Skip to main content
SpringerLink
Log in

Symbiosis as a successful strategy in continental Antarctica: performance and protection of Trebouxia photosystem II in relation to lichen pigmentation

  • Published:
Polar Biology Aims and scope Submit manuscript

Abstract

Lichens as symbiotic associations consisting of a fungus (the mycobiont) and a photosynthetic partner (the photobiont) dominate the terrestrial vegetation of continental Antarctica. The photobiont provides carbon nutrition for the fungus. Therefore, performance and protection of photosystem II is a key factor of lichen survival. Potentials and limitations of photobiont physiology require intense investigation to extend the knowledge on adaptation mechanisms in the lichen symbiosis and to clarify to which extent photobionts benefit from symbiosis. Isolated photobionts and entire lichen thalli have been examined. The contribution of the photobiont concerning adaptation mechanisms to the light regime and temperature conditions was examined by chlorophyll a fluorescence and pigment analysis focusing on the foliose lichen Umbilicaria decussata from North Victoria Land, continental Antarctica. No photoinhibition has been observed in the entire lichen thallus. In the isolated photobionts, photoinhibition was clearly temperature dependent. For the first time, melanin in U. decussata thalli has been proved. Though the isolated photobiont is capable of excess light protection, the results clearly show that photoprotection is significantly increased in the symbiotic state. The closely related photobiont of Pleopsidium chlorophanum, a lichen lacking melanin, showed a higher potential of carotenoid-based excess light tolerance. This fact discriminates the two photobionts of the same Trebouxia clade. Based on the results, it can be concluded that the successful adaptation of lichens to continental Antarctic conditions is in part based on the physiological potential of the photobionts. The findings provide information on the success of symbiotic life in extreme environments.

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

Access this article

Log in via an institution

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
Fig. 6

Similar content being viewed by others

Abbreviations

ANOVA:

Analysis of variance

chl f :

Chlorophyll fluorescence

DEPS:

De-epoxidation state of the xanthophyll pool

DMSO:

Dimethyl sulfoxide

GANOVEX:

German Antarctic North Victoria Land Expedition

HPLC:

High-performance liquid chromatography

MY:

Malt–yeast

NPQ:

Non-photochemical quenching

PAM:

Pulse-amplitude modulation

PAR:

Photosynthetically active radiation

PPFD:

Photosynthetically active photon flux density

PS:

Photosystem

ROS:

Reactive oxygen species

SLC:

Secondary lichen compound

TOM:

Trebouxia organic medium

UVR:

Ultraviolet radiation

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, Vráblíková-Cempírková H, Štepigová J, Hájek J, Váczi P, Večeřová K (2008) Duration of irradiation rather than quantity and frequency of high irradiance inhibits photosynthetic processes in the lichen Lasallia pustulata. Photosynthetica 46:161–169

    Article  Google Scholar 

  • Beckett RP, Minibayeva FV, Liers C (2012) Occurrence of high tyrosinase activity in the non-Peltigeralean lichen Dermatocarpon miniatum (L.) W. Mann. Lichenologist 44:827–832

    Article  Google Scholar 

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

  • Büdel B, Lange OL (1994) The role of cortical and epinecral layers in the lichen genus Peltula. Cryptogam Bot 4:262–269

    Google Scholar 

  • Chen J, Blume HP, Beyer L (2000) Weathering of rocks induced by lichen colonization: a review. Catena 39:121–146

    Article  CAS  Google Scholar 

  • Convey P (2010) Terrestrial biodiversity in Antarctica: recent advances and future challenges. Polar Sci 4:135–147

    Article  Google Scholar 

  • Dietz S, Büdel B, Lange OL, Bilger W (2000) Transmittance of light through the cortex of lichens from contrasting habitats. Bibl Lichenol 75:171–182

    Google Scholar 

  • Domaschke S, Vivas M, Sancho LG, Printzen C (2013) Ecophysiology and genetic structure of polar versus temperate populations of the lichen Cetraria aculeata. Oecologia 173:699–709

    Article  PubMed  CAS  Google Scholar 

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

    Article  Google Scholar 

  • Gauslaa Y, Solhaug KA (2004) Photoinhibition in lichens depends on cortical characteristics and hydration. Lichenologist 36:133–144

    Article  Google Scholar 

  • Gauslaa Y, Coxson DS, Solhaug KA (2012) The paradox of higher light tolerance during desiccation in rare old forest cyanolichens than in more widespread co-occurring chloro- and cephalolichens. N Phytol 195:812–822

    Article  Google Scholar 

  • Gjessing Y, Øvstedal O (1989) Microclimate and water budget of alpine algae, lichens and a moss on some Nunataks in Queen Maud Land. Int J Biometeorol 33:272–281

    Article  Google Scholar 

  • Green TGA, Lange OL (1995) Photosynthesis in poikilohydric plants: a comparison of lichens and bryophytes. In: Schulze ED, Caldwell MM (eds) Ecophysiology of photosynthesis. Springer, Berlin, pp 319–341

    Chapter  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 

  • Havaux M, Niyogi KK (1999) The violoxanthin cycle protects from photoxidative damage by more than one mechanism. Proc Natl Acad Sci 96:8762–8767

    Article  PubMed  CAS  PubMed Central  Google Scholar 

  • Heber U (2008) Photoprotection of green plants: a mechanism of ultra-fast thermal energy dissipation in desiccated lichens. Planta 228:641–650

    Article  PubMed  CAS  Google Scholar 

  • 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 

  • Hidalgo ME, Fernández E, Ponce M, Rubio C, Quilhot W (2002) Photophysical, photochemical, and thermodynamic properties of shikimic acid derivatives: calycin and rhizocarpic acid (lichens). J Photochem Photobiol B Biol 66:213–217

    Article  CAS  Google Scholar 

  • Hughes KA, Ott S, Bölter M, Convey P (2006) Colonisation processes. In: Bergstrom DM, Convey P, Huiskes AHL (eds) Trends in Antarctic terrestrial and limnetic ecosystems. Springer, Dordrecht, pp 35–54

    Chapter  Google Scholar 

  • Huiskes AHL, Convey P, Bergstrom DM (2006) Trends in Antarctic and 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 1–13

    Chapter  Google Scholar 

  • Jahns HM, Fritzler E (1982) Flechtenstandorte auf einer Blockhalde. Herzogia 6:243–270

    Google Scholar 

  • Kappen L (1973) Response to extreme environments. In: Ahmadjian V (ed) The lichens. Academic Press, New York and London, pp 311–380

    Chapter  Google Scholar 

  • Kappen L (1985) Water relations and net photosynthesis of Usnea: a comparison between Usnea fasciata (maritime Antarctic) and Usnea sulphurea (continental Antarctic). In: Brown DH (ed) Lichen physiology and cell biology. Plenum Press, New York and London, pp 41–56

    Chapter  Google Scholar 

  • Kappen L (2000) Some aspects of the great success of lichens in Antarctica. Antarct Sci 12:314–324

    Article  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, Schroeter B, Scheidegger C, Sommerkorn M, Hestmark G (1996) Cold resistance and metabolic activity of lichens below 0°C. Adv Space Res 18:119–128

    Article  Google Scholar 

  • Kappen L, Schroeter B, Green TGA, Seppelt RD (1998) Microclimatic conditions, meltwater moistening, and the distributional pattern of Buellia frigida on rock in a southern continental Antarctic habitat. Polar Biol 19:101–106

    Article  Google Scholar 

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

    Article  PubMed  CAS  Google Scholar 

  • Meeßen J, Sánchez FJ, Sadowsky A, de la Torre R, Ott S, de Vera JP (2013) Extremotolerance and resistance of lichens: comparative studies on five species used in astrobiological research II. Secondary lichen compounds. Orig Life Evol Biosph 43:501–526

    Article  PubMed  Google Scholar 

  • Nybakken L, Solhaug KA, Bilger W, Gauslaa Y (2004) The lichens Xanthoria elegans and Cetraria islandica maintain a high protection against UV-B radiation in Arctic habitats. Oecologia 140:211–216

    Article  PubMed  Google Scholar 

  • Onofri S, de la Torre R, de Vera JP, Ott S, Zucconi L, Selbmann L, Scalzi G, Venkateswaran KJ, Rabbow E, Sánchez Iñigo FJ, Horneck G (2012) Survival of rock-colonizing organisms after 1.5 years in outer space. Astrobiology 12:508–516

    Article  PubMed  Google Scholar 

  • Øvstedal DO, Lewis Smith RI (2001) Lichens of Antarctica and South Georgia: a guide to their identification and ecology. Cambridge University Press, Cambridge

    Google Scholar 

  • Robinson SA, Wasley J, Tobin AK (2003) Living on the edge–plants and global change in continental and maritime Antarctica. Glob Change Biol 9:1681–1717

  • 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

  • Sadowsky A, Ott S (2012) Photosynthetic symbionts in Antarctic terrestrial ecosystems: the physiological response of lichen photobionts to drought and cold. Symbiosis 58:81–90

    Article  Google Scholar 

  • Sadowsky A, Hussner A, Ott S (2012) Submersion tolerance in a habitat of Stereocaulon paschale (Stereocaulaceae) and Cladonia stellaris (Cladoniaceae) from the high mountain region Rondane, Norway. Nova Hedwig 94:323–334

    Article  Google Scholar 

  • Sánchez FJ, Meeßen J, Ruiz MG, Sancho LG, Ott S, Vílchez C, Horneck G, Sadowsky A, de la Torre R (2014) UV-C tolerance of symbiotic Trebouxia sp. in the space-tested lichen species Rhizocarpon geographicum and Circinaria gyrosa: role of the hydration state and cortex/screening substances. Int J Astrobiol 13:1–18

    Article  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

  • 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 

  • Schlensog M, Green TGA, Schroeter B (2013) Life form and water source interact to determine active time and environment in cryptogams: an example from the maritime Antarctic. Oecologia 173:59–72

    Article  PubMed  Google Scholar 

  • Schroeter B, Green TGA, Seppelt RD, Kappen L (1992) Monitoring photosynthetic activity of crustose lichens using a PAM-2000 fluorescence system. Oecologia 92:457–462

    Article  Google Scholar 

  • Schroeter B, Green TGA, Pannewitz S, Schlensog M, Sancho LG (2010) Fourteen degrees of latitude and a continent apart: comparison of lichen activity over two years at continental and maritime Antarctic sites. Antarct Sci 22:681–690

    Article  Google Scholar 

  • Schroeter B, Green TGA, Pannewitz S, Schlensog M, Sancho LG (2011) Summer variability, winter dormancy: lichen activity over 3 years at Botany Bay, 77 S latitude, continental Antarctica. Polar Biol 34:13–22

    Article  Google Scholar 

  • Solhaug KA, Gauslaa Y, Nybakken L, Bilger W (2003) UV induction of sun-screening pigments in lichens. New Phytol 158:91–100

    Article  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 

  • Wornik S, Grube M (2010) Joint dispersal does not imply maintenance of partnerships in lichen symbioses. Microb Ecol 59:150–157

    Article  PubMed  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. Springer, Berlin, pp 3–33

    Chapter  Google Scholar 

Download references

Acknowledgments

Special thanks to Eva Posthoff for her substantial help with the photobiont cultures. Thanks are also due to the organization committee of the XIth SCAR Biology Symposium 2013, Barcelona. The first author thanks the Studienstiftung des Deutschen Volkes for financial support. The second author is grateful to the German Research Foundation (DFG) for financing the research project Ot 96/15–1 as part of the Antarctic Priority Program (SPP 1158). 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. 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

  1. Institute of Botany, Heinrich Heine University, Universitaetsstrasse 1, 40225, Duesseldorf, Germany

    Andres Sadowsky & Sieglinde Ott

Authors
  1. Andres Sadowsky
    View author publications

    You can also search for this author in PubMed Google Scholar

  2. Sieglinde Ott
    View author publications

    You can also search for this author in PubMed Google Scholar

Corresponding author

Correspondence to Sieglinde Ott.

Additional information

This article is an invited contribution on Life in Antarctica: Boundaries and Gradients in a Changing Environment as the main theme of the XIth SCAR Biology Symposium.

Rights and permissions

Reprints and permissions

About this article

Check for updates. Verify currency and authenticity via CrossMark

Cite this article

Sadowsky, A., Ott, S. Symbiosis as a successful strategy in continental Antarctica: performance and protection of Trebouxia photosystem II in relation to lichen pigmentation. Polar Biol 39, 139–151 (2016). https://doi.org/10.1007/s00300-015-1677-0

Download citation

  • Received:

  • Revised:

  • Accepted:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1007/s00300-015-1677-0

Keywords

Search

Navigation