Resistance of Symbiotic Eukaryotes

Survival to Simulated Space Conditions and Asteroid Impact Cataclysms
Chapter
Part of the Cellular Origin, Life in Extreme Habitats and Astrobiology book series (COLE, volume 17)

Abstract

Carbon isotope data suggest that microbial life was present on Earth as early as 3.5 Ga ago, and probably even 4 Ga ago, and indicates that biological CO2 fixation was an early feature (Schidlowski, 2001). The early biosphere was dominated by microbial life forms for a long period, during which they evolved to exploit new niches. For some, this involved interaction between different microbial groups, and now symbiosis represents one of the most successful strategies in evolution (Margulis, 1993). There is now little doubt that eukaryotes arose through uptake of a heterotrophic eubacterial symbiont by an autotrophic archaebacterial host (Martin and Russell, 2003). This milestone in evolution, and the paradigm of the endosymbiont hypothesis, initiated the evolution of the eukaryotic kingdoms of fungi, plants, and animals. Evidence from dating sequence divergence (Wang et al., 1999) suggests that the ancestors of today’s plants, animals, and fungi diverged possibly as early as 1.5 Ga ago. Independent of this major evolutionary step, other symbioses arose as exosymbiosis, without the ingestion of one partner. These involve both syntrophic partnerships among prokaryotes, and also associations with or among eukaryotes. Such symbioses are particularly complex in biofilms and biocrusts (Belnap et al., 2001; Flemming and Wingender, 2001), and in associations that are often found in stressful terrestrial habitats that are not amenable to higher plant community development, for instance, due to periodic aridity. In such habitats, lichen symbioses can form the dominant and conspicuous biological elements of the landscape. Lichens can be characterized as a specific exosymbiotic life form that results in an exposed and integrated phenotype of clearly different morphology than that of the constituent organisms alone (Lawrey, 1991; Ahmadjian et al., 1987; Galun, 1988 Grube and Hawksworth 2007). Taylor et al. (1997, 2005) and Yuan et al. (2005) date the first occurrence of the lichen symbiosis from fossil records in the Lower Devonian period (0.6 Ga), but the evolution of the lichen symbiosis could well pre-date the available fossil records (Lutzoni 2001).

Keywords

Lichen Species Biological Soil Crust Lichen Thallus Asteroid Impact Lichen Symbiosis 
These keywords were added by machine and not by the authors. This process is experimental and the keywords may be updated as the learning algorithm improves.

References

  1. Ahmadjian, V. and Jacobs, J.B. (1987) Studies on the development of synthetic lichens. Biblioth. Lichenol. 25: 47–58.Google Scholar
  2. Bachereau, F. and Asta, J. (1997) Effects of solar ultraviolet radiation at high altitudes on the physiology and biochemistry of a terricolous lichen (Cetraria islandica (L.) Ach.). Symbiosis 23: 197–217.Google Scholar
  3. Belnap, J., Büdel, B. and Lange, O.L. (2001) Biological soil crusts. Characteristics and distribution, In: J. Belnap and O.L. Lange (eds.) Biological Soil Crusts: Structure, Function, and Management. Springer, Berlin, pp. 3–30.CrossRefGoogle Scholar
  4. Berenbaum, M. (2001) Rad Roaches. Am. Entomol. 47: 132–133.Google Scholar
  5. Bletchly, J.D. and Fisher, R.C. (1957) Use of gamma radiation for the destruction of wood-boring insects. Nature 179: 670.CrossRefGoogle Scholar
  6. Brodo, I.M., Sharnoff, S.D. and Sharnoff, S. (2001) Lichens of North America. Yale University Press, New Haven and London.Google Scholar
  7. Büdel, B. and Wessels, D.C.J. (1986) Parmelia hueana Gyeln, a vagrant lichen from Namib Desert SWA/Namibia. I. Anatomical and reproductive adaptations. Dinteria 18: 3–36.Google Scholar
  8. Cork, J.M. (1957) Gamma radiation and longevity of the flour beetle. Radiat. Res. 7: 551–557.PubMedCrossRefGoogle Scholar
  9. Davey, W.P. (1919) Prolongation of life of Tribolium confusum apparently due to small doses of X-rays. J. Exp. Zool. 28: 447–458.CrossRefGoogle Scholar
  10. de la Torre, R., Horneck, G., Sancho, L.G., Pintado, A., Scherer, K., Facius, R., Deutschmann, U., Reina, M., Baglioni, P. and Demets, R. (2004) Studies of lichens from high mountain regions in outer space: the BIOPAN experiment. Proc. Of the III European Workshop on Exo-Astrobiology. Mars: The search for Life, Madrid, Spain. ESA SP-545, pp. 193–194.Google Scholar
  11. de Vera, J.P. (2005) Grenzen des Überlebens: Flechten als Modellsystem für das Potential von Adaptationsmechanismen eines Symbioseorganismus unter Extrembedingungen. Ph.D. thesis, Heinrich-Heine-University, Düsseldorf.Google Scholar
  12. de Vera, J.P., Horneck, G., Rettberg, P. and Ott, S. (2003) The potential of 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: 285–293.CrossRefGoogle Scholar
  13. de Vera, J.P., Horneck, G., Rettberg, P. and Ott, S. (2004a) The potential of 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.PubMedCrossRefGoogle Scholar
  14. de Vera, J.-P., Horneck, G., Rettberg, P. and Ott, S. (2004b) In the context of panspermia: May lichens serve as shuttles for their bionts in Space? Proc. of the III European Workshop on Exo-Astrobiology. Mars: The search for Life, Madrid, Spain, 18–20 November 2003 (ESA SP-545, March 2004), pp. 197–198.Google Scholar
  15. de Vera, J.P., Rettberg, P. and Ott, S. (2008) Life at the limits: Capacities of isolated and cultured lichen symbionts to resist extreme environmental stresses. Orig. Live Evol. Biosph. 38: 457–468.CrossRefGoogle Scholar
  16. Edwards, H.G.M., Newton, E.M., Wynn-Williams, D.D. and Coombes, S.R. (2003) Molecular spectroscopic studies of lichen substances 1: parietin and emodin. J. Mol. Struct. 648: 49–59.CrossRefGoogle Scholar
  17. Fahselt, D. (1995) Growth form and reproductive character of lichens near active fumaroles in Japan. Symbiosis 18: 211–231.Google Scholar
  18. Feofilova, E.P. (2003) Deceleration of vital activity as a universal biochemical mechanism ensuring adaptation of microorganisms to stress factors: a review. Appl. Biochem. Microbiol. 39: 1–18.CrossRefGoogle Scholar
  19. Flemming, H.C. and Wingender, J. (2001) Biofilme – die bevorzugte Lebensform der Bakterien. Biologie in unserer Zeit. 3: 169–180.CrossRefGoogle Scholar
  20. Galun, M. (1988) Lichenization, In: M. Galun (ed.) CRC Handbook of Lichenology. Vol. 2. CRC Press, Boca Raton, pp. 153–169.Google Scholar
  21. Grube, M. and Hawksworth, D.L. (2007) Trouble with lichen: the re-evaluation and re-interpretation of thallus form and fruit body types in the molecular era. Mycol. Res. 111: 1116–1132.PubMedCrossRefGoogle Scholar
  22. Henssen, A., Jahns, H.M. (1974) Lichenes; Eine Einführung in die Flechtenkunde. Georg Thieme Verlag, Stuttgart.Google Scholar
  23. Honegger, R. and Kutasi, V. (1990) Anthraquinone production in the aposymbiotically cultured telochistacean lichen mycobiont: the role of the carbon source, In: P. Nardon, V. Gianinazzi-Pearson, A.M. Grenier, L. Margulis, and D.C. Smith (eds.), Endocytobiology IV D.C. INRA, Paris pp. 175–178.Google Scholar
  24. Horneck, G. (1993) Responses of Bacillus subtilis spores to space environment: results of experiments in space. Orig. Life Evol. Biosphere 23: 37–52.CrossRefGoogle Scholar
  25. Horneck, G., Stöffler, D., Eschweiler, U. and Hornemann, U. (2001a) Bacterial spores survive simulated meteorite impact. Icarus 149: 285–290.CrossRefGoogle Scholar
  26. Horneck, G., Rettberg, P., Reitz, G., Wehner, J., Eschweiler, U., Strauch, K., Panitz, C., Starke, V. and Baumstark-Khan, C. (2001b) Protection of bacterial spores in space, a contribution to the discussion of Panspermia. Orig. Life Evol. Biosphere 31: 527–547.CrossRefGoogle Scholar
  27. Horneck, G. (2001c) Likelihood of transport of life between the planets of our solar system, In: J. Chela-Flores et-al. (eds.), First steps in the origin of life in the Universe, Kluwer Academic publishers, Netherlands.Google Scholar
  28. Horneck, G., Stöffler, D., Ott, S., Hornemann, U., Cockell, C.S., Moeller, R., Meyer, C., de Vera, J.P., Fritz, J., Schade, S. and Artemieva, N. (2008) Microbial rock inhabitants survive hypervelocity impacts on Mars-like host planets: first phase experimentally tested. Astrobiology 8: 17–44.PubMedCrossRefGoogle Scholar
  29. Jahns, H.M. (1995) Farne, Moose, Flechten Mittel-, Nord- und Westeuropas. BLV Verlagsgesellschaft, München.Google Scholar
  30. Jennings, D.H. and Lysek, G. (1999) Fungal Biology. Understanding the Fungal Lifestyle. 2nd ed. Springer, New York.Google Scholar
  31. Kappen, L. (1973) Responses to extreme environments, In: V. Ahmadjian and M.E. Hale (eds.) The Lichens. Academic Press, New York, pp. 310–380.Google Scholar
  32. Kappen, L. (1993) Lichens in the Antarctic region, In: E.I. Friedmann (ed.) Antarctic Microbiology. Wiley-Liss, New York, pp. 433–490.Google Scholar
  33. Kappen, L., Schroeter, B., Green, T.G.A. and Seppelt, R.D. (1998) Microclimatic conditions, meltwater moistening, and the distributal pattern of Buellia frigida on rock in a southern continental Antarctic habitat. Polar Biol. 19: 101–106.CrossRefGoogle Scholar
  34. Kranz, A.R., Bork, U., Búcker, H. and Reitz, G. (1990) Biological damage induced by ionizing cosmic rays in dry Arabidopsis seeds. Nucl. Tracks Radiat. Meas. 17: 155–165.CrossRefGoogle Scholar
  35. Lange, O.L., Geiger, I.L. and Schulze, E.D. (1977) Ecophysiological investigations on lichens of the Negev desert. Oecologia 28: 247–259.Google Scholar
  36. Lange, O.L., Pfanz, H., Kilian, E. and Meyer, A. (1990) Effect of low water potential on photosynthesis in intact lichens and their liberated algal components. Planta 182: 467–472.CrossRefGoogle Scholar
  37. Lange, O.L., Büdel, B., Meyer, A., Zellner, H. and Zotz, G. (2000) Lichen carbon gain under tropical conditions: water relations and CO2 exchange of three Leptogium species of a lower montane rain forest in Panama. Flora 195: 172–190.Google Scholar
  38. Lawrey, J.D. (1991) Biotic interactions in lichen community development: a review. Lichenologist 23: 205–214.Google Scholar
  39. Lee, Y.J. and Ducoff, H.S. (1984) Radiation-enhanced resistance to oxygen: a possible relationship to radiation-enhanced longevity. Mech. Ageing Dev. 27: 101–109.PubMedCrossRefGoogle Scholar
  40. Lud, D. (2001) Biotic responses to UV-B in Antarctica. Ph.D. thesis, University of Amsterdam.Google Scholar
  41. Lutzoni, F., Pagel M. and Reeb, V. (2001) Major fungal lineages are derived from lichen symbiotic ancestors. Nature 411: 937–940.PubMedCrossRefGoogle Scholar
  42. Lütz, C., Seidlitz, H.K. and Meindl, U. (1997) Physiological and structural changes in the chloroplast of the green alga Micrasterias denticulata induced by UV B simulation. Plant Ecol. 128: 55–64.CrossRefGoogle Scholar
  43. Mancinelli, R.L., White, M.R. and Rothschild, L.J. (1998) Biopan survival I: exposure of the ­osmophiles Synechoccocus sp. (Nageli) and Haloarcula sp. to the space environment. Adv. Space Res. 22: 327–334.CrossRefGoogle Scholar
  44. Margulis, L. (1993) Symbiosis in Cell Evolution. 2nd edn. Freeman, New York.Google Scholar
  45. Martin, W. and Russell, M.J. (2003) On the origin of cells: a hypothesis for the evolutionary transitions from abiotic geochemistry to chemoautotrophic prokaryotes to nucleated cells. Phil. Trans. R. Soc. Lond. B. 158: 59–85.CrossRefGoogle Scholar
  46. Meyer, C. (2005) Stoßwellenexperimente zur Simulation des Transfers von Mikroorganismen vom Mars zur Erde. Diplomarbeit im Fach Mineralogie, Museum für Naturkunde (Humboldt Universität), Freie Universität, Berlin.Google Scholar
  47. Meyer-Rochow, V.B., Kashivagi, T. and Eguchi, E. (2002) Selective photoreceptor damage in four species of insects induced by experimental exposures to UV-irradiation. Micron 33: 23–31.PubMedCrossRefGoogle Scholar
  48. Misra Parvathy Bhatia, H.P. (1998) Gamma radiation susceptibility of strains of Tribolium castaneum (Herbst) resistant and susceptible to fenvalerate. Int. J. Pest Management 44: 145–147.CrossRefGoogle Scholar
  49. Moeller, R., Horneck, G., Stackebrandt, E., Edwards, H.G.M. and Villar, S.E.J. (2003) Do endogenous pigments protect Bacillus spores against UV-radiation? Proc. of the III European Workshop on Exo-Astrobiology: Mars: The search for life, Madrid, Spain, pp. 241–242.Google Scholar
  50. Moeller, R., Horneck, G., Facius, R., Stackebrandt, E. (2005) Role of pigmentation in protecting Bacillus sp. endospores against environmental UV radiation. FEMS Microbiol. Ecol. 51: 231–236.PubMedCrossRefGoogle Scholar
  51. Nash III, T.H. (1996) Lichen Biology. Cambridge University Press.Google Scholar
  52. Neuberger, K., Lux-Endrich, A., Rattler, S., Panitz, C., Horneck, G., and Hock, B. (2004) Fungal and fern spores in space simulation experiments. Proceedings of the Third European Workshop on Exo-Astrobiology, 18–20 November 2003, Madrid, Spain. Ed.: R. A. Harris & L. Ouwehand. ESA SP-545, Noordwijk, Netherlands: ESA Publications Division, ISBN 92-9092-856-5, pp. 251–252.Google Scholar
  53. Nicholson, W.L., Munakata, N., Horneck, G., Melosh, H.J. and Setlow, P. (2000) Resistance of Bacillus endospores to extreme terrestrial and extraterrestrial environments. Microbiol. Mol. Biol. Rev. 64: 548–572.PubMedCrossRefGoogle Scholar
  54. Øvstedal, D.O. and Lewis-Smith, R.I. (2001) Lichens of Antarctica and South Georgia. A guide to their identification and Ecology. Cambridge University Press, Cambridge.Google Scholar
  55. Poelt, J. (1969) Bestimmungsschlüssel Europäischer Flechten. J. Cramer, Lehre.Google Scholar
  56. Quilhot, W., Fernandez, E., Rubio, C., Cavieres, M.F., Hidalgo, M.E., Goddard, M. and Galloway, D. (1996) Preliminary data on the accumulation of usnic acid related to ozone depletion in two Antarctic lichens. Seria Cientas INACH. 46: 105–111.Google Scholar
  57. Rettberg, P. and Rothschild, L.J. (2002) Ultraviolet radiation in planetary atmospheres and biological implications, In: G. Horneck and Ch. Baumstark-Khan (eds.) Astrobiology – The quest for the conditions of life. Springer, Berlin, pp. 233–243.CrossRefGoogle Scholar
  58. Ross, M.H. and Cochran, D.G. (1963) Some early effects of ionizing radiation on the German cochroach, Blattella germanica. Ann. Entomol. Soc. Am. 56: 256–261.Google Scholar
  59. Sancho, L.G., de la Torre, R., Horneck, G., Ascaso, C., de los Rios, A., Pintado, A., Wierzchos, J. and Schuster, M. (2007) Lichens survive in space: results from the 2005 LICHENS experiment. Astrobiology 7: 443–454.PubMedCrossRefGoogle Scholar
  60. Schidlowski, M. (2001) Carbon isotopes as biogeochemical recorders of life over 3.8 Ga of Earth ­history: evolution of a concept. Precambrian Res. 106: 117–134.CrossRefGoogle Scholar
  61. Solhaug, A.A. and Gauslaa, Y. (1996) Parietin, a photoprotective secondary product of the lichen Xanthoria parietina. Ocoelogia 108: 412–418.CrossRefGoogle Scholar
  62. Solhaug, A.A., Gauslaa, Y., Nybakken, L. and Bilger, W. (2003) UV-induction of sun-screening ­pigments in lichens. New Phytol. 158: 91–100.CrossRefGoogle Scholar
  63. Stetter, K.O. (1996) Hyperthermophilic prokaryotes. FEMS Microbiol. Rev. 18: 149–158.CrossRefGoogle Scholar
  64. Stöffler, D., Horneck G., Ott, S., Hornemann, U., Cockell, C.S., Möller, R., Meyer, C., de Vera, J.P., Fritz, J. and Artemieva, N.A. (2007) Experimental evidence for the impact ejection of viable microorganisms from Mars-like planets. Icarus 186: 585–588.CrossRefGoogle Scholar
  65. Swanson, A. and Fahselt, D. (1997) Effects of ultraviolet on polyphenolics of Umbilicaria americana. Can. J. Bot. 75: 284–289.CrossRefGoogle Scholar
  66. Taylor, T.N., Hass, H. and Kerp, H. (1997) A cyanolichen from the Lower Devonian Rhynie chert. Am. J. Bot. 84: 992–1004.PubMedCrossRefGoogle Scholar
  67. Taylor, T.N., Hass, H., Kerp, H., Krings, M. and Hanlin, R.T. (2005 [‘2004’]) Perithecial ascomycetes from the 400 million year old Rhynie chert: an example of ancestral polymorphism. Mycologia 96: 1403–1419.CrossRefGoogle Scholar
  68. Tepfer, D. and Leach, S. (2006) Plant seeds as model vectors for transfer of life through space. ­Astophys. Space Sci. 306: 69–75.CrossRefGoogle Scholar
  69. Thoss, V. (1999) Chemical characterization of dissolved organic matter in natural matrices. Ph.D.-thesis, University of Wales, Bangor.Google Scholar
  70. Upton, A.C. (2001) Radiation hormesis: data and interpretations. Crit. Rev. Toxicol. 31: 681–695.PubMedCrossRefGoogle Scholar
  71. van der Drift, K.M.G.M., Spaink, H.P., Bloemberg, G.V., van Brussel, A.A.N. and Lugtenberg, B.J.J., Haverkamp, J., Thomas-Oates, J.E. (1996) Rhizobium leguminosarum bv. Trifolii produces Lipochitin Oligosaccharides with node-dependent highly unsaturated fatty acyl moieties. J. Biol. Chem. 271: 22563–22569.PubMedCrossRefGoogle Scholar
  72. Vernós, I., Carratalá, M., González-Jurado, J., Valverde, J.R., Calleja, M., Domingo, A., Vinós, J., Cervera, M. and Marco, R. (1989) Insects as test systems for assessing the potential role of microgravity in biological development and evolution. Adv. Space Res. 9: 137–146.PubMedCrossRefGoogle Scholar
  73. Wang, D.Y.C., Kunar, S. and Hedges, S.B. (1999) Divergence time estimates for the early history of animal phyla and the origin of plants, animals and fungi. Proc. R. Soc. Lond. B. 266: 163–171.CrossRefGoogle Scholar
  74. Wharton, D.R.A. and Wharton, M.L. (1957) The production of sex attractant substance and of oothecae by the normal and irradiated American cockroach, Periplaneta americana (L.). J. Insect Physiol. 1: 229–239.CrossRefGoogle Scholar
  75. Wharton, D.R.A. and Wharton, M.L. (1959) The effect of radiation on the longevity of the cockroach, Periplaneta americana, as affected by dose, age, sex and food intake. Radiat. Res. 11: 600–615.PubMedCrossRefGoogle Scholar
  76. Wieners, P. (2005) Das evolutionäre Potential der Flechtensymbiose gegenüber Extrembedingungen. Diplomarbeit, Heinrich-Heine-Universität Düsseldorf.Google Scholar
  77. Wynn-Williams, D.D., Holder, J.M. and Edwards, H.G.M. (2000). Lichens at the limits of life: past perspectives and modern technology. Biblioth. Lichenol. 75: 275–288.Google Scholar
  78. Wynn-Williams, D.D. and Edwards, H.G.M. (2002) Environmental UV radiation: biological strategies for protection and avoidance, In: G. Horneck and C. Baumstark-Kahn (eds.) Astrobiology. The Quest for the conditions of Life. Springer, Berlin, pp. 245–258.CrossRefGoogle Scholar
  79. Yuan, X., Xiao, S., Taylor, T.N. (2005) Lichen-like symbiosis 600 million years ago. Science 308: 1017.PubMedCrossRefGoogle Scholar

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© Springer Science+Business Media B.V. 2010

Authors and Affiliations

  1. 1.Deutsches Zentrum für Luft- und Raumfahrt e.V. (DLR) in der Helmholtz -Gemeinschaft, Institut für PlanetenforschungBerlinGermany
  2. 2.Institute of Botany, Universitätsstr. 1 (Geb.26.13.02)Heinrich-Heine-UniversityDüsseldorfGermany

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