Skip to main content Accessibility help

Desiccation and low temperature attenuate the effect of UVC254 nm in the photobiont of the astrobiologically relevant lichens Circinaria gyrosa and Buellia frigida

  • T. Backhaus (a1), R. de la Torre (a2), K. Lyhme (a1), J.-P. de Vera (a3) and J. Meeßen (a1)...


Several investigations on lichen photobionts (PBs) after exposure to simulated or real-space parameters consistently reported high viability and recovery of photosynthetic activity. These studies focused on PBs within lichen thalli, mostly exposed in a metabolically inactive state. In contrast, a recent study exposed isolated and metabolically active PBs to the non-terrestrial stressor UVC254 nm and found strong impairment of photosynthetic activity and photo-protective mechanisms (Meeßen et al. in 2014b). Under space and Mars conditions, UVC is accompanied by other stressors as extreme desiccation and low temperatures. The present study exposed the PBs of Buellia frigida and Circinaria gyrosa, to UVC in combination with desiccation and subzero temperatures to gain better insight into the combined stressors' effect and the PBs' inherent potential of resistance. These effects were examined by chlorophyll a fluorescence which is a good indicator of photosynthetic activity (Lüttge & Büdel in 2010) and widely used to test the viability of PBs after (simulated) space exposure. The present results reveal fast recovery of photosynthetic activity after desiccation and subzero temperatures. Moreover, they demonstrate that desiccation and cold confer an additional protective effect on the investigated PBs and attenuate the PBs' reaction to another stressor – even if it is a non-terrestrial one such as UVC. Besides other protective mechanisms (anhydrobiosis, morphological–anatomical traits and secondary lichen compounds), these findings may help to explain the high resistance of lichens observed in astrobiological studies.


Corresponding author


Hide All
Ahmadjian, V. (1967). A guide to the algae occuring as lichen symbionts: isolation, culture, cultural physiology, and identification. Phycology 6, 127160.
Aro, E.M., Virgin, I. & Andersson, B. (1993). Photoinhibition of photosystem II. Inactivation, protein damage and turnover. Biochim. Biophys. Acta 1143, 113134.
Beblo, K., Rabbow, E., Rachel, R., Huber, H. & Rettberg, P. (2009). Tolerance of thermophilic and hyperthermophilic micro-organisms to desiccation. Extremophiles 13, 521531.
Berger, T., Hajek, M., Bilski, P., Körner, C., Vanhavere, P. & Reitz, G. (2012). Cosmic radiation exposure of biological test systems during the EXPOSE-E mission. Astrobiology 12(5), 387392.
Brandt, A., de Vera, J.-P., Onofri, S. & Ott, S. (2014). Viability of the lichen Xanthoria elegans and its symbionts after 18 months of space exposure and simulated Mars conditions on the ISS. International Journal of Astrobiology, published online 24 July 2014, doi:
Britt, A.B. (1999). Molecular genetics of DNA repair in higher plants. Trends Plant Sci. 4, 2025.
Cockell, C.S. (2014). Trajectories of Martian habitability. Astrobiology 14(2), 182203.
Cockell, C.S., Catling, D., Davis, W.L., Kepner, R.N., Lee, P.C., Snook, K. & McKay, C.P. (2000). The ultraviolet environment of Mars: biological implications past, present and future. Icarus 146, 343359.
Crowe, J.H., Hoekstra, F.A. & Crowe, L.M. (1992). Anhydrobiosis. Annu. Rev. Physiol. 54, 579599.
Cruces, E., Huovinen, P. & Gómez, I. (2013). Interactive effects of UV radiation and enhanced temperature on photosynthesis, phlorotannin induction and antioxidant activities of two sub-Antarctic brown algae. Marine Biol. 160(1), 113.
Darbishire, O.V. (1910). Lichenes. National Antarctic Expedition 1901–1904. Natural History 5, Zoology and Botany, 111.
de la Torre, 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, R., et al. (2010). Survival of lichens and bacteria exposed to outer space conditions – Results of the Lithopanspermia experiments. Icarus 208(2), 735748.
de Vera, J.P. & Ott, S. (2010). Resistance of symbiotic eukaryotes. Survival to simulated space conditions and asteroid impact cataclysms. In Symbioses and Stress: Joint Ventures in Biology. Cellular Origin, Life in Extreme Habitats and Astrobiology, ed. Seckbach, J. & Grube, M., vol. 17, pp. 595611. Springer, the Netherlands.
de Vera, J.P., Horneck, G., Rettberg, P. & Ott, S. (2003). The potential of the lichen symbiosis to cope with the 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, 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, 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 Astrobiology. ESA SP-545, ESA Publications Division, ESTEC, Noordwijk, pp. 197–198.
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, 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, 215227.
Ertl, L. (1951). Über die Lichtverhältnisse in Laubflechten. Planta 39, 245270.
Harańczyk, H., Ligezowska, A. & Olech, M.A. (2003). Desiccation resistance of the lichen Turgidosculum complicatulum and its photobiont Prasiola crispa by proton magnetic relaxation, and sorption isotherm. Inst. Nucl. Phys. 32, 3233.
Häubner, N., Schumann, R. & Karsten, U. (2006). Aeroterrestrial microalgae growing in biofilms on facades – response to temperature and water stress. Microb. Ecol. 51, 285293.
Horneck, G. (1999). European activities in exobiology in earth orbit: results and perspectives. Adv. Space Res. 23(2), 381386.
Horneck, G., Baumstark-Khan, C. & Facius, R. (2006). Radiation biology. In Fundamentals of Space Biology, ed. Clément, G. & Slenska, K., Space Technology Library, 18, pp. 291336. Springer, New York.
Horneck, G. et al. (2008). Microbial rock inhabitants survive hypervelocity impacts on Mars-like host planets: first phase of lithopanspermia experimentally tested. Astrobiology 8(1), 1744.
Jahns, H.M. (1988). The lichen thallus. In CRC Handbook of Lichenology, ed. Galun, M., vol. I, pp. 95143. CRC Press, Boca Ranton, FL.
Jansen, M.A.K., Babu, T.S., Heller, D., Gaba, V., Mattoo, A.K. & Edelman, M. (1996). Ultraviolet-B effects on Spirodela oligorhiza: induction of different protection mechanisms. Plant Sci. 115, 217223.
Jansen, M.A.K., Gaba, V. & Greenberg, B.M. (1998). Higher plants and UV-B radiation: balancing damage, repair and acclimation. Trends Plant Sci. 3(4), 131135.
Jenkins, G.I., Christie, J.M., Fuglevand, G., Long, J.C. & Jackson, J.A. (1995). Plant responses to UV and blue light: biochemical and genetic approaches. Plant Science 112, 117138.
Kappen, L. (2000). Some aspects of the great success of lichens in Antarctica. Antarct. Sci. 12(3), 314324.
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.
Kieft, T.L. & Ahmadjian, V. (1989). Biological ice nucleation activity in lichen mycobionts and photobionts. Lichenologist 21(4), 355362.
Kosugi, M., Arita, M., Shizuma, R., Moriyama, Y., Kashino, Y., Koike, H. & Satoh, K. (2009). Responses to desiccation stress in lichens are different from those in their photobionts. Plant Cell Physiol. 50(4), 879888.
Kranner, I. & Birtić, S. (2005). A modulating role for antioxidants in desiccation tolerance. Integr. Comp. Biol. 45(5), 734740.
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. U. S. A. 102(8), 31413146.
Kranner, I., Beckett, R., Hochman, A. & Nash, T.H. III (2008). Desiccation-tolerance in lichens: a review. Bryologist 111(4), 576593.
Lüttge, U. & Büdel, B. (2010). Resurection kinetics of photosynthesis in desiccation-tolerant terrestrial green-algae (Chlorophyta) on tree bark. Plant Biology 12, 437444.
Marchant, D.R. & Head, J.W. (2010). Geologic analogies between the surface of Mars and the McMurdo dry Valleys: microclimate-related geomorphic features and evidence for climate change. In Life in Antarctic Deserts and Other Cold Dry Environments, ed. Doran, P.T., Lyons, W.B. & McKnight, D.M., pp. 977. Cambridge University Press, Cambridge.
Meeßen, J., Sánchez, F.J., Brandt, A., Balzer, E.M., de la Torre, R., Sancho, L.G., de Vera, J.P. & Ott, S. (2013). 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. online-first publ. (2013).
Meeßen, J., Sánchez, F.J., Sadowsky, A., de Vera, J.P., de la Torre, R. & Ott, S. (2014a). Extremotolerance and resistance of lichens: comparative studies on five lichen species used in astrobiological research II. Secondary lichen compounds. Orig. Life Evol. Biosph. 43(6), 501526. online-first publ. (2013).
Meeßen, J., Backhaus, T., Sadowsky, A., Mrkalj, M., Sánchez, F.J., de la Torre, R. & Ott, S. (2014b). Effects of UVC254 nm on the photosynthetic activity of photobionts from the astrobiologically relevant lichens Buellia frigida and Circinaria gyrosa . Int. J. Astrobiol. (in print, doi: 10.1017/S1473550414000275)
Nasibi, F. & M'Kalantari, K.H. (2005). The effects of UV-A, UV-B and UV-C on protein and ascorbate content, lipid peroxidation and biosynthesis of screening compounds in Brassica napus . Iran. J. Sci. Technol., Trans. A 29(A1), 3948.
Nicholson, W.L., Schuerger, A.C. & Setlow, P. (2005). The solar UV environment and bacterial spore UV resistance: considerations for Earth-to-Mars transport by natural processes and human spaceflight. Mutat. Res. 571, 249264.
Nogués, S. & Baker, N.R. (1995). Evaluation of the role of damage to photosystem II in the inhibition of CO2 assimilation in pea leaves on exposure to UV-B radiation. Plant Cell Environ. 18, 781787.
Onofri, S. et al. (2012). Survival of rock-colonizing organisms after 1.5 years in outer space. Astrobiology 12(5), 508516.
Øvstedal, D.O. & Lewis Smith, R.I. (2001). Lichens of Antarctica and South Georgia. A Guide to their Identification and Ecology, pp. 66365. Cambridge University Press, Cambridge.
Pandey, V., Ranjan, S., Deeba, F., Pandey, A.K., Singh, R., Shirke, P.A. & Pathre, U.V. (2010). Desiccation-induced physiological and biochemical changes in resurrection plant, Selaginella bryopteris . Plant Physiol. 167(16), 13511359.
Pannewitz, S., Schlensog, M., Green, T.G.A., Sancho, L.G. & Schroeter, B. (2002). Are lichens active under snow in continental Antarctica? Oecologia 135, 3038.
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.
Rahimzadeh, P., Hosseini, S. & Dilmaghani, K. (2011). Effects of UV-A and UV-C radiation on some morphological and physiological parameters in savory (Satureja hortensis L.). Ann. Biol. Res. 2(59), 164171.
Rao, M.V., Paliyath, G. & Ormrod, D.P. (1996). Ultraviolet-B- and ozone-induced biochemical changes in antioxidant enzymes of Arabidopsis thaliana . Plant Physiol. 110, 125136.
RedShift, Report. Reviewers: van Bavinchove, C., Beuselinck, T. (2011). EXPOSE: environmental history by calculation – EXPOSE-E simulation results. Ref: EXP-RP-017-RS ISS.A(2). RedShift Design and Engineering BVBA (125pp).
Rozema, J., van de Staaij, J., Björn, L.O. & Caldwell, M. (1997). UV-B as an environmental factor in plant life: stress and regulation. TREE 12(1), 2228.
Sadowsky, A. & Ott, S. (2012). Photosynthetic symbionts in Antarctic terrestrial ecosystems: the physiological response of lichen photobionts to drought and cold. Symbiosis 58, 8190.
Sánchez, F.J., Mateo-Martí, E., Raggio, J., Meeßen, J., Martínez-Frías, J., Sancho, L.G., Ott, S. & de la Torre, R. (2012). The resistance of the lichen Circinaria gyrosa (nom. provis.) towards simulated Mars conditions − a model test for the survival capacity of an eukaryotic extremophile. Planet. Space Sci. 72(1), 102110.
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., Schroeter, B. & del Prado, R. (2000). Ecophysiology and morphology of the globular erratic lichen Aspicilia fruticulosa (Eversm.) Flag. from Central Spain. Bibl. Lichenol. 7, 137147.
Sancho, L.G., de la Torre, R., Horneck, G., Ascaso, C., de los Ríos, A., Pintado, A., Wierzchos, J. & Schuster, M. (2007). Lichens survive in space: results from 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, 103109.
Sass, L., Spetea, C., Máté, Z., Nagy, F. & Vass, I. (1997). Repair of UV-B induced damage of Photosystem II via de novo synthesis of D1 and D2 reaction centre subunits in Synechocystis sp. PCC 6803. Photosynth. Res. 54(1), 5562.
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, 253262.
Schlensog, M., Schroeter, B., Pannewitz, S. & Green, T.G.A. (2003). Adaptation of mosses and lichens to irridiance 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. & Wolf, W.J., pp. 161166. Backhuis Publishers, Leiden.
Schreiber, U., Bilger, W. & Neubauer, C. (1994). Chlorophyll fluorescence as a non-intrusive indicator for rapid assessment of in vivo photosynthesis. Ecol. Stud. 100, 4970.
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.
Sohrabi, M. (2012). Taxonomy and phylogeny of the manna lichens and allied species (Megasporaceae). PhD Thesis, Publications in Botany from the University of Helsinki.
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 189, 585588.
Strid, Å., Chow, W.S. & Anderson, J.M. (1994). UV-B damage and protection at the molecular level in plants. Photosynth. Res. 39(3), 475489.
Suzuki, N., Koussevitzki, S., Mittler, R. & Miller, G. (2012). ROS and redox signalling in the response of plants to abiotic stress. Plant Cell Environ. 35, 259270.
Takeuchi, Y., Murakami, M., Nakajima, N., Kondo, N. & Nikaido, O. (1996). Induction of repair and damage to DNA in cucumber cotyledons irradiated with UV-B. Plant Cell Physiol. 37(2), 181187.
Teramura, A.H. & Sullivan, J.H. (1994). Effects of UV-B radiation on photosynthesis and growth of terrestrial plants. Photosynth. Res 39, 463473.
Valladares, F., Sancho, L.G. & Ascaso, C. (1997). Water storage in the lichen family Umbilicariaceae. Bot. Acta 111, 99107.
Vass, I., Szilárd, A. & Sicora, C. (2005). Adverse effects of UV-B light on the structure and function of the photosynthetic apparatus. In Handbook of Photosynthesis, ed. Pessarakli, M., pp. 931949. Marcel Dekker Inc., New York.
Wassmann, M., Moeller, R., Reitz, G. & Rettberg, P. (2010). Adaptation of Bacillus subtilis cells to Archean-like UV climate: relevant hints of microbial evolution to remarkably increased radiation resistance. Astrobiology 10(6), 605615.
Yoshimura, I., Yamamoto, Y., Nakano, T. & Finnie, J. (2002). Isolation and culture of lichen photobionts and mycobionts. In Protocols in Lichenology. Culturing, Biochemistry, Ecophysiology and Use in Biomonitoring, ed. Krammer, I., Beckett, R. & Varma, A., pp. 333, Springer, Berlin.


Desiccation and low temperature attenuate the effect of UVC254 nm in the photobiont of the astrobiologically relevant lichens Circinaria gyrosa and Buellia frigida

  • T. Backhaus (a1), R. de la Torre (a2), K. Lyhme (a1), J.-P. de Vera (a3) and J. Meeßen (a1)...


Full text views

Total number of HTML views: 0
Total number of PDF views: 0 *
Loading metrics...

Abstract views

Total abstract views: 0 *
Loading metrics...

* Views captured on Cambridge Core between <date>. This data will be updated every 24 hours.

Usage data cannot currently be displayed.