Skip to main content
Log in

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

  • Environmental Microbiology
  • Published:
Microbial Ecology Aims and scope Submit manuscript

Abstract

Members of the cosmopolitan green algal genus Klebsormidium (Klebsormidiales, Streptophyta) are typical components of terrestrial microbiotic communities such as biological soil crusts, which have many important ecological functions. In the present study, Klebsormidium dissectum (Gay) Ettl & Gärtner was isolated from a high alpine soil crust in the Tyrolean Alps, Austria. Physiological performance in terms of growth and photosynthesis was investigated under different controlled abiotic conditions and compared with ultrastructural changes under the treatments applied. K. dissectum showed very low light requirements as reflected in growth patterns and photosynthetic efficiency. Increasing temperatures from 5°C to 40°C led to different effects on respiratory oxygen consumption and photosynthetic oxygen evolution. While at low temperatures (5–10°C), respiration was not detectable or on a very low level, photosynthesis was relatively high, Reversely, at the highest temperature, respiration was unaffected, and photosynthesis strongly inhibited pointing to strong differences in temperature sensitivity between both physiological processes. Although photosynthetic performance of K. dissectum was strongly affected under short-term desiccation and recovered only partly after rehydration, this species was capable to survive even 3 weeks at 5% relative air humidity. K. dissectum cells have a cell width of 5.6 ± 0.3 μm and a cell length of 8.4 ± 2.0 μm. Desiccated cells showed a strongly reduced cell width (46% of control) and cell length (65% of control). In addition, in desiccated cells, fewer mitochondria were stained by DIOC6, and damaged plasma membranes were detected by FM 1–43 staining. High-pressure freeze fixation as well as chemical fixation allowed visualizing ultrastructural changes caused by desiccation. In such cells, the nucleus and chloroplast were still visibly intact, but the extremely thin cell walls (75–180 nm) were substantially deformed. The cytoplasm appeared electron dense and mitochondria were altered. Although K. dissectum can be characterized as euryoecious species, all ecophysiological and ultrastructural data indicate susceptibility to desiccation. However, the steadily occurring fragmentation of filaments into smaller units leads to improved self protection and thus may represent a life strategy to better survive longer periods of drought in exposed alpine soil crusts.

This is a preview of subscription content, log in via an institution to check access.

Access this article

Price excludes VAT (USA)
Tax calculation will be finalised during checkout.

Instant access to the full article PDF.

Figure 1
Figure 2
Figure 3
Figure 4
Figure 5
Figure 6
Figure 7
Figure 8
Figure 9
Figure 10

Similar content being viewed by others

References

  1. Abe K, Mihara H, Hirano M (1998) Characteristics of growth and carotenoid accumulation of the aerial microalga Trentepohlia aurea in liquid culture. J Mar Biotechnol 6:53–58

    CAS  Google Scholar 

  2. Belnap J, Lange OL (2001) Biological soil crusts: structure. Function and Management. Springer, Berlin, Germany, p 503

    Book  Google Scholar 

  3. Bischof K, Hanelt D, Tüg H, Karsten U, Brouwer PEM, Wiencke C (1998) Acclimation of brown algal photosynthesis to ultraviolet radiation in Arctic coastal waters (Spitsbergen, Norway). Polar Biol 20:388–395

    Article  Google Scholar 

  4. Büdel B (2001) Biological soil crusts of European temperate and Mediterranean regions. In: Belnap J, Lange OL (eds) Biological soil crusts: structure. Function and Management, Springer, Berlin, pp 75–85

    Google Scholar 

  5. Cardon ZG, Gray DW, Lewis LA (2008) The green algal underground: evolutionary secrets of desert cells. BioSci 58:114–122

    Article  Google Scholar 

  6. 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 45:1–17

    Article  Google Scholar 

  7. Davey MC (1989) The effects of freezing and desiccation on photosynthesis and survival of terrestrial Antarctic algae and cyanobacteria. Polar Biol 10:29–36

    Article  Google Scholar 

  8. De Winder B, Matthijs HCP, Mur LR (1990) The effect of dehydration and ion stress on carbon dioxide fixation in drought-tolerant phototrophic micro-organisms. FEMS Microbiol Ecol 74:33–38

    Article  Google Scholar 

  9. Domozych DS, Roberts R, Danyow C, Fltter R, Smith B, Providence K (2003) Plasmolysis, hechtian strand formation, and localized membrane-wall adhesions in the desmid, Closterium acerosum (Chlorophyta). J Phycol 39:1194–1206

    Article  CAS  Google Scholar 

  10. Elbert W, Weber B, Büdel B, Andreae MO, Pöschl U (2009) Microbiotic crusts on soil, rock and plants: neglected major players in the global cycles of carbon and nitrogen? Biogeosci Discuss 6:6983–7015

    Article  Google Scholar 

  11. Elster J, Degma P, Kovacik L, Valentova L, Sramkova K, Pereira AB (2008) Freezing and desiccation injury resistance in the filamentous green alga Klebsormidium from the Antarctic, Arctic and Slovakia. Biologia 63:839–847

    Article  Google Scholar 

  12. Ettl H, Gärtner G (1995) Syllabus der Boden-, Luft- und Flechtenalgen. Gustav Fischer, Stuttgart, p 721

    Google Scholar 

  13. Evans RD, Johansen JR (1999) Microbiotic crusts and ecosystem processes. Crit Rev Plant Sci 18:83–225

    Article  Google Scholar 

  14. Gärtner G (2004) ASIB—the culture collection of algae at the Botanical Institute, Innsbruck, Austria. Nova Hed 79:71–76

    Article  Google Scholar 

  15. Gray DW, Lewis LA, Cardon ZG (2007) Photosynthetic recovery following desiccation of desert green algae (Chlorophyta) and their aquatic relatives. Plant Cell Environ 30:1240–1255

    Article  PubMed  CAS  Google Scholar 

  16. Green TGA, Nash TH III, Lange OL (2008) Physiological ecology of carbon dioxide exchange. In: Nash TH III (ed) Lichen biology. Cambridge University Press, Cambridge, pp 152–181

    Chapter  Google Scholar 

  17. Gustavs L, Schumann R, Eggert A, Karsten U (2009) In vivo growth fluorometry: accuracy and limits of microalgal growth rate measurements in ecophysiological investigations. Aqua Microb Ecol 55:95–104

    Article  Google Scholar 

  18. Häubner N, Schumann R, Karsten U (2006) Aeroterrestrial algae growing on facades—response to temperature and water stress. Microb Ecol 51:285–293

    Article  PubMed  Google Scholar 

  19. Holzinger A (2009) Desiccation tolerance in green algae: implications of physiological adaptation and structural requirements. In: Hagen KN (ed) Algae, nutrition, pollution control and energy sources. Nova, Hauppauge, New York, pp 41–56

    Google Scholar 

  20. 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 45:168–177

    Article  Google Scholar 

  21. Holzinger A, Roleda M, Lütz C (2009) The vegetative arctic green alga Zygnema is insensitive to experimental UV exposure. Micron 40:831–838

    Article  PubMed  Google Scholar 

  22. Holzinger A, Tschaikner A, Remias D (2010) Cytoarchitecture of the desiccation-tolerant green alga Zygogonium ericetorum. Protoplasma 243:15–24

    Article  PubMed  CAS  Google Scholar 

  23. Holzinger, A, Lütz, C, Karsten, U (2011). Desiccation stress causes structural and ultra-structural alterations in the aeroterrestrial green alga Klebsormidium crenulatum (Klebsormidiophyceae, Streptophyta) isolated from an alpine soil crust. J Phycol 47:591–602. doi:10.1111/j.1529-8817.2011.00980.x

    Google Scholar 

  24. Honda M, Hashimoto H (2007) Close association of centrosomes to the distal ends of the microbody during its growth, division and partitioning in the green alga Klebsormidium flaccidum. Protoplasma 231:127–135

    Article  PubMed  Google Scholar 

  25. Karsten U, Friedl T, Schumann R, Hoyer K, Lembcke S (2005) Mycosporine-like amino acids (MAAs) and phylogenies in green algae: Prasiola and its relatives from the Trebouxiophyceae (Chlorophyta). J Phycol 41:557–566

    Article  CAS  Google Scholar 

  26. Karsten U, Lütz C, Holzinger A (2010) Ecophysiological performance of the aeroterrestrial green alga Klebsormidium crenulatum (Klebsormidiophyceae, Streptophyta) isolated from an alpine soil crust with an emphasis on desiccation stress. J Phycol 46:1187–1197

    Article  Google Scholar 

  27. Körner C (2003) Alpine plant life—functional plant ecology of high mountain ecosystems. Springer, Berlin, p 344

    Google Scholar 

  28. Kouril R, Ilik P, Tomek P, Naus J, Poulickova A (2001) Chlorophyll fluorescence temperature curve on Klebsormidium flaccidum cultivated at different temperature regimes. J Plant Physiol 158:1131–1136

    Article  CAS  Google Scholar 

  29. Kühl M, Jörgensen BB (1994) The light field of microbenthic communities: radiance distribution and microscale optics of sandy coastal sediments. Limnol Oceanogr 39:1368–1398

    Article  Google Scholar 

  30. Larcher W (2003) Physiological plant ecology: ecophysiology and stress physiology of functional. Springer, Berlin, p 513

    Google Scholar 

  31. Larcher W, Wagner J (2009) High mountain bioclimate: temperatures near the ground recorded from the timber-line to the nival zone in the Central Alps. Contrib Nat Hist 12:857–874

    Google Scholar 

  32. Lewis LA (2007) Chlorophyta on land: independent lineages of green eukaryotes from arid lands. In: Seckbach J (ed) Algae and Cyanobacteria in extreme environments. Springer, Berlin

    Google Scholar 

  33. Lukesova A (2001) Soil algae in brown coal and lignite post-mining areas in central Europe (Czech Republic and Germany). Restor Ecol 9:341–350

    Article  Google Scholar 

  34. Lüttge U, Büdel B (2010) Resurrection kinetics of photosynthesis in desiccation-tolerant terrestrial green algae (Chlorophyta) on tree bark. Plant Biol 12:437–444

    Article  PubMed  Google Scholar 

  35. Morison MO, Sheath RG (1985) Responses to desiccation stress by Klebsormidium rivulare (Ulotrichales, Chlorophyta) from a Rhode Island stream. Phycologia 24:129–145

    Article  CAS  Google Scholar 

  36. Nagao M, Matsui K, Uemura M (2008) Klebsormidium flaccidum, a charophycean green alga, exhibits cold acclimation that is closely associated with compatible solute accumulation and ultrastructural changes. Plant Cell Environ 31:872–885

    Article  PubMed  CAS  Google Scholar 

  37. Porra RJ, Thompson WA, Kriedmann PE (1989) Determination of accurate extinction coefficients and simultaneous equations for assaying chlorophylls a and b extracted with four different solvents: verification of the concentration of chlorophyll standards by atomic absorption spectroscopy. Biochim Biophys Acta 975:384–394

    Article  CAS  Google Scholar 

  38. ap Rees T, Burrell MM, Entwistle TG, Hammond JB, Kirk D, Kruger NJ (1988) Effects of low temperature on the respiratory metabolism of carbohydrates by plants. Symp Soc Exp Biol 42:377–393

    PubMed  CAS  Google Scholar 

  39. Reisigl H (1964) Zur Systematik und Ökologie alpiner Bodenalgen. Österr Bot Z 111:402–499

    Article  Google Scholar 

  40. Remias D, Albert A, Lütz C (2010) Effects of simulated, but realistic, elevated UV irradiation on photosynthesis and pigment composition of the alpine snow alga Chlamydomonas nivalis and the Arctic soil alga Tetracystis sp. (Chlorophyceae). Photosynthetica 48:269–277

    Article  CAS  Google Scholar 

  41. Rindi F, Guiry MD, Lopez-Bautista JM (2008) Distribution, morphology, and phylogeny of Klebsormidium (Klebsormidiales, Charophyceae) in urban environments in Europe. J Phycol 44:1529–1540

    Article  Google Scholar 

  42. Rindi F, Mikhailyuk TI, Sluiman HJ, Friedl T, Lopez-Bautista JM (2011) Phylogenetic relationships in Interfilum and Klebsormidium (Klebsormidiophyceae, Streptophyta). Mol Phylogen Evol 58:218–231

    Article  Google Scholar 

  43. Starr RC, Zeikus JA (1993) UTEX—the culture collection of algae at the University of Texas at Austin 1993 list of cultures. J Phycol 29:1–106

    Article  Google Scholar 

  44. Tan CK, Lee YK, Ho KK (1993) Effect of light intensity and ammonium-N on carotenogenesis of Trentepohlia odorata and Dunaliella bardawil. J Appl Phycol 5:547–549

    Article  CAS  Google Scholar 

  45. Tschaikner A (2008) Soil algae and soil algal crusts in the alpine regions of Tyrol (Ötztal, Austria). Ph.D. thesis, University of Innsbruck, p 58

  46. Tschaikner A, Ingolic E, Holzinger A, Gärtner G (2007) Phycobionts of some species of Evernia and Ramalina. Herzogia 20:53–60

    Google Scholar 

  47. Türk R, Gärtner G (2001) Biological soil crusts in the subalpine, alpine, and nival areas in the Alps. In: Belnap J, Lange OL (eds) Biological soil crusts: structure. Function and Management, Springer, Berlin, pp 67–73

    Google Scholar 

  48. Webb WL, Newton M, Starr D (1974) Carbon dioxide exchange of Alnus rubra: a mathematical model. Oecologia 17:281–291

    Article  Google Scholar 

Download references

Acknowledgements

The present investigation was undertaken during the first author's sabbatical at the University of Innsbruck in Prof. Cornelius Lütz's laboratory. We thank W. Kofler, Institute of Botany, University of Innsbruck for SEM preparations. Prof. U. Lütz-Meindl, University of Salzburg is kindly acknowledged for providing access to her Leica high-pressure freezing device. We thank Mag. A. Andosch, University of Salzburg for technical help with the freeze substitution. Dr. Thomas Pröschold, University of Vienna, undertook the ITS2 rRNA analysis. Financial support by the Deutsche Forschungsgemeinschaft (DFG) (KA899/16-1/2) is gratefully acknowledged by U.K. The study has been supported by a Research Grant from the “Universitätszentrum Obergurgl”, University of Innsbruck to A.H. The authors are grateful to Dr. Daniel Remias for technical support with the photosynthetic oxygen measurements. The authors like to thank Dr. Angelika Tschaikner and Prof. Georg Gärtner for species identification, as well as Prof. Christian Wiencke for lending the PAM.

Author information

Authors and Affiliations

Authors

Corresponding author

Correspondence to Ulf Karsten.

Rights and permissions

Reprints and permissions

About this article

Cite this article

Karsten, U., Holzinger, A. 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, 51–63 (2012). https://doi.org/10.1007/s00248-011-9924-6

Download citation

  • Received:

  • Accepted:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1007/s00248-011-9924-6

Keywords

Navigation