theyact as compatible solutes in fungi? Environmental Chemistry 3: 105–110.Kogej T, Stein M, Volkmann M, Gorbushina AA, Galinski EA, Gunde-CimermanN (2007). Osmotic adaptation of halophilic fungus Hortaea werneckii: role ofosmolytes and melanization. Microbiology (U.K.) 153: 4261–4273.Kotlova ER, Gorbushina AA (2003). Adaptive response of rock inhabitingmicrocolonial ascomycetes to de- and rehydration. Joint MSA/BMS Meeting,Assilomar, July 26–31, 2003.Mattimore V, Battista JR (1996). Radioresistance of Deinococcus radiodurans:functions necessary to survive ionizing radiation are also necessary to surviveprolonged desiccation. Journal of Bacteriology 178: 633–637.Palmer FE, Emery J, Staley JT (1987). Survival and growth of microcolonial fungi asaffected by temperature and humidity. New Phytologist 107: 155–162.Rikkinen J (1995). What’s behind the pretty colours? A study on the photobiology oflichens. Bryobrothera 4: 1–239.Ruibal CV (2004). Isolation and characterization of melanized, slow-growing fungifrom semiarid rock surfaces of central Spain and Mallorca. Ph.D. dissertation,Universidad Autónoma de Madrid Merck, Sharp & Dohme de España, Madrid.Ruibal C, Platas G, Bills GF (2008). High diversity and morphological convergenceamong melanised fungi from rock formations in the Central Mountain Systemof Spain. Persoonia 21: 93–110.Selbmann L, Hoog GS de, Mazzaglia A, Friedmann EI, Onofri S (2005). Fungi atthe edge of life: cryptoendolithic black fungi from Antarctic desert. Studies inMycology 51: 1–32.Simpson KL (1972). The biosynthesis of yeast carotenoids. In: The chemistry ofplant pigments (Chichester CO, eds). Academic Press, New York and London.Simpson KL, Nakayama TOM, Chichester CO (1964). Biosynthesis of yeastcarotenoids. Journal of Bacteriology 88: 1688–1694.Staley JT, Palmer F, Adams JB (1982). Microcolonial fungi: common inhabitants ondesert rocks? Science 215: 1093–1095.Sterflinger K, Prillinger H (2001). Molecular taxonomy and biodiversity of rockfungal communities in an urban environment (Vienna, Austria). Antonie vanLeeuwenhoek 80: 275–286.Sterflinger K (1998). Temperature and NaCl-tolerance of rock-inhabiting meristematicfungi. Antonie van Leeuwenhoek 74: 271–281.Sterflinger K, Krumbein WE (1995). Multiple stress factors affecting growth of rockinhabitingblack fungi. Botanica Acta 108: 490–496.Urzi C, Wollenzien U, Criseo G, Krumbein WE (1995) Biodiversity of the rockinhabiting microbiota with special reference to black fungi and black yeasts. InMicrobial diversity and ecosystem function (Allsopp D, Colwell RR, HawksworthDL, eds). CAB International, Wallingford: 289–302.Vaskovsky VE, Kostetsky EY, Vasendin IM (1975). A universal reagent forphospholipid analysis. Journal of Chromatography 114: 129–141.Vaskovsky VE, Terekhova TA (1979). HPTLC of phospholipid mixtures containingphosphatidylglycerol. Journal of High Resolution Chromatography andChromatography Communications 2: 671–672.Volkmann M, Gorbushina AA (2006). A broadly applicable method for extractionand characterisation of mycosporines and mycosporine-like amino acidsof terrestrial, marine and freshwater origin. FEMS Microbiology Letters 255:286–295.Volkmann M, Whitehead K, Rütters H, Rullkötter J, Gorbushina AA (2003).Mycosporine-glutamicol-glucoside: a native UV-absorbing secondary metaboliteof rock inhabiting microcolonial fungi (MCF). Rapid Communications in MassSpectroscopy 17: 897–902.Weber RWS, Davoli P (2002). Autophagocytosis of carotenoid-rich lipid droplets intovacuoles during aeciospore ageing in Puccinia distincta. New Phytologist 154:471–479.Wollenzien U, Hoog GS de, Krumbein WE, Uijthof JMJ (1997) Sarcinomycespetricola, a new microcolonial fungus from marble in the Mediterranean basin.Antonie van Leeuwenhoek 71: 281–288.www.studiesinmycology.org97
available online at www.studiesinmycology.org St u d i es in My c o l o g y 61: 99–109. 2008.doi:10.3114/sim.2008.61.10Resistance of Antarctic black fungi and cryptoendolithic communities to simulatedspace and Martian conditionsS. Onofri 1 *, D. Barreca 1 , L. Selbmann 1 , D. Isola 1 , E. Rabbow 2 , G. Horneck 2 , J.P.P. de Vera 3 , J. Hatton 4 and L. Zucconi 11DECOS, Università degli Studi della Tuscia, Largo dell’Università, Viterbo, Italy; 2 German Aerospace Center (DLR), Institute of Aerospace Medicine, Cologne, Germany;3Heinrich-Heine-University, Düsseldorf, Germany; 4 ESA-ESTEC (HME-GA) Noordwijk, The Netherlands*Correspondence: Silvano Onofri, onofri@unitus.itAbstract: Dried colonies of the Antarctic rock-inhabiting meristematic fungi Cryomyces antarcticus CCFEE 515, CCFEE 534 and C. minteri CCFEE 5187, as well as fragmentsof rocks colonized by the Antarctic cryptoendolithic community, were exposed to a set of ground-based experiment verification tests (EVTs) at the German Aerospace Center(DLR, Köln, Germany). These were carried out to test the tolerance of these organisms in view of their possible exposure to space conditions outside of the International SpaceStation (ISS). Tests included single or combined simulated space and Martian conditions. Responses were analysed both by cultural and microscopic methods. Thereby,colony formation capacities were measured and the cellular viability was assessed using live/dead dyes FUN 1 and SYTOX Green. The results clearly suggest a general goodresistance of all the samples investigated. C. minteri CCFEE 5187, C. antarcticus CCFEE 515 and colonized rocks were selected as suitable candidates to withstand space flightand long-term permanence in space on the ISS in the framework of the LIchens and Fungi Experiments (LIFE programme, European Space Agency).Key words: Astrobiology, cryptoendolithic community, fungi, ground-based experiments, lithopanspermia, panspermia, space conditions, stress resistance, viability.INTRODUCTIONAstrobiology raises the fascinating question about the possibleexistence of life forms on other planets, survival in space conditionsand possible interplanetary transfers. This emerging field of researchencounters evident challenges in carrying out in situ experiments.Most of the information on the behaviour of organism underextraterrestrial conditions has been obtained by space simulationexperiments performed on Earth (Nicholson et al. 2000, Rettberg etal. 2004, de Vera et al. 2003, 2004). Earth is our only reference forstudying the possibility of life on other planetary bodies: extremeterrestrial environments host specifically adapted organisms,among which anhydrobionts are generally considered the bestmodels for exobiological studies (Finster et al. 2007). Extremeenvironments include the cold and dry polar regions, permafrostsoils, deep sea, alkaline and hypersaline habitats, arid regions, oracidic sites (González-Toril et al. 2003, McKay et al. 2003, Gunde-Cimerman et al. 2005, Gilichinsky et al. 2007, Onofri et al. 2007a).Organisms able to thrive in extreme environments are generallydefined as ‘extremophiles’. The existence of extremophiles has ledto speculations about the survival of organisms during interplanetarytransfer and that life could be present even on other planets of theSolar system, where water might be present e.g. under the icysurfaces of some of Jupiter’s moons or in the underground cavernsof Mars (Miller 2005, Mustard et al. 2008).Antarctica is a continent where a combination of dry, cold,and oligotrophic extremes exists, and huge fluxes of dangerousradiations such as UV radiation can be present as well. Theseconditions become harsher in the ice-free McMurdo Dry Valleysarea in continental Antarctica where cryptoendolithic microbialcommunities are almost the only life-form possible. Blackmeristematic microfungi of these communities were alreadysuggested as eukaryotic models for the biological exploration ofMars (Onofri et al. 2004). The McMurdo Dry Valleys area, alsoknown as Ross Desert, is the largest ice-free area in Antarctica.It is located within the Transantarctic Mountains in the Southernpart of Victoria Land. Winter air temperature fluctuates between–20 and –50 °C (occasionally lower), rising to mean daily valuesof about –15 °C in the summer, up to 15 °C or higher values atground surfaces. Wide and repeated thermal fluctuations are astress factor, more than the minimum values reached. Dryness isalso extreme: water is mainly supplied by snow (less than 100 mmwater equivalent / yr), that mostly sublimes without visibly wettingthe ground or it is blown away (Nienow & Friedmann 1993). Highevaporation leads to high salt concentration on rock surfacesand a poor nutrient soil is occasionally present because of thescarcity of organic matter. Finally, UV radiation is high, mainly inthe springtime, as a consequence of stratospheric ozone depletionduring this period. As for it’s oxygenic atmosphere no place on Earthis truly comparable to what is present on Mars, the McMurdo DryValleys could be called the closest terrestrial analogue. Therefore,they are one of the best investigated areas as a model environmentfor astrobiological studies since the 1970ies (Horowitz et al. 1972,Wynn-Williams & Edwards 2000, Onofri et al. 2004).Friedmann and co-workers (Friedmann & Ocampo-Friedmann 1976, Friedmann 1982, Nienow & Friedmann 1993)discovered various microbial communities in the Ross Desert.The communities live sheltered under the rock surface, wherethey find a more favorable nanoclimate in the rock pore-spaces.Among these, the "lichen dominated cryptoendolithic community"is the most studied and known (Friedmann 1982). Under a reddishsuperficial crust, eukaryotic and prokaryotic autotrophic andheterotrophic microorganisms form a clearly stratified community.Antarctic black non-lichenised rock fungi, showing meristematicgrowth, are recurrent components of this community and commonCopyright 2008 CBS Fungal Biodiversity Centre, P.O. Box 85167, 3508 AD Utrecht, The Netherlands.You are free to share - to copy, distribute and transmit the work, under the following conditions:Attribution:You must attribute the work in the manner specified by the author or licensor (but not in any way that suggests that they endorse you or your use of the work).Non-commercial: You may not use this work for commercial purposes.No derivative works: You may not alter, transform, or build upon this work.For any reuse or distribution, you must make clear to others the license terms of this work, which can be found at http://creativecommons.org/licenses/by-nc-nd/3.0/legalcode. Any of the above conditions can be waived if you getpermission from the copyright holder. Nothing in this license impairs or restricts the author’s moral rights.99
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Studies in Mycology 61 (2008)Black
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homogentisate 165, 171, 173Hortaea
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CBS Biodiversity SeriesNo. 6: Alter
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Studies in Mycology (ISSN 0166-0616
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Satow MM, Attili-Angelis D, Hoog GS
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