Advertisement

Cyanobacterial Responses to UV Radiation

  • Richard W. Castenholz
  • Ferran Garcia-Pichel
Chapter

Summary

The influence of ultraviolet radiation (UVR) on populations of microorganisms has been the subject of serious investigation for at least the past 20–25 years. UVR that is applicable to the Earth’s surface (past or present) is arbitrarily divided into UVA (400–320 or 315 nm), UVB (280–320 or 315 nm), UVC (∼180–280 nm). Although essentially all organisms are affected by UVR, microorganisms show more rapid, immediate and measurable effects than macro-organisms. This chapter is mainly relegated to UVR and cyanobacteria, although UV effects on other phototrophs and microorganisms, when relevant, will be included. Some ancestors of living cyanobacteria, the oldest oxygenic organisms, may have evolved in the Archean or early Proterozoic Eons, from 3.5 to 2.5 Gyr, respectively, in a time when UV radiation fluxes reaching the surface, particularly UVB and UVC, were much higher than at present. The latter wavelength region (UVC) does not reach the Earth’s surface at present. Thus, cyanobacteria and other microorganisms in that distant age had to have evolved a strategy to tolerate these greater levels of UV radiation, and at present this strategy may demonstrably involve multiple devices, even within one organism. The best understood in the past several years for numerous organisms has been the active metabolic strategies that compensate for the destruction of vital genetic components, such as the development of efficient metabolic DNA repair systems. The implementation of gliding motility system for escaping the effects of high visible and UV radiation has been better described and understood. Some of the most revealing results in the last 10 years have been an almost complete understanding of the regulation of the UV-protective compounds, scytonemin and mycosporine-like compounds, that partially or completely avoid the damage caused by UV radiation.

Keywords

Unicellular Cyanobacterium Shikimic Acid Pathway High Solar Irradiance Clear Oceanic Water Agmenellum Quadruplicatum 
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.

Notes

Acknowledgements

RWC is very grateful to the US National Science Foundation, which for over many years has supported research on UV effects on cyanobacteria.

References

  1. Asada K, Takahashi M (1987) Production and scavenging of active oxygen in photosynthesis. In: Kyle DJ, Osmond CB, Arntzen CJ (eds) Photoinhibition. Elsevier Science Publishers, Amsterdam, pp 227–287Google Scholar
  2. Bailey S, Grossman A (2008) Photoprotection in cyanobacteria: regulation of light harvesting. Photochem Photobiol 84:1410–1420PubMedCrossRefGoogle Scholar
  3. Balskus EP, Walsh CT (2008) Investigating the initial steps in the biosynthesis of cyanobacterial sunscreen scytonemin. J Am Chem Soc 130:15260–15261PubMedCrossRefGoogle Scholar
  4. Balskus EP, Walsh CT (2010) The genetic and molecular basis of sunscreen biosynthesis in cyanobacteria. Science 329:1653–1656PubMedCrossRefGoogle Scholar
  5. Bebout BM, Garcia-Pichel F (1995) UVB-induced vertical migrations of cyanobacteria in a microbial mat. Appl Environ Microbiol 61:4215–4222PubMedGoogle Scholar
  6. Billi D, Friedmann EI, Hofer KG, Caiola MG, Ocampo-Friedmann R (2000) Ionizing-radiation resistance in the desiccation-tolerant cyanobacterium Chroococcidiopsis. Appl Environ Microbiol 66:1489–1492PubMedCrossRefGoogle Scholar
  7. Bonilla SE, Villeneuve V, Vincent WF (2005) Benthic and planktonic algal communities in a High Arctic lake: pigment structure and contrasting responses to nutrient enrichment. J Phycol 41:1120–1130CrossRefGoogle Scholar
  8. Booth CR, Morrow JH (1997) The penetration of UV into natural waters. Photochem Photobiol 65:254–257CrossRefGoogle Scholar
  9. Bothwell ML, Sherbot D, Roberg AC, Daley RJ (1993) Influence of natural ultraviolet radiation on lotic periphytic diatom community growth, biomass accrual, and species composition: short-term versus long-term effects. J Phycol 29:24–35CrossRefGoogle Scholar
  10. Bothwell ML, Sherbot DMJ, Pollock CM (1994) Ecosystem response to solar ultraviolet-B radiation: influence of trophic level interactions. Science 265:97–100PubMedCrossRefGoogle Scholar
  11. Bouchard JN, Roy S, Ferreyra G, Campbell DA, Curtosi A (2005) Ultraviolet-B effects on photosystem II efficiency of natural phytoplankton communities from Antarctica. Polar Biol 28:607–618CrossRefGoogle Scholar
  12. Brenowitz S, Castenholz RW (1997) Long-term effects of UV and visible irradiance on natural populations of a scytonemin-containing cyano­bacterium (Calothrix sp.). FEMS Microbiol Ecol 24:343–352CrossRefGoogle Scholar
  13. Britton G (1995) Structure and properties of carotenoids in relation to function. FASEB J 9:1551–1558PubMedGoogle Scholar
  14. Büdel B, Karsten U, Garcia-Pichel F (1997) Ultraviolet-absorbing scytonemin and mycosporine-like amino acid derivatives in exposed, rock-inhabiting cyanobacterial lichens. Oecologia 112:165–172CrossRefGoogle Scholar
  15. Campbell D, Eriksson M-J, Öquist G, Gustafsson P, Clarke AK (1998) The cyanobacterium Synechococcus resists UV-B by exchanging photosystem II reaction center D1 proteins. Proc Natl Acad Sci USA 95:364–369PubMedCrossRefGoogle Scholar
  16. Castenholz RW (1968) The behavior of Oscillatoria terebriformis in hot springs. J Phycol 4:132–139CrossRefGoogle Scholar
  17. Castenholz RW (2004) Phototrophic bacteria under UV stress. In: Seckbach J (ed) Origins, evolution and biodiversity of microbial life. Kluwer Academic Publishers, Dordrecht, pp 445–461Google Scholar
  18. Castenholz RW (2009) Mats, microbial. In: Encyclopedia of Microbiology, Elsevier, pp 278–292Google Scholar
  19. Castenholz RW, Garcia-Pichel F (2000) Cyanobacterial responses to UV-radiation. In: Whitton BA, Potts M (eds) The ecology of cyanobacteria. Their diversity in time and space. Kluwer Academic Publishers, Dordrecht, pp 591–611, 669 ppGoogle Scholar
  20. Castenholz RW, Schneider A (1993) Cyanobacterial dominance at high and low temperatures: optimal conditions or precarious existence? In: Guerrero R, Pedros-Alio C (eds) Trends in microbial ecology. Spanish Society for Microbiology, Barcelona, pp 19–24Google Scholar
  21. Choi J-S, Chung Y-H, Moon Y-J, Kim C, Watanabe M, Song P-S, Joe C-O, Bogorad L, Park YM (1999) Photomovement of the gliding cyanobacterium Synechocystis sp. PCC 6803. Photochem Photobiol 70:95–102PubMedCrossRefGoogle Scholar
  22. Cockell CS (1998) The biological effects of high ultraviolet radiation on early Earth: a theoretical evaluation. J Theor Biol 193:717–729PubMedCrossRefGoogle Scholar
  23. Cockell CS (2001) A photobiological history of Earth. In: Cockell CS, Blaustein AR (eds) Ecosystems, evolution, and ultraviolet radiation. Springer, New York, pp 1–35, 221 ppGoogle Scholar
  24. Cockell CS, Rothschild LJ (1999) The effects of UV radiation A and B on diurnal variation in photosynthesis in three taxonomically and ecologically diverse microbial mats. Photochem Photobiol 69:203–210PubMedCrossRefGoogle Scholar
  25. Cullen JJ, Neale PJ (1994) Ultraviolet radiation, ozone depletion and marine photosynthesis. Photosynth Res 39:303–320CrossRefGoogle Scholar
  26. Day TA, Neale PJ (2002) Effects of UV-B radiation on terrestrial and aquatic primary producers. Annu Rev Ecol Syst 33:371–396CrossRefGoogle Scholar
  27. Des Marais DJ (1995) The biogeochemistry of hypersaline microbial mats. Adv Microbiol Ecol 14:251–274CrossRefGoogle Scholar
  28. Diffey BL, Green AT, Loftus MJ, Johnson GJ, Lee PS (1995) A portable instrument for measuring ground reflectance in the ultraviolet. Photochem Photobiol 61:68–70CrossRefGoogle Scholar
  29. Dillon JG, Castenholz RW (1999) Scytonemin, a cyanobacterial sheath pigment, protects against UVC radiation: implications for early photosynthetic life. J Phycol 35:673–681CrossRefGoogle Scholar
  30. Dillon JG, Castenholz RW (2003) The synthesis of the UV-screening pigment, scytonemin, and photosynthetic performance in isolates from closely related natural populations of cyanobacteria (Calothrix sp.). Environ Microbiol 5:484–491PubMedCrossRefGoogle Scholar
  31. Dillon JG, Tatsumi CM, Tandingan PG, Castenholz RW (2002) Effect of environmental factors on the synthesis of scytonemin, a UV-screening pigment, in a cyanobacterium (Chroococcidiopsis sp.). Arch Microbiol 177:322–331PubMedCrossRefGoogle Scholar
  32. Dillon JG, Miller SR, Castenholz RW (2003) UV-acclimation responses in natural populations of cyanobacteria (Calothrix sp.). Environ Microbiol 5:473–483PubMedCrossRefGoogle Scholar
  33. Dodds WK, Castenholz RW (1988) The biological effects of nitrate fertilization and water replacement in an oligotrophic cold water pond. Hydrobiologia 162:141–146CrossRefGoogle Scholar
  34. Eguchi M, Oketa T, Miyamoto N, Maeda H, Kawai A (1996) Occurrence of viable photoautotrophic picoplankton in the aphotic zone of Lake Biwa, Japan. J Plankton Res 18:539–550CrossRefGoogle Scholar
  35. Ehling-Schulz M, Scherer S (1999) UV protection in cyanobacteria. Eur J Phycol 34:329–338CrossRefGoogle Scholar
  36. Ehling-Schulz M, Bilger W, Scherer S (1997) UV-B-induced synthesis of photoprotective pigments and extracellular polysaccharides in the terrestrial cyanobacterium Nostoc commune. J Bacteriol 179:1940–1945PubMedGoogle Scholar
  37. Fleming ED, Castenholz RW (2007) Effects of periodic desiccation on the synthesis of the UV-screening compound, scytonemin, in cyanobacteria. Environ Microbiol 9:1448–1455PubMedCrossRefGoogle Scholar
  38. Fleming ED, Castenholz RW (2008) Effects of nitrogen source on the synthesis of the UV-screening compound, scytonemin, in the cyanobacterium Nostoc punctiforme PCC 73102. FEMS Microbiol Ecol 63:301–308PubMedCrossRefGoogle Scholar
  39. Fleming ED, Bebout BM, Castenholz RW (2007) Effects of salinity and light intensity on the resumption of photosynthesis in a rehydrated cyanobacterial mat from Baja California Sur, Mexico. J Phycol 43:15–24CrossRefGoogle Scholar
  40. Frederick JE, Snell HE, Haywood EK (1989) Solar ultraviolet radiation at the earth’s surface. Photochem Photobiol 50:443–450CrossRefGoogle Scholar
  41. Gao K, Ye C (2007) Photosynthetic insensitivity of the terrestrial cyanobacterium Nostoc flagelliforme to solar UV radiation while rehydrated or desiccated. J Phycol 43:628–635CrossRefGoogle Scholar
  42. Gao K, Li P, Watanabe T, Heibling EW (2008) Combined effects of ultraviolet radiation and temperature on morphology, photosynthesis, and DNA of Arthrospira (Spirulina) platensis (Cyanophyta). J Phycol 44:777–786CrossRefGoogle Scholar
  43. Gao Q, Garcia-Pichel F (2011) Microbial ultraviolet sunscreens. Nat Rev Microbiol 9:791–802CrossRefGoogle Scholar
  44. Garcia-Pichel F (1994) A model for internal self-shading in planktonic microorganisms and its implications for the usefulness of sunscreens. Limnol Oceanogr 39:1704–1717CrossRefGoogle Scholar
  45. Garcia-Pichel F (1998) Solar ultraviolet and the evolutionary history of cyanobacteria. Orig Life Evol Biosph 28:321–347PubMedCrossRefGoogle Scholar
  46. Garcia-Pichel F, Bebout BM (1996) The penetration of ultraviolet radiation into shallow water sediments: high exposure for photosynthetic communities. Mar Ecol Prog Ser 131:257–262CrossRefGoogle Scholar
  47. Garcia-Pichel F, Belnap J (1996) Microenvironments and microscale productivity of cyanobacterial desert crusts. J Phycol 32:774–782CrossRefGoogle Scholar
  48. Garcia-Pichel F, Castenholz RW (1991) Charaterization and biological implications of scytonemin, a cyanobacterial sheath pigment. J Phycol 27:395–409CrossRefGoogle Scholar
  49. Garcia-Pichel F, Castenholz RW (1993) Occurrence of UV-absorbing, mycosporine-like compounds among cyanobacterial isolates and an estimate of their screening capacity. Appl Environ Microbiol 59:163–169PubMedGoogle Scholar
  50. Garcia-Pichel F, Sherry ND, Castenholz RW (1992) Evidence for an ultraviolet sunscreen role of the extracellular pigment scytonemin in the terrestrial cyanobacterium Chlrogloeopsis sp. Photochem Photobiol 56:17–23PubMedCrossRefGoogle Scholar
  51. Garcia-Pichel F, Wingard CE, Castenholz RW (1993) Evidence regarding the UV-sunscreen role of a mycosporine-like compound in the cyanobacterium Gloeocapsa sp. Appl Environ Microbiol 59:170–176PubMedGoogle Scholar
  52. Garcia-Pichel F, Mechling M, Castenholz RW (1994) Diel migrations of microorganisms within a benthic, hypersaline mat community. Appl Environ Microbiol 60:1500–1511PubMedGoogle Scholar
  53. Gieskes WWC, Buma AGJ (1997) UV damage to plant life in a photobiologically dynamic environment: the case of marine phytoplankton. Plant Ecol 128:16–25CrossRefGoogle Scholar
  54. Gill RT, Katsoulakis E, Schmitt W, Taroncher-Oldenburg G, Misra J, Stephanopoulos G (2002) Genome-wide dynamic transcriptional profiling of the light-to-dark transition in Synechocystis sp. strain PCC 6803. J Bacteriol 184:3671–3681PubMedCrossRefGoogle Scholar
  55. Girotti AW (2001) Photooxidized oxidation of membrane lipids: reaction pathways, cytotoxic effects, and cytoprotective mechanisms. J Photochem Photobiol B 63:103–113PubMedCrossRefGoogle Scholar
  56. Häder D-P (1984) Effects of UV-B on motility and photoorientation in the cyanobacterium, Phormidium uncinatum. Arch Microbiol 140:34–39CrossRefGoogle Scholar
  57. Häder D-P (2001) Ultraviolet radiation and aquatic microbial ecosystems. In: Cockell CS, Blaustein AR (eds) Ecosystems, evolution, and ultraviolet radiation. Springer, New York, pp 150–169Google Scholar
  58. Häder D-P, Lebert M, Schuster M, Del Ciampo L, Helbling EW, McKenzie R (2007) ELDONET-a decade of monitoring solar radiation on five continents. Photochem Photobiol 83:1348–1357PubMedCrossRefGoogle Scholar
  59. He Y-Y, Klisch M, Häder D-P (2002) Adaptation of cyanobacteria to UV-B stress correlated with oxidative stress and oxidative damage. Photochem Photobiol 76:188–196PubMedCrossRefGoogle Scholar
  60. Helbling EW, Villafañe V, Holm-Hansen O (1994) Effects of ultraviolet radiation on Antarctic marine plankton photosynthesis with particular attention to the influence of mixing. In: Weiler CS, Penhale PA (eds) Ultraviolet radiation in Antarctica: measurements and biological effects, vol 62. American Geophysical Union, Washington, DC, pp 207–227CrossRefGoogle Scholar
  61. Hockberger PE (2002) A history of ultraviolet photobiology for humans, animals and microorganisms. Photochem Photobiol 76:561–579PubMedCrossRefGoogle Scholar
  62. Holm-Hansen O, Lubin D, Helbling EW (1993) Ultraviolet radiation and its effects on organisms in aquatic environments. In: Young AR, Björn LO, Moan J, Nultsch W (eds) Environmental UV photobiology. Plenum Press, New York, pp 379–425Google Scholar
  63. Hren MT, Tice MM, Chamberlain CP (2009) Oxygen and hydrogen isotope evidence for a temperate climate 3.42 billion years ago. Nature 462:205–208PubMedCrossRefGoogle Scholar
  64. Jägger J (1985) Solar-UV action on living cells. Praeger, New YorkGoogle Scholar
  65. Javor BJ, Castenholz RW (1981) Laminated microbial mats, Laguna Guerrero Negro, Mexico. Geomicrobiology 2:237–273CrossRefGoogle Scholar
  66. Javor BJ, Castenholz RW (1984) Productivity studies of microbial mats, Laguna Guerrero Negro, Mexico. In: Cohen Y, Castenholz RW, Halvorson HO (eds) Microbial mats: stromatolites. Alan R. Liss, Inc., New York, pp 149–170Google Scholar
  67. Jeffrey WH, Pledger RJ, Aas P, Hager S, Coffin RB, Von Haven R, Mitchell DL (1996) Diel and depth profiles of DNA photodamage in bacterioplankton exposed to ambient solar ultraviolet radiation. Mar Ecol Prog Ser 137:283–291CrossRefGoogle Scholar
  68. Johnson AC, Castenholz RW (2000) Preliminary observations of the benthic cyanobacteria of Waldo Lake and their potential contribution to lake productivity. Lake Reserv Manag 16:85–90CrossRefGoogle Scholar
  69. Josue JS, Frank HA (2002) Direct determination of the S1 excited-state energies of xanthophylls by low-temperature fluorescence spectroscopy. J Phys Chem A 106:2815–2824CrossRefGoogle Scholar
  70. Kanofsky JR, Sima PD (2009) Quenching of singlet oxygen by a carotenoid-cyclodextrin complex: the importance of aggregate formation. Photochem Photobiol 85:391–399PubMedCrossRefGoogle Scholar
  71. Karlsson J, Byström P, Ask J, Ask P, Persson L, Jansson M (2009) Light limitation of nutrientpoor lake ecosystems. Nature 460:506–509CrossRefGoogle Scholar
  72. Karsten U, Maier J, Garcia-Pichel F (1998) Seasonality in UV-absorbing compounds of cyanobacterial mat communities from an intertidal mangrove. Aquat Microb Ecol 16:37–44CrossRefGoogle Scholar
  73. Kasting JF (1987) Theoretical constraints on oxygen and carbon dioxide concentrations in the Precambrian atmosphere. Precambrian Res 34:205–229PubMedCrossRefGoogle Scholar
  74. Kasting JF, Zahnle KJ, Pinto JP, Young AT (1989) Sulfur, ultraviolet radiation, and the early evolution of life. Orig Life Evol Biosph 19:95–108PubMedCrossRefGoogle Scholar
  75. Kelman D, Ben-Amotz A, Berman-Frank I (2009) Carotenoids provide the major antioxidant defence in the globally significant N2-fixing marine cyanobacterium Trichodesmium. Environ Microbiol 11:1897–1908PubMedCrossRefGoogle Scholar
  76. Knoll AH (2008) Cyanobacteria and earth history. In: Herrero A, Flores E (eds) The cyanobacteria – molecular biology, genomics and evolution. Caister Academic Press, Norfolk, pp 1–19, 484 ppGoogle Scholar
  77. Koller LR (1965) Ultraviolet radiation. Wiley, New York, 312 ppGoogle Scholar
  78. Kruschel C, Castenholz RW (1998) The effect of solar UV and visible irradiance on the vertical movements of cyanobacteria in microbial mats of hypersaline waters. FEMS Microbiol Ecol 27:53–72CrossRefGoogle Scholar
  79. Kvalevåg MM, Myhre G, Lund Myhre CE (2009) Extensive reduction of surface UV radiation since 1750 in world’s populated regions. Atmos Chem Phys 9:7737–7751CrossRefGoogle Scholar
  80. Lao K, Glazer AN (1996) Ultraviolet-B photodestruction of a light-harvesting complex. Proc Natl Acad Sci USA 93:5258–5263PubMedCrossRefGoogle Scholar
  81. Laurion I, Roy S (2009) Growth and photoprotection in three ­dinoflagellates (including two strains of Alexandrium tamarense) and one diatom exposed to four weeks of natural and enhanced ultraviolet-B radiation. J Phycol 45:16–33CrossRefGoogle Scholar
  82. Lehr CR, Frank SD, D’Imperio S, Kalinin A, Toplin JA, Norris TB, Castenholz RW, McDermott TR (2007) Cyanidial (Cyanidiales) population diversity and dynamics in an acid-sulfate chloride spring in Yellowstone National Park. J Phycol 43:3–14CrossRefGoogle Scholar
  83. Los DA, Suzuki I, Zinchenko VV, Murata N (2008) Stress responses in Synechocystis: regulated genes and regulated systems. In: Herrero A, Flores E (eds) The cyanobacteria – molecular biology, genomics and evolution. Caister Academic Press, Norfolk, pp 117–157, 484 ppGoogle Scholar
  84. MacDonald TM, Dubois L, Smith LC, Campbell DA (2003) Sensitivity of cyanobacterial antenna, reaction center and CO2 assimilation transcripts and proteins to moderate UVB: light acclimation potentiates resistance to UVB. Photochem Photobiol 77:405–412PubMedCrossRefGoogle Scholar
  85. Máté Z, Sass L, Szekeres M, Vass I, Nagy F (1998) UV-B-induced differential transcription of psbA genes encoding the D1 protein of photosystem II in the cyanobacterium Synechocystis 6803. J Biol Chem 273:17439–17444PubMedCrossRefGoogle Scholar
  86. Matthes U, Turner SJ, Larson DW (2001) Light attenuation by limestone rock and its constraint on the depth distribution of endolithic algae and cyanobacteria. Int J Plant Sci 162:262–270CrossRefGoogle Scholar
  87. Mazor G, Kidron GJ, Vonshak A, Abeliovich A (1996) The role of cyanobacterial exopolysaccharides in structuring desert microbial crusts. FEMS Microbiol Ecol 21:21–130CrossRefGoogle Scholar
  88. Meador JA, Baldwin AJ, Catala P, Jeffrey WH, Joux F, Moss JA, Pakulski D, Stevens R, Mitchell DL (2009) Sunlight-induced DNA damage in marine micro-organisms collected along a latitudinal gradient from 70°N to 68°S. Photochem Photobiol 85:412–420PubMedCrossRefGoogle Scholar
  89. Miller SR, Wingard CE, Castenholz RW (1998) Effects of visible light and UV radiation on photosynthesis in a population of a hot spring cyanobacterium, a Synechococcus sp., subjected to high-temperature stress. Appl Environ Microbiol 64:3893–3899PubMedGoogle Scholar
  90. Morel A, Gentili B, Claustrre H, Babin M, Bricaud A, Ras J, Tièche F (2007) Optical properties of the “clearest” natural waters. Limnol Oceanogr 52:217–229CrossRefGoogle Scholar
  91. Nadeau T-L, Castenholz RW (2000) Characterization of psychrophilic oscillatorians (Cyanobacteria) from Antarctic meltwater ponds. J Phycol 36:914–923CrossRefGoogle Scholar
  92. Nadeau T-L, Howard-Williams H, Castenholz RW (1999) Effects of solar UV and visible irradiance on photosynthesis and vertical migration of Oscillatoria sp (cyanobacteria) in an Antarctic microbial mat. Aquat MicrobEcol 20:231–243CrossRefGoogle Scholar
  93. Nicholson P, Osborn RW, Howe CJ (1987) Induction of protein synthesis in response to ultraviolet light, nalidixic acid and heat shock in the cyanobacterium Phormidium laminosum. FEBS Lett 221:110–114CrossRefGoogle Scholar
  94. Nielsen T, Ekelund NGA (1995) Influence of solar ultraviolet radiation on photosynthesis and motility of marine phytoplankton. FEMS Microbiol Ecol 18:281–288CrossRefGoogle Scholar
  95. Nienow JA, Friedmann EI (1993) Terrestrial lithophytic (rock) communities. In: Friedmann EI (ed) Antarctic microbiology. Wiley-Liss, New York, pp 343–412Google Scholar
  96. Niyogi KK (1999) Photoprotection revisited: genetic and molecular approaches. Annu Rev Plant Physiol Plant Mol Biol 50:333–359PubMedCrossRefGoogle Scholar
  97. Norris TB, Castenholz RW (2006) Endolithic photosynthetic communities within ancient and recent travertine deposits in Yellowstone National Park. FEMS Microbiol Ecol 57:470–483PubMedCrossRefGoogle Scholar
  98. Norris TB, McDermott TR, Castenholz RW (2002) The long-term effects of UV exclusion on the microbial composition and photosynthetic competence of bacteria in hot-spring microbial mats. FEMS Microbiol Ecol 39:193–209PubMedCrossRefGoogle Scholar
  99. Olsson-Francis K, de la Torre R, Cockell CS et al (2010) Isolation of novel extreme-tolerant cyanobacteria from a rock-dwelling microbial community by using exposure to low Earth orbit. Appl Environ Microbiol 76:2115–2121PubMedCrossRefGoogle Scholar
  100. Orce VL, Helbling EW (1997) Latitudinal UVR-PAR measurements in Argentina: extent of the “ozone hole”. Glob Planet Change 15:113–121CrossRefGoogle Scholar
  101. Oren A (1997) Mycosporine-like amino acids as osmotic solutes in a community of halophilic cyanobacteria. Geomicrobiol J 14:231–240CrossRefGoogle Scholar
  102. Pakker H, Martins RST, Boelen P, Buma AGJ, Nikaido O, Breeman AM (2000) Effects of temperature on the photoreactivation of ultraviolet-B-induced DNA damage in Palmaria palmata (Rhodophyta). J Phycol 36:334–341CrossRefGoogle Scholar
  103. Pavlov AA, Kasting JF (2002) Mass-independent fractionation of sulfur isotopes in Archean sediments: strong evidence for an anoxic Archean atmosphere. Astrobiology 2:27–41PubMedCrossRefGoogle Scholar
  104. Pescheck F, Bischof K, Bilger W (2010) Screening of ultraviolet-A and ultraviolet-B radiation in marine green macroalgae (Chlorophyta). J Phycol 46:444–455CrossRefGoogle Scholar
  105. Phoenix VR, Bennett PC, Engel AS, Tyler SW, Ferris FG (2006) Chilean high-altitude hot spring sinters: a model system for UV screening mechanisms by early Precambrian cyanobacteria. Geobiology 4:15–28CrossRefGoogle Scholar
  106. Pierson BK (1994) The emergence, diversification, and role of photosynthetic eubacteria. In: Bengtson S, Bergström J, Vidal G, Knoll A (eds) Early life on earth. Columbia University Press, New York, pp 161–180, 605 ppGoogle Scholar
  107. Pierson BK, Mitchell HK, Ruff-Roberts AL (1993) Chloroflexus aurantiacus and ultraviolet radiation: implications for Archean shallow-water stromatolites. Orig Life Evol Biosph 23:243–260CrossRefGoogle Scholar
  108. Porankiewicz J, Schelin J, Clarke AK (1998) The ATP-dependent Clp protease is essential for acclimation to UV-B and low temperature in the cyanobacterium Synechococcus. Mol Microbiol 29:275–283PubMedCrossRefGoogle Scholar
  109. Portwich A, Garcia-Pichel F (1999) Ultraviolet and osmotic stresses induce and regulate the synthesis of mycosporines in the cyanobacterium Chlorogloeopsis PCC 6912. Arch Microbiol 172:187–192PubMedCrossRefGoogle Scholar
  110. Portwich A, Garcia-Pichel F (2000) A novel prokaryotic UVB photoreceptor in the cyanobacterium Chlorogloeopsis PCC 6912. Photochem Photobiol 71:493–498PubMedCrossRefGoogle Scholar
  111. Portwich A, Garcia-Pichel F (2003) Biosynthetic pathway of mycosporines (mycosporine-like amino acids) in the cyanobacterium Chlorogloeopsis sp. strain PCC 6912. Phycologia 42:384–392CrossRefGoogle Scholar
  112. Postius C, Ernst A, Kenter U, Böger P (1996) Persistence and genetic diversity among strains of the phycoerythrin-rich cyanobacteria from the picoplankton of Lake Constance. J Plankton Res 18:1159–1166CrossRefGoogle Scholar
  113. Potts M (1994) Desiccation tolerance of prokaryotes. Microbiol Rev 58:755–805PubMedGoogle Scholar
  114. Prezelin BB, Boucher NP, Smith RC (1994) Marine primary production under the influence of the Antarctic ozone hole: Icecolors’90. In: Weiler CS, Penhale PA (eds) Ultraviolet radiation in Antarctica: measurement and biological effects, vol 62. American Geophysical Union, Washington, DC, pp 159–186CrossRefGoogle Scholar
  115. Proteau PJ, Gerwick WH, Garcia-Pichel F, Castenholz RW (1993) The structure of scytonemin, an ultraviolet sunscreen pigment from the sheaths of cyanobacteria. Experientia 49:825–829PubMedCrossRefGoogle Scholar
  116. Quesada A, Vincent WF (1997) Strategies of adaptation by Antarctic cyanobacteria to ultraviolet radiation. Eur J Phycol 32:335–342Google Scholar
  117. Ramsing NB, Prufert-Bebout L et al (1994) Motility of Microcoleus chthonoplastes subjected to different light intensities quantified by digital image analysis. In: Stal LJ, Caumette P (eds) Microbial mats. Structure, development and environmental significance, vol 35, NATO ASI series. Springer, Berlin, pp 183–191Google Scholar
  118. Ramsing NB, Ferris MJ, Ward DM (1997) Light-induced motility of thermophilic Synechococcus isolates from Octopus Spring, Yellowstone National Park. Appl Environ Microbiol 63:2347–2354PubMedGoogle Scholar
  119. Rasmussen B, Blake TM, Fletcher IR, Kilburn MR (2009) Evidence for microbial life in synsedimentary cavities from 2.75 Ga terrestrial environments. Geology 37:423–426CrossRefGoogle Scholar
  120. Ravanat J-L, Douki T, Cadet J (2001) Direct and indirect effects of UV radiation on DNA and its components. J Photochem Photobiol B 63:88–102PubMedCrossRefGoogle Scholar
  121. Richardson LL, Castenholz RW (1987) Diel vertical movements of the cyanobacterium Oscillatoria terebriformis in a sulfide-rich hot spring microbial mat. Appl Environ Microbiol 53:2142–2150PubMedGoogle Scholar
  122. Robinson N (1966) Solar radiation. Elsevier, AmsterdamGoogle Scholar
  123. Roy S (2000) Strategies for the minimization of UV-induced damage. In: de Mora S, Demers S, Vernet M (eds) The effects of UV radiation in the marine environment. Cambridge University Press, Cambridge, pp 176–205Google Scholar
  124. Roy CR, Gies HP, Tomlinson DW, Lugg DL (1994) Effects of ozone depletion on the ultraviolet radiation environment at the Australian stations in Antarctica. In: Weiler CS, Penhale PA (eds) Ultraviolet radiation in Antarctica: measurement and biological effects, vol 62. American Geophysical Union, Washington, DC, pp 1–15CrossRefGoogle Scholar
  125. Sancar A (1994) Mechanisms of DNA excision repair. Science 266:1954–1956PubMedCrossRefGoogle Scholar
  126. Sancar A (1996) No “end of history” for photolyases. Science 272:48–49PubMedCrossRefGoogle Scholar
  127. Sass L, Spetea C, Máté Z, Nagy F, Vass I (1997) Repair of UVB induced damage of photosystem II via de novo synthesis of the D1 and D2 reaction centre subunits in Synechocystis sp. PCC 6803. Photosynth Res 54:55–62CrossRefGoogle Scholar
  128. Scully NM, McQueen DJ, Lean DRS (1996) Hydrogen peroxide formation: the interaction of ultraviolet radiation and dissolved organic carbon in lake waters along a 43–75°N gradient. Limnol Oceanogr 41:540–548CrossRefGoogle Scholar
  129. Sheridan RP (2001) The role of ultraviolet radiation in maintaining the three-dimensional structure of a cyanobacterial mat community and facilitating nitrogen fixation. J Phycol 37:731–737CrossRefGoogle Scholar
  130. Shibata H, Katsuya B, Ochiai H (1991) Near-UV irradiation induces shock proteins in Anacystis nidulans R-2; possible role of active oxygen. Plant Cell Physiol 32:771–776Google Scholar
  131. Shick JM, Dunlap WC (2002) Mycosporine-like amino acids and related gadusols: biosynthesis, accumulation, and UV-­protective functions in aquatic organisms. Annu Rev Physiol 64:223–262PubMedCrossRefGoogle Scholar
  132. Singh SP, Kumari S, Rostagi RP, Singh KL, Richa SRP (2010) Photoprotective and biotechnical potentials of cyanobacterial sheath pigment, scytonemin. Afr J Biotechnol 9:580–588Google Scholar
  133. Sinha RP, Klisch M, Helbling EW, Häder D-P (2001) Induction of mycosporine-like amino acids (MAAs) in cyanobacteria by solar ultraviolet-B radiation. J Photochem Photobiol B 60:129–135PubMedCrossRefGoogle Scholar
  134. Smith RC, Baker KS (1981) Optical properties of the clearest natural seawaters. Appl Opt 20:177–188PubMedCrossRefGoogle Scholar
  135. Sobrino C, Ward ML, Neale PJ (2008) Acclimation to elevated carbon dioxide and ultraviolet radiation in the diatom Thallasiosira pseudonana: effects on growth, photosynthesis, and spectral sensitivity of photoinhibition. Limnol Oceanogr 53:494–505CrossRefGoogle Scholar
  136. Sorrels CM, Proteau PJ, Gerwick WH (2009) Organization, evolution, and expression analysis of the biosynthetic gene cluster for scytonemin, a cyanobacterial UV-absorbing pigment. Appl Environ Microbiol 75:4861–4869PubMedCrossRefGoogle Scholar
  137. Soule T, Stout V, Swingley WD, Meeks JC, Garcia-Pichel F (2007) Molecular genetics and genomic analysis of scytonemin biosynthesis in Nostoc punctiforme ATCC 29133. J Bacteriol 189:4465–4472PubMedCrossRefGoogle Scholar
  138. Soule T, Palmer K, Gao Q, Potrafka RM, Stout V, Garcia-Pichel F (2009a) A comparative genomics approach to understanding the biosynthesis of the sunscreen scytonemin in cyanobacteria. BMC Genomics 10:336–345PubMedCrossRefGoogle Scholar
  139. Soule T, Garcia-Pichel F, Stout V (2009b) Gene expression patterns associated with the biosynthesis of the sunscreen scytonemin in Nostoc punctiforme ATCC 29133 in response to UVA radiation. J Bacteriol 191:4639–4646PubMedCrossRefGoogle Scholar
  140. Tang EPY, Tremblay R, Vincent WF (1997) Cyanobacterial dominance of polar freshwater ecosystems: are high latitude mat formers adapted to low temperature? J Phycol 33:171–181CrossRefGoogle Scholar
  141. Tichy M, Vermaas W (1999) In vivo role of catalase-peroxidase in Synechocystis sp. strain PCC 6803. J Bacteriol 181:1875–1882PubMedGoogle Scholar
  142. Van Baalen C (1968) The effects of ultraviolet irradiation on a coccoid blue-green alga: survival, photosynthesis, and photoreactivation. Plant Physiol 43:1689–1695PubMedCrossRefGoogle Scholar
  143. Van Baalen C, O’Donnell K (1972) Action spectra for ultraviolet killing and photoreactivation in the blue-green alga Agmenellum quadruplicatum. Photochem Photobiol 15:269–274PubMedCrossRefGoogle Scholar
  144. Vincent WF (1988) Microbial ecosystems of Antarctica. Cambridge University Press, Cambridge, 304 ppGoogle Scholar
  145. Vincent WF (2000) Cyanobacterial dominance in the polar regions. In: Whitton BA, Potts M (eds) The ecology of cyanobacteria. Their diversity in time and space. Kluwer Academic Publishers, Dordrecht, pp 321–340, 669 ppGoogle Scholar
  146. Vincent WF, Neale PJ (2000) Mechanisms of UV damage to aquatic organisms. In: de Mora S, Demers S, Vernet M (eds) The effects of UV radiation in the marine environment. Cambridge University Press, Cambridge, pp 149–176CrossRefGoogle Scholar
  147. Vincent WF, Roy S (1993) Solar ultraviolet–B radiation and aquatic primary production: damage, protection, and recovery. Environ Rev 1:1–12CrossRefGoogle Scholar
  148. Vincent WF, Downes MT, Castenholz RW, Howard-Williams C (1993) Community structure and pigment organisation of cyanobacteria-dominated microbial mats in Antarctica. Eur J Phycol 28:213–221CrossRefGoogle Scholar
  149. Vincent WF, Mueller DR, Van Hove P, Howard-Williams C (2004) Glacial periods on early Earth and implications for the evolution of life. In: Seckbach J (ed) Origins: genesis, evolution and diversity of life. Kluwer Academic Publishers, Dordrecht, pp 481–501Google Scholar
  150. Vinebrooke RD, Leavitt PR (1996) Effects of ultraviolet radiation on periphyton in an alpine lake. Limnol Oceanogr 41:1035–1040CrossRefGoogle Scholar
  151. Walker JJ, Pace NR (2007) Phylogenetic composition of Rocky Mountain endolithic microbial ecosystems. Appl Environ Microbiol 73:3497–3504PubMedCrossRefGoogle Scholar
  152. Walsby AE (1994) Gas vesicles. Microbiol Rev 58:94–144PubMedGoogle Scholar
  153. Ward DM, Castenholz RW (2000) Cyanobacteria in geothermal habitats. In: Whitton BA, Potts M (eds) Ecology of cyanobacteria: their diversity in time and space. Kluwer Academic Publishers, Dordrecht, pp 7–59, 669 ppGoogle Scholar
  154. Weisse T (1993) Dynamics of autotrophic picoplankton in marine and freshwater ecosystems. Adv Microb Ecol 13:327–370CrossRefGoogle Scholar
  155. Whitehead RF, de Mora SJ, Demers S (2000) Enhanced UV radiation – a new problem for the marine environment. In: de Mora S, Demers S, Vernet M (eds) The effects of UV radiation in the marine environment. Cambridge University Press, Cambridge, pp 1–34CrossRefGoogle Scholar
  156. Willis KJ, Bennett KD, Birks HJB (2009) Variability in thermal and UV-B energy fluxes through time and their influence on plant diversity and speciation. J Biogeogr 36:1630–1644CrossRefGoogle Scholar
  157. Wingard CE, Schiller JR, Castenholz RW (1997) Evidence regarding the possible role of c-phycoerythrin in ultraviolet-B tolerance in a thermophilic cyanobacterium. Photochem Photobiol 65:833–842CrossRefGoogle Scholar
  158. Wu H, Gao K, Villafañe VE, Watanabe T, Helbling EW (2005) Effects of solar UV radiation on morphology and photosynthesis of filamentous cyanobacterium Arthrospira platensis. Appl Environ Microbiol 71:5004–5013PubMedCrossRefGoogle Scholar
  159. Xing P, Hahn MW, Wu QL (2009) Low taxon richness of bacterioplankton in high-altitude lakes of the eastern Tibetan Plateau with a predominance of Bacteroidetes and Synechococcus spp. Appl Environ Microbiol 75:7017–7025PubMedCrossRefGoogle Scholar
  160. Zalar A, Tepfer D, Hoffmann SV, Kenney JM, Leach S (2007a) Directed exospermia: I. biological modes of resistance to UV light are implied through absorption spectroscopy of DNA and potential UV screens. Int J Astrobiol 6:229–240CrossRefGoogle Scholar
  161. Zalar A, Tepfer D, Hoffmann SV, Kollmann A, Leach S (2007b) Directed exospermia: II. VUV-UV spectroscopy of specialized UV screens, including plant flavonoids, suggests using metabolic engineering to improve survival in space. Int J Astrobiol 7:1–11CrossRefGoogle Scholar

Copyright information

© Springer Science+Business Media B.V. 2012

Authors and Affiliations

  1. 1.Institute of Ecology and Evolutionary BiologyUniversity of OregonEugeneUSA
  2. 2.School of Life SciencesArizona State UniversityTempeUSA

Personalised recommendations