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

Published online by Cambridge University Press:  18 November 2014

T. Backhaus ,
R. de la Torre ,
K. Lyhme ,
J.-P. de Vera  and
J. Meeßen
T. Backhaus
Affiliation:
Institut für Botanik, Heinrich-Heine-Universität (HHU), Universitätsstr.1, 40225 Düsseldorf, Germany
R. de la Torre
Affiliation:
Instituto Nacional de Técnica Aeroespacial (INTA), Ctra. de Ajalvir km. 4, 28850 Torrejón de Ardoz, Madrid, Spain
K. Lyhme
Affiliation:
Institut für Botanik, Heinrich-Heine-Universität (HHU), Universitätsstr.1, 40225 Düsseldorf, Germany
J.-P. de Vera
Affiliation:
Institut für Planetenforschung, Deutsches Zentrum für Luft- und Raumfahrt (DLR), Rutherfordstraße 2, 12489 Berlin, Germany
J. Meeßen*
Affiliation:
Institut für Botanik, Heinrich-Heine-Universität (HHU), Universitätsstr.1, 40225 Düsseldorf, Germany
*
e-mail: [email protected]
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Abstract

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.

Keywords

astrobiologyBIOMEXextremotolerancelichensphotobiontphotodamageUVC.
Type
Research Article
Information
International Journal of Astrobiology , Volume 14 , Issue 3 , July 2015 , pp. 479 - 488
Copyright
Copyright © Cambridge University Press 2014 

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References

Ahmadjian, V. (1967). A guide to the algae occuring as lichen symbionts: isolation, culture, cultural physiology, and identification. Phycology 6, 127–160.Google Scholar
Aro, E.M., Virgin, I. & Andersson, B. (1993). Photoinhibition of photosystem II. Inactivation, protein damage and turnover. Biochim. Biophys. Acta 1143, 113–134.CrossRefGoogle ScholarPubMed
Beblo, K., Rabbow, E., Rachel, R., Huber, H. & Rettberg, P. (2009). Tolerance of thermophilic and hyperthermophilic micro-organisms to desiccation. Extremophiles 13, 521–531.Google Scholar
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), 387–392.Google Scholar
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: http://dx.doi.org/10.1017/S1473550414000214.Google Scholar
Britt, A.B. (1999). Molecular genetics of DNA repair in higher plants. Trends Plant Sci. 4, 20–25.CrossRefGoogle ScholarPubMed
Cockell, C.S. (2014). Trajectories of Martian habitability. Astrobiology 14(2), 182–203.Google Scholar
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, 343–359.CrossRefGoogle ScholarPubMed
Crowe, J.H., Hoekstra, F.A. & Crowe, L.M. (1992). Anhydrobiosis. Annu. Rev. Physiol. 54, 579–599.Google Scholar
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), 1–13.Google Scholar
Darbishire, O.V. (1910). Lichenes. National Antarctic Expedition 1901–1904. Natural History 5, Zoology and Botany, 1–11.Google Scholar
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), 1665–1671.Google Scholar
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), 735–748.Google Scholar
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. 595–611. Springer, the Netherlands.Google Scholar
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, 285–293.Google Scholar
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, 1236–1243.Google Scholar
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.Google Scholar
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, 457–468.Google Scholar
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, 215–227.Google Scholar
Ertl, L. (1951). Über die Lichtverhältnisse in Laubflechten. Planta 39, 245–270.Google Scholar
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, 32–33.Google Scholar
Häubner, N., Schumann, R. & Karsten, U. (2006). Aeroterrestrial microalgae growing in biofilms on facades – response to temperature and water stress. Microb. Ecol. 51, 285–293.Google Scholar
Horneck, G. (1999). European activities in exobiology in earth orbit: results and perspectives. Adv. Space Res. 23(2), 381–386.Google Scholar
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. 291–336. Springer, New York.Google Scholar
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), 17–44.CrossRefGoogle ScholarPubMed
Jahns, H.M. (1988). The lichen thallus. In CRC Handbook of Lichenology, ed. Galun, M., vol. I, pp. 95–143. CRC Press, Boca Ranton, FL.Google Scholar
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, 217–223.Google Scholar
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), 131–135.Google Scholar
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, 117–138.Google Scholar
Kappen, L. (2000). Some aspects of the great success of lichens in Antarctica. Antarct. Sci. 12(3), 314–324.Google Scholar
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), 119–128.Google Scholar
Kieft, T.L. & Ahmadjian, V. (1989). Biological ice nucleation activity in lichen mycobionts and photobionts. Lichenologist 21(4), 355–362.Google Scholar
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), 879–888.Google Scholar
Kranner, I. & Birtić, S. (2005). A modulating role for antioxidants in desiccation tolerance. Integr. Comp. Biol. 45(5), 734–740.Google Scholar
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), 3141–3146.Google Scholar
Kranner, I., Beckett, R., Hochman, A. & Nash, T.H. III (2008). Desiccation-tolerance in lichens: a review. Bryologist 111(4), 576–593.Google Scholar
Lüttge, U. & Büdel, B. (2010). Resurection kinetics of photosynthesis in desiccation-tolerant terrestrial green-algae (Chlorophyta) on tree bark. Plant Biology 12, 437–444.Google Scholar
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. 9–77. Cambridge University Press, Cambridge.CrossRefGoogle Scholar
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), 283–303. online-first publ. (2013).Google Scholar
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), 501–526. online-first publ. (2013).Google Scholar
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)Google Scholar
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), 39–48.Google Scholar
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, 249–264.Google Scholar
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, 781–787.Google Scholar
Onofri, S. et al. (2012). Survival of rock-colonizing organisms after 1.5 years in outer space. Astrobiology 12(5), 508–516.Google Scholar
Øvstedal, D.O. & Lewis Smith, R.I. (2001). Lichens of Antarctica and South Georgia. A Guide to their Identification and Ecology, pp. 66–365. Cambridge University Press, Cambridge.Google Scholar
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), 1351–1359.Google Scholar
Pannewitz, S., Schlensog, M., Green, T.G.A., Sancho, L.G. & Schroeter, B. (2002). Are lichens active under snow in continental Antarctica? Oecologia 135, 30–38.Google Scholar
Rabbow, E. et al. (2012). EXPOSE-E: an ESA astrobiology mission 1.5 years in space. Astrobiology 12(5), 374–386.Google Scholar
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), 281–292.CrossRefGoogle ScholarPubMed
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), 164–171.Google Scholar
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, 125–136.Google Scholar
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).Google Scholar
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), 22–28.Google Scholar
Sadowsky, A. & Ott, S. (2012). Photosynthetic symbionts in Antarctic terrestrial ecosystems: the physiological response of lichen photobionts to drought and cold. Symbiosis 58, 81–90.Google Scholar
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), 102–110.Google Scholar
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), 1–18.Google Scholar
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, 137–147.Google Scholar
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), 443–454.Google Scholar
Sancho, L.G., de la Torre, R. & Pintado, A. (2008). Lichens, new and promising material from experiments in astrobiology. Fungal Biol. Rev. 22, 103–109.Google Scholar
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), 55–62.Google Scholar
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, 253–262.Google Scholar
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. 161–166. Backhuis Publishers, Leiden.Google Scholar
Schreiber, U., Bilger, W. & Neubauer, C. (1994). Chlorophyll fluorescence as a non-intrusive indicator for rapid assessment of in vivo photosynthesis. Ecol. Stud. 100, 49–70.Google Scholar
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), 393–402.Google Scholar
Sohrabi, M. (2012). Taxonomy and phylogeny of the manna lichens and allied species (Megasporaceae). PhD Thesis, Publications in Botany from the University of Helsinki. http://urn.fi/URN:ISBN:978-952-10-7400-4 Google Scholar
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, 585–588.Google Scholar
Strid, Å., Chow, W.S. & Anderson, J.M. (1994). UV-B damage and protection at the molecular level in plants. Photosynth. Res. 39(3), 475–489.Google Scholar
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, 259–270.Google Scholar
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), 181–187.Google Scholar
Teramura, A.H. & Sullivan, J.H. (1994). Effects of UV-B radiation on photosynthesis and growth of terrestrial plants. Photosynth. Res 39, 463–473.Google Scholar
Valladares, F., Sancho, L.G. & Ascaso, C. (1997). Water storage in the lichen family Umbilicariaceae. Bot. Acta 111, 99–107.Google Scholar
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. 931–949. Marcel Dekker Inc., New York.Google Scholar
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), 605–615.Google Scholar
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. 3–33, Springer, Berlin.Google Scholar