Microbial Ecology

, Volume 67, Issue 2, pp 327–340 | Cite as

UV-Induced Effects on Growth, Photosynthetic Performance and Sunscreen Contents in Different Populations of the Green Alga Klebsormidium fluitans (Streptophyta) from Alpine Soil Crusts

  • C. Kitzing
  • T. Pröschold
  • U. KarstenEmail author
Environmental Microbiology


Members of the green algal genus Klebsormidium (Klebsormidiales, Streptophyta) are typical components of biological soil crust communities worldwide, which exert important ecological functions. Klebsormidium fluitans (F. Gay) Lokhorst was isolated from an aeroterrestrial biofilm as well as from four different biological soil crusts along an elevational gradient between 600 and 2350 m in the Tyrolean and South Tyrolean Alps (Austria, Italy), which are characterised by seasonally high solar radiation. Since the UV tolerance of Klebsormidium has not been studied in detail, an ecophysiological and biochemical study was applied. The effects of controlled artificial ultraviolet radiation (UVR; <9 W m–2 UV-A, <0.5 W m–2 UV-B) on growth, photosynthetic performance and the capability to synthesise mycosporine-like amino acids (MAAs) as potential sunscreen compounds were comparatively investigated to evaluate physiological plasticity and possible ecotypic differentiation within this Klebsormidium species. Already under control conditions, the isolates showed significantly different growth rates ranging from 0.42 to 0.74 μm day−1. The UVR effects on growth were isolate specific, with only two strains affected by the UV treatments. Although all photosynthetic and respiratory data indicated strain-specific differences under control conditions, UV-A and UV-B treatment led only to rather minor effects. All physiological results clearly point to a high UV tolerance in the K. fluitans strains studied, which can be explained by their biochemical capability to synthesize and accumulate a putative MAA after exposure to UV-A and UV-B. Using HPLC, a UV-absorbing compound with an absorption maximum at 324 nm could be identified in all strains. The steady-state concentrations of this Klebsormidium MAA under control conditions ranged from 0.09 to 0.93 mg g−1 dry weight (DW). While UV-A led to a slight stimulation of MAA accumulation, exposure to UV-B was accompanied by a strong but strain-specific increase of this compound (5.34–12.02 mg−1 DW), thus supporting its function as UV sunscreen. Although ecotypic differences in the UVR response patterns of the five K. fluitans strains occurred, this did not correlate with the altitude of the respective sampling location. All data indicate a generally high UV tolerance which surely contributes to the aeroterrestrial lifestyle of K. fluitans in soil crusts of the alpine regions of the European Alps.


Photosynthetically Active Radiation Biological Soil Crust Scytonemin Photon Flux Density Biological Soil Crust Community 
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.



Financial support by the Deutsche Forschungsgemeinschaft (DFG) (KA899/16-1/2/3/4) is gratefully acknowledged by U.K.


  1. 1.
    Bandaranayake WM (1998) Mycosporines: are they nature's sunscreens? Nat Prod Rep 15:159–172CrossRefPubMedGoogle Scholar
  2. 2.
    Belnap J, Lange OL (2001) Biological soil crusts: structure, function and management. Springer, Berlin, p 503Google Scholar
  3. 3.
    Belnap J, Büdel B, Lange OL (2001) Biological soil crusts: characteristics and distribution. In: Belnap J, Lange OL (eds) Biological soil crusts: structure, function and management. Springer, Berlin, pp 3–30CrossRefGoogle Scholar
  4. 4.
    Belnap J, Phillips SL, Flint S, Money J, Caldwell M (2008) Global change and biological soil crusts: effects of ultraviolet augmentation under altered precipitation regimes and nitrogen additions. Glob Chang Biol 14:670–686CrossRefGoogle Scholar
  5. 5.
    BMEPC-Baltic Marine Environment Protection Commission (1988) Guidelines for the Baltic monitoring programme for the third stage. Loose Sheet Version Baltic Sea Environ Proc 27D:16–23Google Scholar
  6. 6.
    Bischof K, Rautenberger R, Brey L, Perez-Llorens JL (2006) Physiological acclimation along gradients of solar irradiance within mats of the filamentous green macroalga Chaetomorpha linum from southern Spain. Mar Ecol Prog Ser 306:165–175CrossRefGoogle Scholar
  7. 7.
    Bornman JF (1989) Target sites of UV-radiation in photosynthesis of higher plants. J Photochem Photobiol B Biol 4:145–158CrossRefGoogle Scholar
  8. 8.
    Blumthaler M, Ambach W (1990) Indication of increasing solar ultraviolet-B radiation flux in Alpine regions. Science 248:206–208CrossRefPubMedGoogle Scholar
  9. 9.
    Blumenthaler M, Ambach W, Möller R (1996) Increase in solar UV radiation with altitude. J Photochem Photobiol 39B:130–134Google Scholar
  10. 10.
    Buma AGJ, Bölen P, Jeffrey WH (2003) UVR-induced DNA damage in aquatic organisms. In: Helbing W, Zagarese S (eds) UV effects in aquatic organisms and ecosystem. Comprehensive series in photoscience. Elsevier, Amsterdam, pp 291–327CrossRefGoogle Scholar
  11. 11.
    Chiew-Yen W, Wan-Loy C, Marchant H, Siew-Moi P (2004) Growth response, biochemical composition and fatty acid profiles of four Antarctic microalgae subjected to UV radiation stress. Malays J Sci 23:103–118Google Scholar
  12. 12.
    Conde FR, Churio MS, Previtali CM (2000) The photoprotector mechanism of mycosporine-like amino acids. Excited-state properties and photostability of porphyra-334 in aqueous solution. J Photochem Photobiol 56B:139–144CrossRefGoogle Scholar
  13. 13.
    Darienko T, Gustavs L, Mudimu O, Menendez CR, Schumann R, Karsten U, Friedl T, Pröschold T (2010) Chloroidium, a common terrestrial coccoid green alga previously assigned to Chlorella (Trebouxiophyceae, Chlorophyta). Eur J Phycol 1–17Google Scholar
  14. 14.
    Elbert W, Weber B, Burrows S, Steinkamp J, Büdel B, Andreae MO, Pöschl U (2012) Contribution of cryptogamic covers to the global cycles of carbon and nitrogen. Nat Geosci 5:459–462CrossRefGoogle Scholar
  15. 15.
    Ettl H, Gärtner G (1995) Syllabus der Boden-, Luft- und Flechtenalgen. Gustav Fischer, Stuttgart, p 721Google Scholar
  16. 16.
    Garcia-Pichel F (1995) Scalar irradiance fiber-optic microprobe for the measurement of ultraviolet radiation at high spatial resolution. Photochem Photobiol 61:248–254CrossRefGoogle Scholar
  17. 17.
    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 59:163–169PubMedCentralPubMedGoogle Scholar
  18. 18.
    Garcia-Pichel F, Castenholz RW (1991) Characterization and biological implications of scytonemin, a cyanobacterial sheath pigment. J Phycol 27:395–409CrossRefGoogle Scholar
  19. 19.
    Genty B, Briantais JM, Baker NR (1994) The relationship between the quantum yield of photosynthetic electron transport and quenching of chlorophyll fluorescence. Biochim Biophys Acta 990:87–92CrossRefGoogle Scholar
  20. 20.
    Gustavs L, Eggert A, Michalik D, Karsten U (2010) Physiological and biochemical responses of green microalgae from different habitats to osmotic and matric stress. Protoplasma 243:3–14CrossRefPubMedGoogle Scholar
  21. 21.
    Gustavs L, Schumann R, Eggert A, Karsten U (2009) In vivo growth fluorometry: accuracy and limits of microalgal growth rate measurements in ecophysiological investigations. Aquat Microb Ecol 55:95–104CrossRefGoogle Scholar
  22. 22.
    Hanelt D (1998) Capability of dynamic photoinhibition in Arctic macroalgae is related to their depth distribution. Mar Biol 131:361–369CrossRefGoogle Scholar
  23. 23.
    Holzinger A, Lütz C, Karsten U, Wiencke C (2004) The effect of ultraviolet radiation on ultrastructure and photosynthesis in the red macroalgae Palmaria palmata and Odonthallia dentata from Arctic waters. Plant Biol 6:568–577CrossRefPubMedGoogle Scholar
  24. 24.
    Holzinger A, Karsten U, Lütz C, Wiencke C (2006) Ultrastructure and photosynthesis in the supralittoral green macroalga Prasiola crispa (Lightfoot) Kützing from Spitsbergen (Norway) under UV exposure. Phycologia 45:168–177CrossRefGoogle Scholar
  25. 25.
    Holzinger A, Lütz C, Karsten U (2011) Desiccation stress causes structural and ultrastructural alterations in the aeroterrestrial green alga Klebsormidium crenulatum (Klebsormidiophyceae, Streptophyta) isolated from an alpine soil crust. J Phycol 47:591–602CrossRefGoogle Scholar
  26. 26.
    Holzinger A, Roleda MY, Lütz C (2009) The vegetative arctic freshwater green alga Zygnema is insensitive to experimental UV exposure. Micron 40:831–838CrossRefPubMedGoogle Scholar
  27. 27.
    Hoyer K, Karsten U, Sawall T, Wiencke C (2001) Photoprotective substances in Antarctic macroalgae and their variation with respect to depth distribution, different tissues and developmental stages. Mar Ecol Prog Ser 211:117–129CrossRefGoogle Scholar
  28. 28.
    John DM (2002) Orders chaetophorales, klebsormidiales, microsporales, ulotrichales. In: John DM, Whitton BA, Brook AJ (eds) The freshwater algal flora of the British Isles. An identification guide to freshwater and terrestrial algae. Cambridge University Press, Cambridge, pp 433–468Google Scholar
  29. 29.
    Johnson ZI, Zinser ER, Coel A, McNulty NP, Woodward M, Chisholm SW (2006) Niche partitioning among Prochlorococcus ecotypes along ocean-scale environmental gradients. Science 311:1737–1740CrossRefPubMedGoogle Scholar
  30. 30.
    Karsten U (2008) Defense strategies of algae and cyanobacteria against solar UVR. In: Amsler CD (ed) Algal chemical ecology. Springer, Berlin, pp 273–296CrossRefGoogle Scholar
  31. 31.
    Karsten U, Maier J, Garcia-Pichel F (1998) Seasonality in UV-absorbing compounds of cyanobacterial mat communities from an intertidal mangrove flat. Aquat Microb Ecol 16:37–44CrossRefGoogle Scholar
  32. 32.
    Karsten U, Friedl T, Schumann R, Hoyer K, Lembcke S (2005) Mycosporin-like amino acids and phylogenies in green algae: Prasiola and its relatives from the Trebouxiophyceae (Chlorophyta). J Phycol 41:557–566CrossRefGoogle Scholar
  33. 33.
    Karsten U, Lütz C, Holzinger A (2010) Ecophysiological performance of the aeroterrestrial green alga Klebsormidium crenulatum (Charophyceae, Streptophyta) isolated from an alpine soil crust with an emphasis on desiccation stress. J Phycol 46:1187–1197CrossRefGoogle Scholar
  34. 34.
    Karsten U, Holzinger A (2012) Light, temperature, and desiccation effects on photosynthetic activity, and drought-induced ultrastructural changes in the green alga Klebsormidium dissectum (Streptophyta) from a high alpine soil crust. Microb Ecol 63:51–63CrossRefPubMedGoogle Scholar
  35. 35.
    Karsten U, Sawall T, Hanelt D, Bischof K, Figueroa FL, Flores-Moya A, Wiencke C (1998) An inventory of UV-absorbing mycosporine-like amino acids. Bot Mar 41:443–453CrossRefGoogle Scholar
  36. 36.
    Karsten U, Lembcke S, Schumann R (2007) The effects of ultraviolet radiation on photosynthetic performance, growth and sunscreen compounds in aeroterrestrial biofilm algae isolated from building facades. Planta 225:991–1000CrossRefPubMedGoogle Scholar
  37. 37.
    Karsten U, Escoubeyrou K, Charles F (2009) The effect of re-dissolution solvents and HPLC columns on the analysis of mycosporine-like amino acids in the eulittoral macroalgae Prasiola crispa and Porphyra umbilicalis. Helgol Mar Res 63:231–238CrossRefGoogle Scholar
  38. 38.
    Körner C (2003) Alpine plant life—functional plant ecology of high mountain ecosystems. Springer, Berlin, p 344Google Scholar
  39. 39.
    Kühl M, Jörgensen BB (1994) The light field of microbenthic communities: radiance distribution and microscale optics of sandy coastal sediments. Limnol Oceanogr 39:1368–1398CrossRefGoogle Scholar
  40. 40.
    Lokhorst GM (1996) Comparative taxonomic studies on the genus Klebsormidium (Charophyceae) in Europe. In: Jühlich W (ed) Cryptogamic studies, vol. 5. Fischer, Stuttgart, pp 1–55Google Scholar
  41. 41.
    Lorenz M, Schubert H, Forster RM (1997) In vitro- and in vivo effects of ultraviolet-B radiation on the energy transfer in phycobilisomes. Photosynthetica 33:517–527Google Scholar
  42. 42.
    Lütz C, Engel L (2007) Changes in chloroplast ultrastructure in some high-alpine plants: adaptation to metabolic demands and climate? Protoplasma 231:183–192CrossRefPubMedGoogle Scholar
  43. 43.
    Luo W, Pflugmacher S, Pröschold T, Walz N, Krienitz L (2006) Genotype versus phenotype variability in Chlorella and Micractinium (Chlorophyta, Trebouxiophyceae). Protist 157:315–333CrossRefPubMedGoogle Scholar
  44. 44.
    Mathews DH, Sabina J, Zuker M, Turner DH (1999) Expanded sequence dependence of thermodynamic parameters improves prediction of RNA secondary structure. J Mol Biol 288:911–940CrossRefPubMedGoogle Scholar
  45. 45.
    Pichrtová M, Remias D, Lewis LA, Holzinger A (2013) Changes in phenolic compounds and cellular ultrastructure of Arctic and Antarctic strains of Zygnema (Zygnematophyceae, Streptophyta) after exposure to experimentally enhanced UV to PAR ratio. Microb Ecol 65:68–83PubMedCentralCrossRefPubMedGoogle Scholar
  46. 46.
    Pröschold T, Marin B, Schlösser UG, Melkonian M (2001) Molecular phylogeny and taxonomic revision of Chlamydomonas (Chlorophyta). I. Emendation of Chlamydomonas Ehrenberg and Chloromonas Gobi, and description of Oogamochlamys gen. nov. and Lobochlamys gen. nov. Protist 152:265–300CrossRefPubMedGoogle Scholar
  47. 47.
    Pröschold T, Harris EH, Coleman AW (2005) Portrait of a species: Chlamydomonas reinhardtii. Genetics 170:1601–1610PubMedCentralCrossRefPubMedGoogle Scholar
  48. 48.
    Reisigl H (1964) Zur Systematik und Ökologie alpiner Bodenalgen. Österr Botsch Zagreb 111:402–499CrossRefGoogle Scholar
  49. 49.
    Remias D, Holzinger A, Aigner S, Lütz C (2012) Ecophysiology and ultrastructure of Ancylonema nordenskiöldii (Zygnematales, Streptophyta), causing brown ice on glaciers in Svalbard (high Arctic). Polar Biol 35:899–908CrossRefGoogle Scholar
  50. 50.
    Renger G, Voss M, Grabber P, Schulze A (1986) Effect of UV irradiation on different partial reactions of the primary processes of photosynthesis. In: Worrest RC, Caldwell MM (eds) Stratospheric ozone reduction, solar ultraviolet radiation and plant life. NATO ASI series, G8. Springer, Berlin, pp 171–184CrossRefGoogle Scholar
  51. 51.
    Rindi F, Mikhailyuk TI, Sluiman HJ, Friedl T, Lopez-Bautista JM (2011) Phylogenetic relationships in Interfilum and Klebsormidium (Klebsormidiophyceae, Streptophyta). Mol Phylogenet Evol 58:218–231CrossRefPubMedGoogle Scholar
  52. 52.
    Roleda MY, Clayton MN, Wiencke C (2006) Screening capacity of UV-absorbing compounds in spores of Arctic Laminariales. J Exp Mar Biol Ecol 338:123–133CrossRefGoogle Scholar
  53. 53.
    Schmucki DA, Philipona R (2002) Ultraviolet radiation in the Alps: the altitude effect. Opt Eng 43:3090–3095CrossRefGoogle Scholar
  54. 54.
    Schreiber U, Bilger W, Neubauer C (1994) Chlorophyll fluorescence as a non-instrusive indicator for rapid assessment of in vivo photosynthesis. Ecol Stud 100:49–70Google Scholar
  55. 55.
    Sherwood AR (2004) New records of freshwater macroalgae and diatoms from the Hawaiian Islands. Records of the Hawaii biological survey for 2003. Occasional Papers Bernice P. Bishop Museum. 79:1–8Google Scholar
  56. 56.
    Shick JM, Dunlap WC (2002) Mycosporine-like amino acids and related gadusol: biosynthesis, accumulation and UV-protective functions in aquatic organisms. Ann Rev Physiol 64:223–262CrossRefGoogle Scholar
  57. 57.
    Siebert S, Backofen R (2005) MARNA: multiple alignment and consensus structure prediction of RNAs based on sequence structure comparisons. Bioinformatics 21:3352–3359CrossRefPubMedGoogle Scholar
  58. 58.
    Sommaruga R (2001) The role of UV radiation in the ecology of alpine lakes. J Photochem Photobiol B Biol 62:35–42CrossRefGoogle Scholar
  59. 59.
    Starr RC, Zeikus JA (1993) UTEX—the culture collection of algae at the University of Texas at Austin 1993 list of cultures. J Phycol 29:1–106CrossRefGoogle Scholar
  60. 60.
    Strid A, Chow WS, Anderson JM (1990) Effects of supplementary ultraviolet-B radiation on photosynthesis in Pisum sativum. Biochim Biophys Acta 1020:260–268CrossRefGoogle Scholar
  61. 61.
    Tschaikner A (2008) Soil algae and soil algal crusts in the alpine regions of Tyrol (Ötztal, Austria). Ph.D. thesis, University of Innsbruck, Innsbruck, p 58Google Scholar
  62. 62.
    Türk R, Gärtner G (2001) Biological soil crust in the subalpine, and nival areas in the Alps. In: Belnap J, Lange OL (eds) Biological soil crusts: structure, function and management. Springer, Berlin, pp 67–73CrossRefGoogle Scholar
  63. 63.
    Vass I (1997) Adverse effects of UV-B light on the structure and function of the photosynthetic apparatus. In: Pessarakli M (ed) Handbook of photosynthesis. Dekker, New York, pp 931–949Google Scholar
  64. 64.
    Walsby AE (1997) Numerical integration of phytoplankton photosynthesis through time and depth in a water column. New Phytol 136:189–209CrossRefGoogle Scholar
  65. 65.
    Warkentin M, Freese H, Karsten U, Schumann R (2007) New and fast method to quantify respiration rates of bacterial and plankton communities in freshwater ecosystems by using optical oxygen sensor spots. Appl Environ Microbiol 72:6722–6729CrossRefGoogle Scholar
  66. 66.
    Webb WL, Newton M, Starr D (1974) Carbon dioxide exchange of Alnus rubra: a mathematical model. Oecologia 17:281–291CrossRefGoogle Scholar
  67. 67.
    Yoshiki M, Tsuge K, Tsuruta Y, Yoshimura T, Koganemaru K, Sumi T, Matsui T, Matsumoto K (2009) Production of new antioxidant compounds from mycosporine-like amino acid, porphyra-334 by heat treatment. Food Chem 113:1127–1132CrossRefGoogle Scholar
  68. 68.
    Zepp RG, Erickson DJ III, Paul ND, Sulzberger B (2007) Interactive effects of solar UV radiation and climate change on biogeochemical cycling. Photochem Photobiol Sci 6:286–300CrossRefPubMedGoogle Scholar
  69. 69.
    Zuker M (2003) Mfold web server for nucleic acid folding and hybridization prediction. Nucleic Acids Res 31:3406–3416PubMedCentralCrossRefPubMedGoogle Scholar

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© Springer Science+Business Media New York 2013

Authors and Affiliations

  1. 1.Institute of Biological Sciences, Applied Ecology and PhycologyUniversity of RostockRostockGermany

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