Skip to main content
Log in

Photosynthetic symbionts in Antarctic terrestrial ecosystems: the physiological response of lichen photobionts to drought and cold

  • Published:
Symbiosis Aims and scope Submit manuscript

Abstract

Lichens form an important part of the biodiversity in terrestrial ecosystems of Antarctica where they represent the dominant vegetation. Previous studies on the genetic diversity of photobionts of lichens have indicated that clade S Trebouxia photobionts are the most widespread in continental Antarctica, predominantly in macrolichens. For the first time, a comparative study of the physiology of a variety of isolated Antarctic lichen photobionts (genus Trebouxia) was performed. Photosynthetic activity was examined by chlorophyll a fluorescence and correlated with freezing and desiccation under laboratory conditions and photosynthetic pigments were quantified in response to desiccation. Data were obtained from photobionts collected from the Antarctic regions of North Victoria Land, Coal Nunatak and Rothera Point, as well as from a European site (Gotland, Sweden). While the isolated algae reacted individually to stress treatments, they were highly susceptible to desiccation stress but could rapidly recover from freezing. Photobiont-specific physiological adaptations are considered to explain the dominance of clade S Trebouxia photobionts.

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.

Institutional subscriptions

Fig. 1
Fig. 2
Fig. 3
Fig. 4
Fig. 5

Similar content being viewed by others

Abbreviations

A:

Antheraxanthin

chl FY:

chlorophyll fluorescence yield

DEPS:

de-epoxidation status of the xanthophyll pool

F0 :

minimum chl FY in the dark-acclimatized state

FM :

maximum chl FY in the dark-acclimatized state

FV/FM :

maximum quantum yield of PS II

HPLC:

high performance liquid chromatography

NPQ:

non-photochemical quenching

PAM:

pulse-amplitude modulation

PS II:

photosystem II

ROS:

reactive oxygen species

SE:

standard error of the mean

TOM:

Trebouxia organic medium

V:

violaxanthin

Z:

zeaxanthin

References

  • Ahmadjian V (1967) A guide to the algae occurring as lichen symbionts: isolation, culture, cultural physiology and identification. Phycologia 6:127–160

    Article  CAS  Google Scholar 

  • Barták M, Váczi P, Smykla J (2007) Low-temperature limitation of primary photosynthetic processes in Antarctic lichens Umbilicaria antarctica and Xanthoria elegans. Polar Biol 31:47–51

    Article  Google Scholar 

  • Beck A (2002) Selektivität der Symbionten schwermetalltoleranter Flechten. PhD thesis, München

  • Block W (1996) Cold or drought – the lesser of two evils for terrestrial arthropods? Eur J Entomol 93:325–339

    Google Scholar 

  • Brandt A (2011) Genetische Diversität der Flechtenalgen von NorthVictoria Land, Antarktis. Diploma thesis, HHU Düsseldorf

  • De Vera J-PP, Ott S (2010) Resistance of symbiotic Eukaryotes. In: Seckbach J, Grube M (eds) Cellular origin. Life in extreme habitats and astrobiology. Symbiosis and stress. Springer, Dordrecht, pp 595–611

    Google Scholar 

  • Demmig-Adams B, Adams WW (1996) The role of xanthophyll cycle carotenoids in the protection of photosynthesis. Trends Plant Sci 1:21–26

    Article  Google Scholar 

  • Ertl L (1951) Über die lichtverhältnisse in laubflechten. Planta 39:245–270

    Article  Google Scholar 

  • Fernández-Marín B, Balaguer L, Esteban R, Becerril JM, García-Plazaola JI (2009) Dark induction of the photoprotective xanthophyll cycle in response to dehydration. J Plant Physiol 166:1734–1744

    Article  PubMed  Google Scholar 

  • Fernández-Marín B, Becerril JM, García-Plazaola JI (2010) Unravelling the roles of desiccation-induced xanthophyll cycle activity in darkness: a case study in Lobaria pulmonaria. Planta 231:1335–1342

    Article  PubMed  Google Scholar 

  • Friedl T (1989) Systematik und Biologie von Trebouxia (Microthamniales, Chlorophyta) als Phycobiont der Parmeliaceae (lichenisierte Ascomyceten). PhD thesis, Bayreuth

  • Hájek J, Barták M, Dubová J (2006) Inhibition of photosynthetic processes in foliose lichens induced by temperature and osmotic stress. Biol Plantarum 50:624–634

    Article  Google Scholar 

  • Harańczyk H, Nowak P, Bacior M, Lisowska M, Marzec M, Florek M, Olech MA (2012) Bound water freezing in Antarctic Umbilicaria aprina from Schirmacher Oasis. Antarct Sci 24:342–352

    Article  Google Scholar 

  • Helms G (2003) Taxonomy and Symbiosis in Associations of Physciaceae and Trebouxia, PhD thesis, Tübingen

  • Helms G, Friedl T, Rambold G, Mayrhofer H (2001) Identification of photobionts from the lichen family Physciaceae using algal-specific ITS rDNA sequencing. Lichenologist 33:73–86

    Article  Google Scholar 

  • Honegger R (2009) Ökologische Aspekte der Wechselbeziehung zwischen Pilz und Alge. Rundgespräche Kommission Ökol 36:25–41

    Google Scholar 

  • Huiskes AHL, Convey P, Bergstrom DM (2006) Trends in Antarctic terrestrial and limnetic ecosystems: Antarctica as a global indicator. In: Bergstrom DM, Convey P, Huiskes AHL (eds) Trends in Antarctic terrestrial and limnetic ecosystems. Springer, Dordrecht, pp 1–14

    Chapter  Google Scholar 

  • Kappen L (1973) Response to extreme environments. In: Ahmadjian V, Hale ME (eds) The lichens. Academic, New York, pp 311–380

    Chapter  Google Scholar 

  • Kappen L (1993) Plant activity under Snow and Ice, with particular reference to lichens. Arctic 46:297–302

    Google Scholar 

  • Kappen L (2000) Some aspects of the great success of lichens in Antarctica. Ant Sci 72(3):314–324

    Google Scholar 

  • Kappen L, Breuer M (1991) Ecological and physiological investigations in continental Antarctic cryptogams. II. Moisture relations and photosynthesis of lichens near Casey station, Wilkes land. Antarct Sci 3:273–278

    Google Scholar 

  • Kappen L, Lange OL (1970) The cold resistance of phycobionts from macrolichens of various habitats. Lichenologist 4:289–293

    Article  Google Scholar 

  • Kappen L, Lange OL (1972) Die Kälteresistenz einiger Makrolichenen. Flora 161:1–29

    Google Scholar 

  • Kappen L, Valladares F (1999) Opportunistic growth and desiccation tolerance: The ecological success of poikilohydrous autotrophs. In: Pugnaire FI, Valladares F (eds) Handbook of functional plant ecology. Marcel Dekker, Basel, pp 121–194

    Google Scholar 

  • Kappen L, Sommerkorn M, Schroeter B (1995) Carbon acquisition and water relations of lichens in polar regions – potentials and limitations. Lichenologist 27:531–545

    Google Scholar 

  • Kennedy AD (1993) Water as a limiting factor in the Antarctic terrestrial environment: a biogeographical synthesis. Arct Alp Res 25:308–315

    Article  Google Scholar 

  • Kosugi M, Arita M, Shizuma R, Moriyama Y, Kashino Y, Koike H, Satoh K (2009) Responses to desiccation stress in lichens are different from those in their photobionts. Plant Cell Physiol 50(4):879–888

    Article  PubMed  CAS  Google Scholar 

  • Kranner I, Birtic S (2005) A modulating role for antioxidants in desiccation tolerance. Integr Comp Biol 45:734–740

    Article  PubMed  CAS  Google Scholar 

  • Kranner I, Cram WJ, Zorn M, Wornik S, Yoshimura I, Stabentheiner E, Pfeifhofer HW (2005) Antioxidants and photoprotection in a lichen as compared to its isolated symbiotic partners. Proc Natl Acad Sci USA 102:3141–3146

    Article  PubMed  CAS  Google Scholar 

  • Kranner I, Beckett R, Hochman A, Nash TH (2008) Desiccation-tolerance in lichens: a review. Bryologist 111:576–593

    Article  Google Scholar 

  • Krause GH, Jahns P (2004) Non-photochemical energy dissipation determined by chlorophyll fluorescence quenching: Characterization and function. In: Papageorgiou GC, Govindjee (eds) Chlorophyll a fluorescence: A signature of photosynthesis. Springer, Dordrecht, pp 464–495

    Google Scholar 

  • Lange OL, Kappen L (1972) Photosynthesis of lichens from Antarctica. Antarct Res Ser Antarct Terr Biol 20:83–95

    Article  CAS  Google Scholar 

  • Maxwell K, Johnson GN (2000) Chlorophyll fluorescence – a practical guide. J Exp Bot 51:659–668

    Article  PubMed  CAS  Google Scholar 

  • Øvstedal DO, Lewis SRI (2001) Lichens of Antarctica and South Georgia. Cambridge University Press, Cambridge

    Google Scholar 

  • Pannewitz S, Schlensog M, Green TGA, Sancho LG, Schroeter B (2003) Are lichens active under snow in continental Antarctica? Oecologia 135:30–38

    PubMed  Google Scholar 

  • Pfeifhofer HW, Willfurth R, Zorn M, Kranner I (2002) Analysis of chlorophylls, carotenoids, and tocopherols in lichens. In: Kranner I, Beckett R, Varma A (eds) Protocols in lichenology. Culturing, biochemistry, ecophysiology and use in biomonitoring, 1st edn. Springer, Berlin, pp 363–378

    Chapter  Google Scholar 

  • Richter M, Rühle W, Wild A (1990) Studies on the mechanism of photosystem II photoinhibition I. A two-step degradation of D1-protein. Photosynth Res 24:229–235

    Article  CAS  Google Scholar 

  • Romeike J, Friedl T, Helms G, Ott S (2002) Genetic diversity of algal and fungal partners in four species of Umbilicaria (lichenized ascomycetes) along a transect of the Antarctic Peninsula. Mol Biol Evol 19:1209–1217

    Article  PubMed  CAS  Google Scholar 

  • Schaper T, Ott S (2003) Photobiont selectivity and interspecific interactions in lichen communities. I. Culture experiments with the mycobiont Fulgensia bracteata. Plant Biol 5:441–450

    Article  Google Scholar 

  • Schlensog M, Schroeter B (2000) Poikilohydry in Antarctic cryptogams and its influence on photosynthetic performance in mesic and xeric habitats. In: Davidson W, Howard-Williams C, Broady P (eds) Antarctic ecosystems. Models for wider ecological understanding. Caxton Press, Christchurch, pp 175–183

    Google Scholar 

  • Schlensog M, Schroeter B, Pannewitz S, Green TGA (2003) Adaptations of mosses and lichens to irradiance stress in maritime and continental habitats. In: Huiskes AHL, Gieskes WWC, Rozema J, Schorno RML, van der Vies SM, Wolff WJ (eds) Antarctic biology in a global context. Backhuys Publishers, Leiden, pp 161–166

    Google Scholar 

  • Schroeter B, Green TGA, Kappen L, Seppelt RD (1994) Carbon dioxide exchange at subzero temperatures. Field measurements on Umbilicaria aprina in Antarctica. Crypto Bot 4:233–241

    Google Scholar 

  • Schroeter B, Kappen L, Green TGA, Seppelt RD (1997) Lichens and the Antarctic environment: Effects of temperature and water availability on photosynthesis. In: Lyons W, Howard-Williams BC, Hawes I (eds) Ecosystem processes in Antarctic ice-free landscapes. A. A. Balkema, Rotterdam

    Google Scholar 

  • Schroeter B, Kappen L, Schulz F, Sancho L (2000) Seasonal variation in the carbon balance of lichen in the maritime Antarctic: Long-term measurements of photosynthetic activity in Usnea aurantiaco-atra. In: Davidson W, Howard-Williams C, Broady P (eds) Antarctic ecosystems: models for wider ecological understanding. Caxton, Christchurch, pp 258–262

    Google Scholar 

  • Valladares F, Sancho LG, Ascaso C (1997) Water storage in the lichen family Umbilicariaceae. Bot Acta 111:99–107

    Google Scholar 

  • Veerman J, Vasil’ev S, Paton GD, Ramanauskas J, Bruce D (2007) Photoprotection in the lichen Parmelia sulcata: the origins of desiccation-induced fluorescence quenching. Plant Physiol 145:997–1005

    Article  PubMed  CAS  Google Scholar 

  • Vráblikóvá H, Barták M, Wonisch A (2004) Changes in glutathione and xanthophyll cycle pigments in the high light-stressed lichens Umbilicaria antarctica and Lasallia pustulata. J Photo Biol 79:35–41

    Article  Google Scholar 

  • Walton DWH (1982) The Signy Island terrestrial reference sites: XV. Microclimatic monitoring, 1972–74. Brit Antarct Surv Bull 55:111–126

    Google Scholar 

  • Yoshimura I, Yamamoto Y, Nakano T, Finnie J (2002) Isolation and culture of lichen photobionts and mycobionts. In: Kranner I, Beckett R, Varma A (eds) Protocols in lichenology. Culturing, biochemistry, ecophysiology and use in biomonitoring, 1st edn. Springer, Berlin, pp 3–33

    Chapter  Google Scholar 

Download references

Acknowledgments

Special thanks are due to the BGR (Bundesanstalt für Geologie und Rohstoffe), Andreas Läufer and Detlef Damaske for inviting the second author to the expedition GANOVEX X and logistic support. The staff of the Gondwana Station is thanked for their invaluable help. Sample collection during GANOVEX X was financially supported by the Deutsche Forschungsgemeinschaft (Ot 96/15–1), within the framework of the DFG Antarctic Priority Program 1158. Our special thanks are due to Eva Posthoff for her invaluable technical support. The results are included in the doctoral thesis of Andres Sadowsky. Thanks are also due to the anonymous reviewers for their helpful comments.

Author information

Authors and Affiliations

Authors

Corresponding author

Correspondence to Andres Sadowsky.

Rights and permissions

Reprints and permissions

About this article

Cite this article

Sadowsky, A., Ott, S. Photosynthetic symbionts in Antarctic terrestrial ecosystems: the physiological response of lichen photobionts to drought and cold. Symbiosis 58, 81–90 (2012). https://doi.org/10.1007/s13199-012-0198-7

Download citation

  • Received:

  • Accepted:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1007/s13199-012-0198-7

Keywords

Navigation