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

International Journal of Astrobiology

Volumn 13, Issue 1, 2014, Pages 1-18

  Sánchez, Francisco Javier ^a   Meeen, Joachim ^b   Ruiz, M B Del Carmen ^c   G Sancho, Leopoldo ^d   Ott, Sieglinde ^b   Vílchez, Carlos ^c   Horneck, Gerda ^e   Sadowsky, Andres ^b   De La Torre, Rosa ^a  

^a Torrejón de Ardoz ^*  (Spain)

^b HEINRICH HEINE UNIVERSITY   (Germany)

^c UNIVERSITY OF HUELVA   (Spain)

^d UNIVERSIDAD COMPLUTENSE DE MADRID   (Spain)

^e GERMAN AEROSPACE CENTER DLR   (Germany)

Author keywords

Astrobiology; Circinaria gyrosa; extremophile; Rhizocarpon geographicum; Trebouxia sp.; UV C radiation

Indexed keywords

GREEN ALGA; HYDRATION; LICHEN; LIQUID CHROMATOGRAPHY; PHOTOSYNTHESIS; PHYSIOLOGY; SURVIVAL; ULTRAVIOLET RADIATION;

EID: 84891809500     PISSN: 14735504     EISSN: 14753006     Source Type: Journal    
DOI: 10.1017/S147355041300027X     Document Type: Article

References (95)

1. Ahmadjian, V. (1992). Basic mechanisms of signal exchange, recognition, and regulation lichens. Algae and Symbiosis, ed. Reisser, W., 675-697. Biopress Limited, Bristol.
2. Armstrong, G.A. & Hearst, J.E. (1996). Genetics and molecular biology of carotenoid pigment biosynthesis. FASEB J. 10, 228-237. (Pubitemid 26079942)
3. Atwell, B.J., Kriedemann, P.E. & Turnbull, C.G.N. (eds) (1999). Plants Action: Adaptation Nature, Performance Cultivation. Macmillan Education, Australia.
4. Björn, L.O. (2007). Stratospheric ozone, ultraviolet radiation and cryptogams. Biological Conservation 135(3), 326-333. (Pubitemid 46048749)
5. Bornman, J.F. (1989). Target sites of UV-B radiation photosynthesis of higher plants. J. Photochem. Photobiol. B: Biol. 4, 145-158.
6. Britt, A.B. (1999). Molecular genetics of DNA repair higher plants. Trends Plant Sci. 4(1), 20-25. (Pubitemid 29130800)
7. Brodo, I.M., Sharnoff, S.D. & Sharnoff, S. (2001). Lichens of North America. Yale University Press, New Haven, CT.
8. Bubrick, P., Galun, M. & Frensdorff, A. (1984). Observations on free-living Trebouxia de Puymaly and Pseudotrebouxia Archibald, and evidence that both symbionts from Xanthoria-Parientina (L.) Th. Fr. can be found free-living nature. New Phytol. 97, 455-462.
9. Buffoni Hall, R. (2002). Effects of increased UV-B radiation on the lichen Cladonia arbuscula smitis: UV-absorbing pigments and DNA damage.
10. PhD Dissertation, Department of Cell and Organism Biology, Lund University, Sweden. http://tinyurl.com/d49kkbq Castenholz, R.W. & Garcia-Pichel, F. (2002). Cyanobacterial responses to UV-radiation. The Ecology of Cyanobacteria, ed. Whitton, B.A. & Potts, M., 591-611. Kluwer Academic Publishers, Dordrecht.
11. Castenholz, R.W. & Garcia-Pichel, F. (2012). Cyanobacterial responses to UV radiation. Ecology of Cyanobacteria II, ed. Whitton, E. & Brian, A., 481-499. Springer, The Netherlands.
12. Cockell, C.S. & Knowland, J. (1999). Ultraviolet radiation screening compounds. Biol. Rev. Camb. Philos. Soc. 74(3), 311-345. (Pubitemid 29381273)
13. Culberson, C.F. (1979). Chemical and Botanical Guide to Lichen Products. Otto Koeltz Science Publishers, Koenigstein, 41, 161.
14. de la Torre Noetzel, R. (2002). Estudio de los efectos de la radiación UV sobre ecosistemas epilíticos. Tesis Doctoral, Universidad Complutense de Madrid.
15. de la Torre Noetzel, R., Sancho, L.G., Pintado, A., Rettberg, P., Rabbow, E., Panitz, C., Deutschmann, U., Reina, M. & Horneck, G. (2007a). BIOPAN experiment LICHENS on the Foton M2 mission Pre-flight verification tests of the Rhizocarpon geographicum-granite ecosystem. Adv. Space Res. 40, 1665-1671. (Pubitemid 350016471)
16. de la Torre, R., Garcia-Sancho, L. & Horneck, G. (2007b). Adaptation of the lichen Rhizocarpon geographicum to harsh high altitude conditions: relevance to a habitable Mars. Responses of Organisms to Simulated Mars Environment (ROME), ed. Cockell, C.S. & Horneck, G., 145-150, ESA-SP 1299, ESA Publications Division, ESTEC, Noordwijk, The Netherlands.
17. 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.
18. de los Ríos, A., Ascaso, C., Wierzchos, J., Sancho, L.G. & Green, T.G.A. (2010). Space flight effects on lichen ultrastructure and physiology. 'Symbioses and Stress: Joint Ventures Biology' Cellular Origin, Life Extreme Habitats and Astrobiology, ed. Seckbach, J. & Grube, M., 17, 577-593. Springer, Netherland.
19. de Vera, J.(2005). Grenzen des Überlebens: Flechten als Modellsystem für das Potential von Adaptationsmechanismen eines Symbioseorganismus unter Extrembedingungen. PhD Thesis, Heinrich-Heine-University, Düsseldorf.
20. de Vera, J.-& Ott, S. (2010b). Resistance of symbiotic eukaryotes. Survival to simulated space conditions and asteroid impact cataclysms. 'Symbioses and Stress: Joint Ventures Biology' Cellular Origin, Life Extreme Habitats and Astrobiology, ed. Seckbach, J.&Grube, M., 17, 595-611. Springer, Netherland.
21. de Vera, J.P., Boettger, U., de la Torre, R., Sánchez, F.J., Grunow, D., Schmitz, N., Lange, C., Hübers, H.-W., Jaumann, R., Spohn, T. & Co-I team of BIOMEX (2012). Supporting Mars exploration: BIOMEX Low Earth Orbit and further astrobiological studies on the Moon using Raman and PanCam technology. Planet. Space Sci. 74, 103-110.
22. Fahselt, D. (1994). Secondary biochemistry of lichens. Symbiosis 16, 117-165. (Pubitemid 2089338)
23. Feuerer, T. (1991). Revision der europäischen Arten der Flechtengattung Rhizocarpon mit nichtgelben Lager und vielzelligen Sporen. Bibl. Lichenol. 39, 1-218.
24. Floudas, D. et al. (2012). The Palaeozoic origof enzymatic ligndecomposition reconstructed from 31 fungal genomes. Science 336 (6089), 1715-1719.
25. Friedl, (1995). Inferring taxonomic positions and testing genus level assignments coccoid green lichen algae: a phylogenetic analysis of dl8S ribosomal RNA sequences from Dictyochlorposis reticulata and from members of the genus Myrmecia (Chlorophyta, Trebouxiophyceae cl. nov). J. Phycol. 31, 632-639.
26. Gao, Y., Cui, Y., Xiong,W., Li, X. & Wu, Q. (2009). Effect of UV-C on algal evolution and differences growth rate, pigmentation and photosynthesis between prokaryotic and eukaryotic algae. Photochem. Photobiol. 85, 774-782.
27. Gargaud, M. (editor-in-chief), Amils, R., Cernicharo Quintanilla, J., Cleaves, H.J., Irvine, W.M., Pinti, D., Viso, M., (eds) (2011). Encyclopedia of Astrobiology. ISBN 978-3-642-11279-9. http://www.springerreference.com/docs/ navigation.do?m=Encyclopedia+of +Astrobiology+(Physics+and+Astronomy)-book204.
28. Gärtner, G. (1992). Taxonomy of symbiotic eukaryotic algae. Algae and Symbioses: Plants, Animals, Fungi, Viruses. Interactions Explored, ed. Reisser, W., 325-338. Biopress Ltd, Bristol.
29. Gasulla, F. (2009). Insights on desiccation tolerance of the lichen photobiont Trebouxia spl. both thalline and isolated ones. PhD Thesis, Universitat de València Servei de Publicacions 2010. http://hdl.handle. net/10803/39081
30. Gautam, S., Singh, J. & Pant, A.B. (2011). Effect of UV-B radiations on the pigments of two Antarctic lichens of Schirmacher Oasis, East Antarctica. Pol. Polar Res. 32(3), 279-287.
31. Green, T.G.A. & Lange, O.L. (1994). Photosynthesis Poikilohydric Plants: A Comparison of Lichens and Bryophytes. Ecophysiology of Photosynthesis (Springer Study Edition), 100, 319-341. Springer, Berlin, Heidelberg.
32. Heber, U., Soni, V. & Strasser, R.J. (2011). Photoprotection of reaction centers: thermal dissipation of absorbed light energy vs charge separation lichens. Physiol. Plantarum 142(1), 65-78.
33. Hedges, S.B., Blair, J.E., Venturi, M.L. & Shoe, J.L. (2004). A molecular timescale of eukaryote evolution and the rise of complex multicellular life. BMC EBiol. 4, 2.
34. Henssen, A. & Jahns, H.M. (1974). Lichenes.-Georg Thieme. Verlag, Stuttgart. Holder, J.M. (1998). FT-Raman Spectroscopy of Antarctic Epilithic Lichens. PhD Thesis, University of Bradford, Bradford.
35. Horneck, G. (1999). European activities exobiology earth orbit: results and perspectives. Adv. Space Res. 23(2), 381-386. (Pubitemid 129523503)
36. Horneck, G., Rettberg, P., Reitz, G., Wehner, J., Eschweiler, U., Strauch, K., Panitz, C., Starke, V., Baumstark-Khan, C. (2001). Protection of bacterial spores space, a contribution to the discussion on Panspermia. Orig. Life EBiosph. 31, 527-547. (Pubitemid 34003845)
37. Horneck, G., Baumstark-Khan, C. & Facius, R. (2006). Radiation biology. Fundamentals of Space Biology. Space Technology Library, 18, 291-336. Springer, New York.
38. Huneck, S. (1999). The significance of lichens and their metabolites. Naturwissenchaften 86, 559-570. (Pubitemid 30009978)
39. Huneck, S. & Yoshimura, I. (1996). Identification of Lichen Substances. Springer-Verlag, Berlin, Heidelberg, New York, 1-9.
40. Jansen, M.A.K., Mattoo, A.K. & Edelman, M. (1999). D1-D2 protedegradation the chloroplast. Complex light saturation kinetics. Eur. J. Biochem. 260, 527-532. (Pubitemid 29122552)
41. Kappen, L., Schroeter, B., Scheidegger, C., Sommerkorn, M. & Hestmark, G. (1996). Cold resistance and metabolic activity of lichens below 0 °C. Proceedings of the F3.1, F3.4, F2.4 and F3.8 Symposia of COSPAR Scientific Commission. Adv. Space Res. 18(12), 119-128.
42. Kasting, J.F. (1993). Earth's early atmosphere. Science 259(5097), 920-926.
43. Kirk, P.M., Cannon, P.F., David, J.C. & Stalpers, J.A. (2001). Ainsworth and Bisby's Dictionary of the Fungi, 9th edn. CAB International, Wallingford.
44. Kranner, I., Beckett, R., Hochman, A. & Nash, T.H. (2008). Desiccationtolerance Lichens: a review. Bryologist, 111(4), 576-593.
45. Kroken, S. & Taylor, J.W. (2000). Phylogenetic species, reproductive mode, and specificity of the green alga trebouxia forming lichens with the fungal genus Letharia. Bryologist 103(4), 645-660. (Pubitemid 32108953)
46. Lange, O.L. (1953). Hitze und Trockenresistenz der Flechten Beziehung zu ihrer Verbreitung. Flora 140, 39-97.
47. Lange, O.L., Bilger, W., Rinke, S. & Schreiber, U. (1989). Chlorophyll fluorescence of lichens containing green and blue-green algae during hydration by water vapor and by addition of liquid water. Bot. Acta 102, 306-313.
48. Lange, O.L., Green, T.G.A., Meyer, A. & Zellner, H. (2007). Water relations and carbon dioxide exchange of epiphytic lichens the Namib fog desert. Flora 202, 479-487. (Pubitemid 47126754)
49. Larkum, A.W.D. & Wood, W.F. (1993). The effect of UV-B radiation on photosynthesis and respiration of phytoplankton, benthic macroalgae and seagrasses. Photosynth. Res. 36, 17-23.
50. Larsson, P., Vecerová, K., Cempírková, H., Solhaug, K.A. & Gauslaa, Y. (2009). Does UV-B influence biomass growth lichens deficient sunscreening pigments? Environ. ExBot. 67, 215-221.
51. Lumbsch, H.T. et al. (2011). One hundred new species of lichenized fungi: a signature of undiscovered global diversity. Phytotaxa 18, 1-127.
52. Meeßen, J., Sánchez, F.J., Brandt, A., Balzer, E.-M., de la Torre, R., Sancho, L.G., de Vera, J.-& Ott, S. (2013). Extremotolerance and resistance towards space conditions lichens: Comparative studies on five species used astrobiological research I. Morphological and anatomical characteristics. Orig. Life EBiosph. 43(3), 283-303.
53. Mogedas, B., Casal, C., Forján, E. & Vílchez, C. (2009). Beta-carotene production enhancement by UV-A radiation Dunaliella bardawil cultivated laboratory reactors. J. Biosci. Bioeng. 108(1), 47-51.
54. Nash, T.H. (ed.) (2008). Lichen Biology, 2nd edn. Cambridge University Press, Cambridge.
55. Nicholson, W.L., Schuerger, A.C. & Setlow, (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. (Pubitemid 40320527)
56. Nybakken, L., Solhaug, K.A., Bilger, W. & Gauslaa, Y. (2004). The lichens Xanthoria elegans and Cetraria islandica maintaa high protection against UV-B radiation Arctic habitats. Oecologia 140, 211-216. (Pubitemid 39040076)
57. Olson, J.M. (2006). Photosynthesis the Archean Era. Photosynth. Res. 88(2), 109-117.
58. Onofri, S., de la Torre, R., de Vera, J-.P., Ott, S., Zucconi, L., Selbmann, L., Scalzi, G., Venkateswaran, K.J., Rabbow, E., Sánchez Iñigo, F.J. & Horneck, G. (2012). Survival of rock-colonizing organisms after 1.5 years outer space. Astrobiology 12(5), 508-516.
59. Paerl, H. (1984). Cyanobacterial carotenoids: their roles maintaining optimal photosynthetic production among aquatic bloom forming genera. Oecologia 61(2), 143-149. (Pubitemid 16276477)
60. 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.
61. Rambold, G. & Triebel, D. (1992). The inter-lecanoralean associations. Bibl. Lichen 48, 1-201.
62. Rettberg, & Rothschild, L.J. (2002). Ultraviolet radiation planetary atmospheres and biological implications. Astrobiology, The Quest for the Conditions of Life, ed. Horneck, G. & Baumstark-Khan, C., 233-243. Springer, Berlin, Heidelberg.
63. Rikkinen, J. (1995). What's behind the pretty colours? A study on the photobiology of lichens. Bryobrothera 4, 1-239.
64. Rothschild, L.J. & Cockell, C.S. (1999). Radiation: microbial evolution, ecology, and relevance to Mars missions. Mutat. Res. 430(2), 281-291. (Pubitemid 30021444)
65. Rozema, J. et al. (2002). The role of UV-B radiation aquatic and terrestrial ecosystems-an experimental and functional analysis of the evolution of UV-absorbing compounds. J. Photochem. Photobiol. B: Biol. 66, 2-12. (Pubitemid 34162448)
66. Sadowsky, A. & Ott, S. (2012). Photosynthetic symbionts Antarctic terrestrial ecosystems: the physiological response of lichen photobionts to drought and cold. Symbiosis 58, 81-90.
67. Salguero, A., León, R., Mariotti, A., de la Morena, B., Vega, J.M. & Vílchez, C. (2005). UV-A mediated induction of carotenoid accumulation Dunaliella bardawil with retention of cell viability. Appl. Microbiol. Biotechnol. 66(5), 506-511.
68. Sánchez, F.J., de la Torre, R., Sancho, L.G, Mateo-Martí, E., Martínez-Frías, J. & Horneck, G. (2010). Aspicilia fruticulosa: one of the most resistant organisms to outer space conditions and Mars simulated environment. Special Issue: Abstracts from the 9th European Workshop on Astrobiology, Brussels, October 12-14, 2009. Orig. Life EBiosph. 40(6), 546.
69. 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.
70. Sancho, L.G., Schroeter, B. & del Prado, R. (2000). Ecophysiology and morphology of the globular erratic lichen Aspicilia fruticulosa (EVERSM.) FLAG. From Central Spain. New aspects cryptogamic research. Bibl. Lichenol. 75, 137-147.
71. Sancho, L.G., de la Torre, R., Horneck, G., Ascaso, C., de los Ríos, A., Pintado, A., Wierzchos, J. & Schuster,M. (2007). Lichens survive space: results from 2005 LICHENS experiment. Astrobiology 7(3), 443-454. (Pubitemid 47233011)
72. Sancho, L.G., de la Torre, R. & Pintado, A. (2008). Lichens, new and promising material from experiments Astrobiology. Fungal Biol. Rev. 22, 103-109.
73. Sanderson, M.J. (2003). Molecular data from 27 proteins do not support a Precambrian origof land plants. Am. J. Bot. 90, 954-956. (Pubitemid 36738457)
74. Sass, L. & Vass, I. (1998). Characterization of UV-B tolerance lichens by photosystem II electron transport measurements. Photosynthesis: Mechanisms and Effects, ed. Gareb, G., 2381-2384. Kluwer Academic Publishers, Dordrecht, The Netherlands.
75. Scalzi, G., Selbmann, L., Zucconi, L., Rabbow, E., Horneck, G., Albertano, & 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 EBiosph. 42, 253-262.
76. Schreiber, U., Bilger,W. & Neubauer, C. (1994). Chlorophyll fluorescence as a non-intrusive indicator for rapid assessment of vivo photosynthesis. Ecol. Stud. 100, 49-70.
77. Sohrabi, M. (2012). Taxonomy and phylogeny of the manna lichens and allied species (Megasporaceae). PhD Thesis, Publications Botany from the University of Helsinki. http://urn.fi/URN:ISBN:978-952-10-7400-4
78. Solhaug, K.A. & Gauslaa, Y. (1996). Parietin, a photoprotective secondary product of the lichen Xanthoria parietina. Oecologia 108, 412-418.
79. Solhaug, K.A. & Gauslaa, Y. (2004). Photosynthates stimulate the UV-B induced fungal anthraquinone synthesis the foliose lichen Xanthoria parietina. Plant Cell Environ. 27, 167-176. (Pubitemid 38225416)
80. Solhaug, K.A., Gauslaa, Y., Nybakken, L. & Bilger, W. (2003). UV-induction of sun-screening pigments Lichens. New Phytol. 158(1), 91-100.
81. Sonesson, M., Callaghan, T.V. & Bjorn, L.O. (1995). Short-term effects of enhanced UV-B and CO2 on lichens at different latitudes. Lichenologist 27, 547-557.
82. Strid, A., Chow, W.S. & Anderson, J.M. (1990). Effects of supplementary ultraviolet-B radiation on photosynthesis Pisum sativum. Biochim. Biophys. Acta 1020, 260-268. (Pubitemid 120038265)
83. Strid, A., Chow, W.S. & Anderson, J.M. (1994). UV-B damage and protection at the molecular level plants. Photosynth. Res. 39, 475-489.
84. Teramura, A.H. & Sullivan, J.H. (1994). Effects of UV-B radiation on photosynthesis and growthof terrestrial plants.Photosynth.Res. 39, 463-473.
85. Tevini, M. & Häder, D.-(1985). Allgemeine Photobiologie. Georg Thieme Verlag, Stuttgart, 25.
86. Tschermak-Woess, E. (1978). The Phycobionts the Section Cystophora of Chaenotheca, especially Dictyochloropsis splendid and Trebouxia simplex, spec. nova. Plant Syst. E129, 185-208.
87. Tschermak-Woess, E. (1989). Developmental studies trebouxioid algae and taxonomical consequences. Plant. Syst. E164, 161-195.
88. Ünal, D. & Uyanikgil, Y. (2011). UV-B induces cell death the lichen Physcia semipinnata (J.F. Gmel) Turk. J. Biol. 35, 137-144.
89. Van de Poll, W.H., Hanelt, D., Hoyer, K., Buma, A.G.J. & Breeman, A.M. (2002). Ultraviolet-B-induced cyclobutane-pyrimidine dimer formation and repair Arctic marine macrophytes. Photochem. Photobiol. 76, 493-500.
90. Wynn-Williams, D.D., Holder, J.M. & Edwards, H.G.M. (2000). Lichens at the limits of life: past perspectives and modern technology. Bibl. Lichenol. 75, 275-288.
91. Wynn-Williams, D.D., Edwards, H.G.M., Newton, E.M. & Holder, J.M. (2002a). Pigmentation as a survival strategy for ancient and modern photosynthetic microbes under high ultraviolet stress on planetary surfaces. Int. J. Astrobiol. 1, 39-49.
92. Wynn-Williams, D.D. & Edwards, H.G.M. (2002b). Environmental UV radiation: biological strategies for protection and avoidance. Astrobiology, The Quest for the Conditions of Life, ed. G. Horneck & C. Baumstark-Khan 245-260 Springer, Berlin, Heidelberg Astrobiology, The Quest for the Conditions of Life.
93. Yamazaki, J., Takahisa, S., Emiko, M. & Yasumaro, K. (2005). The stoichiometry and antenna size of the two photosystems marine green algae, Bryopsis maxima and Ulva pertusa, relation to the Alight environment of their natural habitat. J. ExBot. 56(416), 1517-1523. (Pubitemid 40764440)
94. Yoon, H.S., Hackett, J.D., Ciniglia, C., Pinto, G. & Bhattacharya, D. (2004).A molecular timeline for the origof photosynthetic eukaryotes. Mol. Biol. Evol. 21 809-818 A molecular timeline for the origof photosynthetic eukaryotes. Mol. Biol. E21, 809-818.
95. Young, A.J., Phillip, D. & Savill, J. (1997). Carotenoids higher plant photosynthesis. Handbook of Photosynthesis, ed. Pessaraki, M., 575-596. Marcel Dekker, New York.