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Viability of the lichen Xanthoria elegans and its symbionts after 18 months of space exposure and simulated Mars conditions on the ISS

  • Annette Brandt (a1), Jean-Pierre de Vera (a2), Silvano Onofri (a3) and Sieglinde Ott (a1)


The lichen Xanthoria elegans has been exposed to space conditions and simulated Mars-analogue conditions in the lichen and fungi experiment (LIFE) on the International Space Station (ISS). After several simulations and short space exposure experiments such as BIOPAN, this was the first long-term exposure of eukaryotic organisms to the hostile space conditions of the low Earth orbit (LEO). The biological samples were integrated in the EXPOSE-E facility and exposed for 1.5 years outside the ISS to the combined impact of insolation, ultraviolet (UV)-irradiation, cosmic radiation, temperatures and vacuum conditions of LEO space. Additionally, a subset of X. elegans samples was exposed to simulated Martian environmental conditions by applying Mars-analogue atmosphere and suitable solar radiation filters. After their return to Earth the viability of the lichen samples was ascertained by viability analysis of LIVE/DEAD staining and confocal laser-scanning microscopy, but also by analyses of chlorophyll a fluorescence. According to the LIVE/DEAD staining results, the lichen photobiont showed an average viability rate of 71%, whereas the even more resistant lichen mycobiont showed a rate of 84%. Post-exposure viability rates did not significantly vary among the applied exposure conditions. This remarkable viability is discussed in the context of particular protective mechanisms of lichens such as anhydrobiosis and UV-screening pigments.

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      Viability of the lichen Xanthoria elegans and its symbionts after 18 months of space exposure and simulated Mars conditions on the ISS
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Baqué, M., Scalzi, G., Rabbow, E., Rettberg, P. & Billi, D. (2013). Biofilm and planktonic lifestyles differently support the resistance of the desert cyanobacterium Chroococcidiopsis under space and martian simulations. Orig. Life Evol. Biosph. 43(4–5), 377389.
Benardini, J.N., Sawyer, J., Venkateswaran, K. & Nicholson, W.L. (2003). Spore UV and acceleration resistance of endolithic Bacillus pumilus and Bacillus subtilis isolates obtained from Sonoran desert basalt: implications for lithopanspermia. Astrobiology 3(4), 709717.
Berger, T., Hajek, M., Bilski, P., Körner, C., Vanhavere, F. & Reitz, G. (2012). Cosmic radiation exposure of biological test systems during the EXPOSE-E mission. Astrobiology 12(5), 387392.
Brunauer, G. & Stocker-Wörgötter, E. (2005). Culture of lichen fungi for future production of biologically active compounds. Symbiosis 38(2), 187201.
Buffoni Hall, R.S., Paulsson, M., Duncan, K., Tobin, A.K., Widell, S. & Bornman, J.F. (2003). Water-and temperature-dependence of DNA damage and repair in the fruticose lichen Cladonia arbuscula ssp. mitis exposed to UV-B radiation. Physiol. Plantarum 118(3), 371379.
Carlile, M. J. (1995). The Success of the Hypha and Mycelium. In The Growing Fungus, ed. Gow und, N.A.R., Gadd, G.M., pp. 319. Springer Dordrecht, Netherlands.
Clark, B.C. (2001). Planetary interchange of bioactive material: probability factors and implications. Orig. Life Evol. Biosph. 31(1–2), 185197.
Cockell, C.S. (2008). The interplanetary exchange of photosynthesis. Orig. Life Evol. Biosph. 38(1), 87104.
Crick, F.H. & Orgel, L.E. (1973). Directed panspermia. Icarus 19(3), 341346.
Crowe, J.H., Hoekstra, F.A. & Crowe, L.M. (1992). Anhydrobiosis. Annu. Rev. Physiol. 54(1), 579599.
Dachev, T., Horneck, G., Häder, D. P., Schuster, M., Richter, P., Lebert, M. & Demets, R. (2012). Time profile of cosmic radiation exposure during the EXPOSE-E mission: the R3DE instrument. Astrobiology 12(5), 403411.
de la Torre, R., Horneck, G., Sancho, L.G., Scherer, K., Faciu, R., Urling, T. & Pintado, A. (2002) Photoecological characterization of an epilithic ecosystem at a high mountain locality (Central Spain). In Proc. Second European Workshop on Exo-Astrobiology, 16–19 Sep 2002, Granz, Austria, ESA SP-518, ESA ESTEC The Netherlands, pp. 443444.
de la Torre Noetzel, R., Sancho, L. G., Pintado, A., Rettberg, P., Rabbow, E., Panitz, C., Deutschmann, U., Reina, M. & Horneck, G. (2007). BIOPAN experiment LICHENS on the Foton M2 mission: pre-flight verification tests of the Rhizocarpon geographicum-granite ecosystem. Adv. Space Res. 40(11), 16651671.
de la Torre Noetzel, R., Martinez Frías, J., Mateo-Martí, E., Sanchez Iñigo, F.J., García Sancho, L. & Horneck, G. (2010a). Are lichens and cyanobacteria suitable candidates to test the theory of lithopanspermia? In EGU General Assembly Conf. Abstracts, vol. 12, p. 14713.
de la Torre, R. et al. (2010b). Survival of lichens and bacteria exposed to outer space conditions – results of the LITHOPANSPERMIA experiments. Icarus 208(2), 735748.
de Vera, J.P. (2005). Grenzen des Überlebens: Flechten als Modellorganismen für das Potential von Adaptationsmechanismen unter Extrembedingungen. Dissertation at Heinrich-Heine University, ULB Düsseldorf, pp. 1180.
de Vera, J.P. (2012). Lichens as survivors in space and on Mars. Fungal Ecol. 5(4), 472479.
de Vera, J.P. & Ott, S. (2010). Resistance of symbiotic eukaryotes. In Symbioses and Stress, ed. Seckbach, J., Grube, M., pp. 595611, Springer, Netherlands.
de Vera, J.P., Horneck, G., Rettberg, P. & Ott, S. (2003). The potential of the lichen symbiosis to cope with extreme conditions of outer space-I. Influence of UV radiation and space vacuum on the vitality of lichen symbiosis and germination capacity. Int. J. Astrobiol. 1(4), 285293.
de Vera, J.P., Horneck, G., Rettberg, P. & Ott, S. (2004a). The potential of the lichen symbiosis to cope with the extreme conditions of outer space II: germination capacity of lichen ascospores in response to simulated space conditions. Adv. Space Res. 33(8), 12361243.
de Vera, J.P., Horneck, G., Rettberg, P. & Ott, S. (2004b). In the context of panspermia: may lichens serve as shuttles for their bionts in space? In Proc. Third European Workshop on Exo-Astrobiology, 18–20 November 2003, Madrid, Spain, ESA SP-545, ESA ESTEC, The Netherlands, pp. 197198.
de Vera, J.P., Tilmes, F., Heydenreich, T., Meyer, C., Horneck, G. & Ott, S. (2007). Potential of prokaryotic and eukaryotic organisms in Mars-like environments and as a reference system for the search of life on other planets. In Proc. DGLR Int. Symp., p. 10.
de Vera, J.P., Rettberg, P. & Ott, S. (2008). Life at the limits: capacities of isolated and cultured lichen symbionts to resist extreme environmental stresses. Orig. Life Evol. Biosph. 38(5), 457468.
de Vera, J.P., Möhlmann, D., Butina, F., Lorek, A., Wernecke, R. & Ott, S. (2010). Survival potential and photosynthetic activity of lichens under Mars-like conditions: a laboratory study. Astrobiology 10(2), 215227.
de Vera, J.P., Schulze-Makuch, D., Khan, A., Lorek, A., Koncz, A., Möhlmann, D. & Spohn, T. (2014). Adaptation of an Antarctic lichen to Martian niche conditions can occur within 34 days. Planet. Space Sci. 98, 182190.
Dietz, S., Büdel, B., Lange, O.L. & Bilger, W. (2000). Transmittance of light through the cortex of lichens from contrasting habitats. Bibl. Lichenol. 75, 171182.
Dyer, P. & Crittenden, P. (2008). Antarctic lichens: life in the freezer. Microbiol. Today 35(2), 74.
Eker, A.P.M., Yajima, H. & Yasui, A. (1994). DNA photolyase from the fungus Neurospora crassa. Purification, characterization and comparison with other photolyases. Photochem. Photobiol. 60(2), 125133.
Ertl, L. (1951). Über die Lichtverhältnisse in Laubflechten. Planta 39(3), 245270.
Gannutz, T.P. (1972). Effects of gamma radiation on lichens – 1. Acute gamma radiation on lichen algae and fungi. Radiat. Bot. 12, 331338.
Gauslaa, Y. & McEvoy, M. (2005). Seasonal changes in solar radiation drive acclimation of the sun-screening compound parietin in the lichen Xanthoria parietina . Basic Appl. Ecol. 6(1), 7582.
Gauslaa, Y. & Solhaug, K.A. (2004). Photoinhibition in lichens depends on cortical characteristics and hydration. Lichenologist 36(2), 133143.
Hájek, J., Váczi, P., Barták, M. & Jahnová, L. (2012). Interspecific differences in cryoresistance of lichen symbiotic algae of genus Trebouxia assessed by cell viability and chlorophyll fluorescence. Cryobiology 64(3), 215222.
Hawksworth, D.L. (1988). The variety of fungal-algal symbioses, their evolutionary significance, and the nature of lichens. Bot. J. Linnean Soc. 96(1), 320.
Henssen, A. & Jahns, H.M. (1974). Lichenes. Eine Einführung in die Flechtenkunde. Georg Thieme Verlag, Stuttgart, pp. 1171.
Hoekstra, F.A., Golovina, E.A. & Buitink, J. (2001). Mechanisms of plant desiccation tolerance. Trends Plant sci. 6(9), 431438.
Holzinger, A. & Lütz, C. (2006). Algae and UV irradiation: effects on ultrastructure and related metabolic functions. Micron 37(3), 190207.
Honegger, R. (2003). The impact of different long-term storage conditions on the viability of lichen-forming ascomycetes and their green algal photobiont, Trebouxia spp. Plant Biol. 5(3), 324330.
Horneck, G., Stöffler, D., Ott, S., Hornemann, U., Cockell, C.S., Moeller, R., Meyer, C., de Vera, J.P., Fritz, J., Schade, S. & Artemieva, N.A. (2008). Microbial rock inhabitants survive hypervelocity impacts on Mars-like host planets: first phase of lithopanspermia experimentally tested. Astrobiology 8(1), 1744.
Horneck, G., Klaus, D.M. & Mancinelli, R.L. (2010). Space microbiology. Microbiol. Mol. Biol. Rev. 74(1), 121156.
Huneck, S. & Yoshimura, I. (1996). Data of lichen substances (chapter 3). In Identification of Lichen Substances. pp. 125446. Springer, Berlin, Heidelberg.
Jensen, M. (2002). Measurement of chlorophyll fluorescence in lichens. In Protocols in Lichenology, ed. Kranner, I., Beckett, R.P., Varma, A.K., pp. 135151. Springer Laboratory Manuals, Springer Verlag, Berlin, Heidelberg.
Kappen, L. (1985). Lichen-habitats as micro-oases in the Antarctic – the role of temperature. Polarforschung 55(1), 4954.
Kappen, L. (2000). Some aspects of the great success of lichens in Antarctica. Antarct. Sci. 12(3), 314324.
Kappen, L. & Schroeter, B. (1997). Activity of lichens under the influence of snow and ice. In Proc. NIPR Symp. on Polar Biology. pp. 163168.
Kappen, L., Schroeter, B., Scheidegger, C., Sommerkorn, M. & Hestmark, G. (1996). Cold resistance and metabolic activity of lichens below 0 °C. Adv. Space Res. 18(12), 119128.
Kranner, I., Cram, W.J., Zorn, M., Wornik, S., Yoshimura, I., Stabentheiner, E. & Pfeifhofer, H.W. (2005). Antioxidants and photoprotection in a lichen as compared with its isolated symbiotic partners. Proc. Natl. Acad. Sci. USA 102(8), 31413146.
Kranner, I., Beckett, R., Hochman, A. & Nash, T.H. III (2008). Desiccation-tolerance in lichens: a review. Bryologist 111(4), 576593.
Lange, O.L. (1990). Twenty-three years of growth measurements on the crustose lichen Caloplaca aurantia in the central Negev Desert. Israel J. Bot. 39(4–6), 383394.
Lange, O.L. & Kappen, L. (1972). Photosynthesis of lichens from Antarctica. In Antarctic research series, vol. 20 (Antarctic terrestrial biology) , ed. Llano, A., pp. 8395. American Geophysical Union.
Lange, O.L., Bilger, W., Rimke, S. & Schreiber, U. (1989). Chlorophyll fluorescence of lichens containing green and blue-green algae during hydration by water vapor uptake and by addition of liquid water. Bot. Acta 102(4), 306313.
Meeßen, J., Eppenstein, S. & Ott, S. (2013a). Recognition mechanisms during the pre-contact state of lichens: II. Influence of algal exudates and ribitol on the response of the mycobiont of Fulgensia bracteata . Symbiosis 59(3), 131143.
Meeßen, J., Sánchez, F.J., Brandt, A., Balzer, E.M., de la Torre, R., Sancho, L.G., de Vera, J.P. & Ott, S. (2013b). Extremotolerance and resistance of lichens: comparative studies on five species used in astrobiological research I. Morphological and anatomical characteristics. Orig. Life Evol. Biosph. 43(3), 283303.
Melosh, H.J. (1984). Impact ejection, spallation, and the origin of meteorites. Icarus 59(2), 234260.
Meyer, C., Fritz, J., Misgaiski, M., Stoeffler, D., Artemieva, N.A., Hornemann, U., Moeller, R., de Vera, J.P., Cockell, C.S., Horneck, G., Ott, S. & Rabbow, E. (2011). Shock experiments in support of the Lithopanspermia theory: the influence of host rock composition, temperature, and shock pressure on the survival rate of endolithic and epilithic microorganisms. Meteorit. Planet. Sci. 46(5), 701718.
Millard, P.J., Roth, B.L., Thi, H.P., Yue, S.T. & Haugland, R.P. (1997). Development of the FUN-1 family of fluorescent probes for vacuole labeling and viability testing of yeasts. Appl. Environ. Microbiol. 63(7), 28972905.
Nicholson, W.L., Munakata, N., Horneck, G., Melosh, H.J. & Setlow, P. (2000). Resistance of Bacillus endospores to extreme terrestrial and extraterrestrial environments. Microbiol. Mol. Biol. Rev. 64(3), 548572.
Nybakken, L., Solhaug, K.A., Bilger, W. & Gauslaa, Y. (2004). The lichens Xanthoria elegans and Cetraria islandica maintain a high protection against UV-B radiation in Arctic habitats. Oecologia 140(2), 211216.
Onofri, S., Selbmann, L., Zucconi, L. & Pagano, S. (2004). Antarctic microfungi as models for exobiology. Planet. Space Sci. 52(1), 229237.
Onofri, S. et al. (2012). Survival of rock-colonizing organisms after 1.5 years in outer space. Astrobiology 12(5), 508516.
Ott, S. & Sancho, L.G. (1991). Structure and adaptation of lichens to extreme environmental conditions in the maritime Antarctic (Livingston Island, South Shetland Island). In: Actas del cuarto simposio espanol de estudios antarcticos. ed. Castellvi, J., pp. 251256. Comision Interministerial de ciencia y technologia, Madrid.
Øvstedal, D.O. & Lewis Smith, R.I. (2001). Lichens of Antarctica and South Georgia. Cambridge University Press, Cambridge, UK, pp. 361363.
Petersen, J.L., Lang, D.W. & Small, G.D. (1999). Cloning and characterization of a class II DNA photolyase from Chlamydomonas . Plant Mol. Biol. 40(6), 10631071.
Rabbow, E. et al. (2012). EXPOSE-E: an ESA astrobiology mission 1.5 years in space. Astrobiology 12(5), 374386.
Raggio, J., Pintado, A., Ascaso, C., de La Torre, R., de Los Ríos, A., Wierzchos, J., Horneck, G. & Sancho, L.G. (2011). Whole lichen thalli survive exposure to space conditions: results of LITHOPANSPERMIA experiment with Aspicilia fruticulosa . Astrobiology 11(4), 281292.
Rebecchi, L., Altiero, T. & Guidetti, R. (2007). Anhydrobiosis: the extreme limit of desiccation tolerance. Invert. Surviv. J. 4, 6581.
RedShift Report (2011). Reviewers: van Bavinchove, C., Beuselinck, T., EXPOSE: Environmental history by calculation – EXPOSE-E simulation results. Ref: EXP-RP-017-RS ISS. A (2). RedShift Design and Engineering BVBA (125 pp).
Sadowsky, A. & Ott, S. (2012). Photosynthetic symbionts in Antarctic terrestrial ecosystems: the physiological response of lichen photobionts to drought and cold. Symbiosis 58(1–3), 8190.
Sánchez, F.J., Meeßen, J., Ruiz, M., Sancho, L.G., Ott, S., Vílchez, C., Horneck, G., Sadowsky, A. & de la Torre, R. (2014). UV-C tolerance of symbiotic Trebouxia sp. in the space-tested lichen species Rhizocarpon geographicum and Circinaria gyrosa: role of the hydration state and cortex/screening substances. Int. J. Astrobiol. 13(1), 118.
Sancho, L.G., de la Torre, R., Horneck, G., Ascaso, C., de los Rios, A., Pintado, A., Wierzchos, J. & Schuster, M. (2007). Lichens survive in space: results from the 2005 LICHENS experiment. Astrobiology 7(3), 443454.
Sancho, L.G., de la Torre, R. & Pintado, A. (2008). Lichens, new and promising material from experiments in astrobiology. Fungal Biol. Rev. 22(3), 103109.
Scalzi, G., Selbmann, L., Zucconi, L., Rabbow, E., Horneck, G., Albertano, P. & Onofri, S. (2012). LIFE Experiment: isolation of cryptoendolithic organisms from Antarctic colonized sandstone exposed to space and simulated Mars conditions on the International Space Station. Orig. Life Evol. Biosph. 42(2–3), 253262.
Schaper, G.M. (2003). Komplexe Interaktionsmuster und die Dynamik von Entwicklungsprozessen in Flechtenökosystemen. Dissertation at the Heinrich-Heine University, ULB Düsseldorf, pp. 1220.
Schlensog, M., Schroeter, B., Pannewitz, S. & Green, T.G.A. (2003). Adaptation of mosses and lichens to irradiance stress in maritime and continental antarctic habitats. In Antarctic Biology in a Global Context, ed. Huiskes, A.H.L., Gieskes, W.W.C., Rozema, J., Schorno, R.M.L., van der Vies, S.M., Wolff, W.J., pp. 161166. Backhuys Publisher, Leiden.
Schroeter, B., Green, T.G.A., Seppelt, R.D. & Kappen, L. (1992). Monitoring photosynthetic activity of crustose lichens using a PAM-2000 fluorescence system. Oecologia 92(4), 457462.
Schuster, M., Dachev, T., Richter, P. & Häder, D.P. (2012). R3DE: radiation risk radiometer-dosimeter on the International Space Station—optical radiation data recorded during 18 months of EXPOSE-E exposure to open space. Astrobiology 12(5), 393402.
Shuster, D.L. & Weiss, B.P. (2005). Martian surface paleotemperatures from thermochronology of meteorites. Science 309(5734), 594600.
Smith, D. (1982). Liquid nitrogen storage of fungi. Trans. Br. Mycol. Soc. 79(3), 415421.
Solhaug, K.A. & Gauslaa, Y. (1996). Parietin, a photoprotective secondary product of the lichen Xanthoria parietina . Oecologia 108(3), 412418.
Solhaug, K.A. & Gauslaa, Y. (2004). Photosynthates stimulate the UV-B induced fungal anthraquinone synthesis in the foliose lichen Xanthoria parietina . Plant, Cell Environ. 27(2), 167176.
Solhaug, K.A., Gauslaa, Y., Nybakken, L. & Bilger, W. (2003). UV-induction of sun-screening pigments in lichens. New Phytol. 158(1), 91100.
Solhaug, K.A., Larsson, P. & Gauslaa, Y. (2010). Light screening in lichen cortices can be quantified by chlorophyll fluorescence techniques for both reflecting and absorbing pigments. Planta 231(5), 10031011.
Stöffler, D., Horneck, G., Ott, S., Hornemann, U., Cockell, C.S., Moeller, R., Meyer, C., de Vera, J.P., Fritz, J. & Artemieva, N.A. (2007). Experimental evidence for the potential impact ejection of viable microorganisms from Mars and Mars-like planets. Icarus 186(2), 585588.
Thomson, W. (1871). Presidential address to the British Association for the Advancement of Science. Nature 4, 262270.
Westall, F. (2013). Microbial scale habitability on Mars. In Habitability of Other Planets; Cellular Origin, Life in Extreme Habitats and Astrobiology, 28. Springer, Springer Dordrecht, NL, pp. 183202.
Wieners, P.C., Mudimu, O. & Bilger, W. (2012). Desiccation-induced non-radiative dissipation in isolated green lichen algae. Photosynth. Res. 113(1–3), 239247.
Wynn-Williams, D.D., Edwards, H.G.M., Newton, E.M. & Holder, J.M. (2002). Pigmentation as a survival strategy for ancient and modern photosynthetic microbes under high ultraviolet stress on planetary surfaces. Int. J. Astrobiol. 1(1), 3949.


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Viability of the lichen Xanthoria elegans and its symbionts after 18 months of space exposure and simulated Mars conditions on the ISS

  • Annette Brandt (a1), Jean-Pierre de Vera (a2), Silvano Onofri (a3) and Sieglinde Ott (a1)


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