, Volume 173, Issue 3, pp 699–709 | Cite as

Ecophysiology and genetic structure of polar versus temperate populations of the lichen Cetraria aculeata

  • S. DomaschkeEmail author
  • M. Vivas
  • L. G. Sancho
  • C. Printzen
Physiological ecology - Original research


We studied polar and temperate samples of the lichen Cetraria aculeata to investigate whether genetical differences between photobionts are correlated with physiological properties of the lichen holobiont. Net photosynthesis and dark respiration (DR) at different temperatures (from 0 to 30 °C) and photon flux densities (from 0 to 1,200 μmol m−2 s−1) were studied for four populations of Cetraria aculeata. Samples were collected from maritime Antarctica, Svalbard, Germany and Spain, representing different climatic situations. Sequencing of the photobiont showed that the investigated samples fall in the polar and temperate clade described in Fernández-Mendoza et al. (Mol Ecol 20:1208–1232, 2011). Lichens with photobionts from these clades differ in their temperature optimum for photosynthesis, maximal net photosynthesis, maximal DR and chlorophyll content. Maximal net photosynthesis was much lower in Antarctica and Svalbard than in Germany and Spain. The difference was smaller when rates were expressed by chlorophyll content. The same is true for the temperature optima of polar (11 °C) and temperate (15 and 17 °C) lichens. Our results indicate that lichen mycobionts may adapt or acclimate to local environmental conditions either by selecting algae from regional pools or by regulating algal cell numbers (chlorophyll content) within the thallus.


Photosynthesis Lichens Cetrariaaculeata Trebouxiajamesii Acclimation Genetic adaptation 



The staff of the Grunelius-Möllgaard-lab, especially Heike Kappes, and Selina Becker, Jasmin Seifried (Frankfurt) and Bastian Millgramm (Kassel) are thanked for technical support in the lab, Prof. Dr. Claudia Büchel and Markus Fauth for their help with chlorophyll measurements, Markus Bingmer for statistical support and Toby Spribille (Graz), Viktoria Wagner (Halle) and Sergio Pérez-Ortega (Madrid) for population samples of C. aculeata. Funding by the German Research Foundation (DFG) grant Pr 567/10-1 and Pr 567/12-1, the European Union through Synthesys grant ES-TAF 3621 to C.P., the Marga und Kurt Möllgaard-Stiftung and the Spanish Ministerio de Ciencia e Innovación (grant CTM2009-12838-C04-01 and FPI grant BES-2007-17323 to M.V.) are gratefully acknowledged. The present study was also financially supported by the research funding programme “LOEWE —Landes-Offensive zur Entwicklung Wissenschaftlich-ökonomischer Exzellenz” of Hesse’s Ministry of Higher Education, Research, and the Arts.

Supplementary material

442_2013_2670_MOESM1_ESM.pdf (263 kb)
Supplementary material 1 (PDF 262 kb)


  1. Baker AC, Starger CJ, McClanahan TR, Glynn PW (2004) Coral’s adaptive response to climate change. Nature 430:741PubMedCrossRefGoogle Scholar
  2. Barnes JD, Balaguer L, Manrique E, Elvira S, Davison AW (1992) A reappraisal of the use of DMSO for the extraction and determination of the chlorophylls a and b in lichens and higher plants. Environ Exp Bot 32:85–100CrossRefGoogle Scholar
  3. Beneragama CK, Goto K (2010) Chlorophyll a:b ratio under low-light in “shade-tolerant” Euglena gracilis. Trop Agric Res 22:12–25Google Scholar
  4. Blaha J, Baloch E, Grube M (2006) High photobiont diversity in symbioses of the euryoecious lichen Lecanora rupicola (Lecanoraceae, Ascomycota). Biol J Linn Soc 88:283–293CrossRefGoogle Scholar
  5. Cardinale M, Steinová J, Rabensteiner J, Berg G, Grube M (2012) Age, sun and substrate: triggers of bacterial communities in lichens. Environ Microbiol Rep 4:23–28PubMedCrossRefGoogle Scholar
  6. Casano LM, del Campo EM, Garcia-Breijo FJ, Reig-Arminana J, Gasulla F, del Hoyo A, Guera A, Barreno E (2011) Two Trebouxia algae with different physiological performances are ever-present in lichen thalli of Ramalina farinacea. Coexistence versus competition? Environ Microbiol 13:806–818PubMedCrossRefGoogle Scholar
  7. Clement M, Posada D, Crandall KA (2000) TCS: a computer program to estimate gene genealogies. Mol Ecol 9:1657–1660PubMedCrossRefGoogle Scholar
  8. Dale MP, Causton DR (1992) Use of the chlorophyll a/b ratio as a bioassay for the light environment of a plant. Funct Ecol 6:190–196CrossRefGoogle Scholar
  9. del Hoyo A, Álvarez R, del Campo EM, Gasulla F, Barreno E, Casano LM (2011) Oxidative stress induces distinct physiological responses in the two Trebouxia phycobionts of the lichen Ramalina farinacea. Ann Bot 107:109–118PubMedCrossRefGoogle Scholar
  10. Del Prado R, Sancho LG (2000) Water relations and photosynthetic performance of fruticose lichens from semiarid Southeast of Spain. Flora 195:51–60Google Scholar
  11. Drummond AJ, Ashton B, Buxton S, Cheung M, Cooper A, Duran C, Field M, Heled J, Kearse M, Markowitz S, Moir R, Stones-Havas S, Sturrock S, Thierer T, Wilson A (2009) Geneious v4.7. Available from
  12. Fernández-Mendoza F, Domaschke S, García MA, Jordan P, Martín MP, Printzen C (2011) Population structure of mycobionts and photobionts of the widespread lichen Cetraria aculeata. Mol Ecol 20:1208–1232PubMedCrossRefGoogle Scholar
  13. Friedmann EI, Sun HJ (2005) Communities adjust their temperature optima by shifting producer-to-consumer ratio, shown in lichens as models: I. Hypothesis. Microb Ecol 49:523–527PubMedCrossRefGoogle Scholar
  14. Gardes M, Bruns TD (1993) ITS primers with enhanced specificity for basidiomycetes—application to the identification of mycorrhizae and rusts. Mol Ecol 2:113–118Google Scholar
  15. Gasulla F, Guéra A, Barreno E (2010) A simple and rapid method for isolating lichen photobionts. Symbiosis 51:175–179CrossRefGoogle Scholar
  16. Gilbert SF, McDonald E, Boyle N, Buttino N, Gyi L, Mai M, Prakash N, Robinson J (2010) Symbiosis as a source of selectable epigenetic variation: taking the heat for the big guy. Philos Trans R Soc Lond B 365:671–678CrossRefGoogle Scholar
  17. Green TGA (2009) Lichens in arctic, Antarctic and alpine ecosystems. In: Claudia Deigele: Rundgespräche der Komission für Ökologie, Bd. 36 „Ökologische Rolle der Flechten“, Verlag Dr. Friedrich Pfeil, München, pp 45–65Google Scholar
  18. Green TGA, Büdel B, Meyer A, Zellner H, Lange OL (1997) Temperate rainforest lichens in New Zealand: light response of photosynthesis. NZ J Bot 35:493–504CrossRefGoogle Scholar
  19. Green TGA, Nash TH III, Lange OL (2008) Physiological ecology of carbon dioxide exchange. In: Nash TH III (ed) Lichen biology, 2nd edn. Cambridge University Press, Cambridge, pp 152–181Google Scholar
  20. Harper AL, von Gesjen SE, Linford AS, Peterson MP, Faircloth RS, Thissen MM, Brusslan JA (2004) Chlorophyllide a oxygenase mRNA and protein levels correlate with the chlorophyll a/b ratio in Arabidopsis thaliana. Photosynth Res 79:149–159PubMedCrossRefGoogle Scholar
  21. Henskens FL, Green TGA, Wilkins A (2012) Cyanolichens can have both cyanobacteria and green algae in a common layer as major contributors to photosynthesis. Ann Bot 110:555–563PubMedCrossRefGoogle Scholar
  22. Hodkinson BP, Gottel NR, Schadt CW, Lutzoni F (2012) Photoautotrophic symbiont and geography are major factors affecting highly structured and diverse bacterial communities in the lichen microbiome. Environ Microbiol 14:147–161PubMedCrossRefGoogle Scholar
  23. Humbeck K, Hoffmann B, Senger H (1988) Influence of energy flux and quality of light on the molecular organization of the photosynthetic apparatus in Scenedesmus. Planta 173:205–212CrossRefGoogle Scholar
  24. Johansson O, Olofsson J, Giesler R, Palmqvist K (2011) Lichen responses to nitrogen and phosphorus additions can be explained by the different symbiont responses. New Phytol 191:795–805PubMedCrossRefGoogle Scholar
  25. Johnson GN, Scholes JD, Horton P, Young AJ (1993) Relationships between carotenoid composition and growth habitat in British plant species. Plant Cell Environ 16:681–686CrossRefGoogle Scholar
  26. Jones AM, Berkelmans R, van Oppen MJH, Mieog JC, Sinclair W (2008) A community change in the algal endosymbionts of a scleractinian coral following a natural bleaching event: field evidence of acclimatization. Proc R Soc Lond B 275:1359–1365CrossRefGoogle Scholar
  27. Kärenlampi L, Pelkonen M (1971) Studies on the morphological variation of the lichen Cladonia uncialis. Rep Kevo Subarct Res Stn 7:1–8Google Scholar
  28. Kershaw KA (1985) Physiological ecology of lichens. Cambridge University Press, CambridgeGoogle Scholar
  29. Körner C, Larcher W (1988) Plant life in cold climates. In: Long SP, Woodward FI (eds) Plants and temperature. The Company of Biologista, Cambridge, pp 25–57Google Scholar
  30. Kroken S, Taylor JW (2000) Phylogenetic species, reproductive mode and specificity of the green alga Trebouxia forming lichens with the fungal genus Letharia. Bryologist 103:645–660CrossRefGoogle Scholar
  31. Kunkel G (1980) Microhabitat and structural variation in the Aspicilia desertorum group (lichenized ascomycetes). Am J Bot 67:1137–1144CrossRefGoogle Scholar
  32. Lange OL, Green TGA (2005) Lichens show that fungi can acclimate their respiration to seasonal changes in temperature. Oecologia 142:11–19PubMedCrossRefGoogle Scholar
  33. Lange OL, Meyer A, Ullmann I, Zellner H (1991) Mikroklima, Wassergehalt und Photosynthese von Flechten in der küstennahen Nebelzone der Namib-Wüste: Messungen während der herbstlichen Witterungsperiode. Flora 185:233–266Google Scholar
  34. Larcher W, Vareschi V (1988) Variation in morphology and functional traits of Dictyonema glabratum from contrasting habitats in the Venezuelan Andes. Lichenologist 20:269–277CrossRefGoogle Scholar
  35. Larson DW (1978) Patterns of lichen photosynthesis and respiration following prolonged frozen storage. Can J Bot, 56:2119–2123Google Scholar
  36. Lechowicz MJ (1982) Ecological trends in lichen photosynthesis. Oecologia 53:330–336CrossRefGoogle Scholar
  37. Lechowicz MJ, Hellens LE, Simon J-P (1980) Latitudinal trends in the responses of growth respiration and maintenance respiration to temperature in the beach pea, Lathyrus japonicus. Can J Bot 52:1521–1524Google Scholar
  38. Lücking R, Lawrey JD, Sikaroodi M, Gillevet PM, Chaves JL, Sipman HJM, Bungartz F (2009) Do lichens domesticate photobionts like farmers domesticate crops? evidence from a previously unrecognized lineage of filamentous cyanobacteria. Am J Bot 96:1409–1418PubMedCrossRefGoogle Scholar
  39. Meyer MA, Huang GH, Morris GJ, Friedmann EI (1988) The effect of low temperatures on Antarctic endolithic green algae. Polarforsch 58:113–119Google Scholar
  40. Morita RY (1975) Psychrophilic bacteria. Bact Rev 39:144–167PubMedGoogle Scholar
  41. Muggia L, Grube M, Tretiach M (2008) Genetic diversity and photobiont associations in selected taxa of the Tephromela atra group (Lecanorales, lichenised Ascomycota). Mycol Prog 7:147–160CrossRefGoogle Scholar
  42. Murtagh GJ, Dyer PS, Furneaux PA, Crittenden PD (2002) Molecular and physiological diversity in the bipolar lichen-forming fungus Xanthoria elegans. Mol Res 106:1277–1286Google Scholar
  43. Opanowicz M, Grube M (2004) Photobiont genetic variation in Flavocetraria nivalis from Poland (Parmeliaceae, lichenized Ascomycota). Lichenologist 36:125–131CrossRefGoogle Scholar
  44. Palmqvist K (2000) Carbon economy in lichens. New Phytol 148:11–36CrossRefGoogle Scholar
  45. Palmqvist K, Dahlman L, Valladares F, Tehler A, Sancho LG, Mattson J-E (2002) CO2 exchange and thallus nitrogen across 75 contrasting lichen associations from different climatic zones. Oecologia 133:295–306CrossRefGoogle Scholar
  46. Peksa O, Škaloud P (2011) Do photobionts influence the ecology of lichens? A case study of environmental preferences in symbiotic green alga Asterochloris (Trebouxiophyceae). Mol Ecol 20:3936–3948PubMedCrossRefGoogle Scholar
  47. Piercey-Normore MD (2005) The lichen-forming ascomycete Evernia mesomorpha associates with multiple genotypes of Trebouxia jamesii. New Phytol 169:331–344CrossRefGoogle Scholar
  48. Piercey-Normore MD, Deduke C (2011) Fungal farmers or algal escorts: lichen adaptation from the algal perspective. Mol Ecol 20:3708–3710PubMedCrossRefGoogle Scholar
  49. Pigliucci M (2001) Phenotypic plasticity: beyond nature and nurture. John Hopkins University Press, BaltimoreGoogle Scholar
  50. Printzen C, Fernández-Mendoza F, Muggia L, Berg G, Grube M (2012) Alphaproteobacterial communities in geographically distant populations of the lichen Cetraria aculeata. FEMS Microbiol Ecol 82:316–325PubMedCrossRefGoogle Scholar
  51. Quispel A (1960) Respiration of lichens. In: Wolf J (ed) Pflanzenatmung einschliesslich Gärung und Säurestoffwechsel Handbuch der Pflanzenphysiologie, vol XII/2. Springer, Berlin, pp 455–460Google Scholar
  52. R Development Core Team (2009) R: A language and environment for statistical computing. R Foundation for Statistical Computing, Vienna, Austria. ISBN 3-900051-07-0, URL
  53. Reiter R, Höftberger M, Green TGA, Türk R (2008) Photosynthesis of lichens from lichen-dominated communities in the alpine/nival belt of the Alps: II. Laboratory and field measurements of CO2 exchange and water relations. Flora 203:34–46CrossRefGoogle Scholar
  54. Robinson CH (2001) Cold adaptation in Arctic and Antarctic fungi. New Phytol 151:341–353CrossRefGoogle Scholar
  55. Rodriguez RJ, Henson J, Van Volkenburgh E, Hoy M, Wright L, Beckwith F, Kim Y-O, Redman RS (2008) Stress tolerance in plants via habitat-adapted symbiosis. ISME J 2:404–416PubMedCrossRefGoogle Scholar
  56. Sancho LG, Schroeter B, Valladares F (1997) Photosynthetic performance of two closely related Umbilicaria species in central Spain: temperature as a key factor. Lichenologist 29:67–82Google Scholar
  57. Sancho LG, Valladres F, Schroeter B, Kappen L (2000) Ecophysiology of Antarctic versus temperate populations of bipolar lichens: the key role of photosynthetic partner. In: Howard-Williams C, Davison B (eds) Antarctic ecosystems: models for wider ecological understanding. Natural Science, Christchurch, pp 190–194Google Scholar
  58. Schipperges B, Kappen L, Sonesson M (1995) Intraspecific variations of morphology and physiology of temperate to arctic populations of Cetraria nivalis. Lichenol 27:517–529Google Scholar
  59. Sonesson M, Schipperges B, Carlsson BÅ (1992) Seasonal patterns of photosynthesis in alpine and subalpine populations of the lichen Nephroma arcticum. Oikos 65:3–12CrossRefGoogle Scholar
  60. Sun HJ, Friedmann EI (2005) Communities adjust their temperature optima by shifting producer-to-consumer ratio, shown in lichens as models: II. Experimental verification. Microb Ecol 49:528–535PubMedCrossRefGoogle Scholar
  61. Sundberg B, Ekblad A, Näsholm T, Palmqvist K (1999) Lichen respiration in relation to active time, temperature, nitrogen and ergosterol concentrations. Funct Ecol 13:119–125CrossRefGoogle Scholar
  62. Vrábliková H, McEvoy M, Solhaug KA, Barták M, Gauslaa Y (2006) Annual variation in photo acclimation and photoprotection of the photobiont in the foliose lichen Xanthoria parietina. J Photochem Photobiol 83:151–162CrossRefGoogle Scholar
  63. Werth S, Sork VL (2010) Identity and genetic structure of the photobiont of the epiphytic lichen Ramalina menziesii on three oak species in southern California. Am J Bot 95:821–830CrossRefGoogle Scholar
  64. Yahr R, Vilgalys R, DePriest PT (2006) Geographic variation in algal partners of Cladonia subtenuis (Cladoniaceae) highlights the dynamic nature of a lichen symbiosis. New Phytol 171:847–860PubMedCrossRefGoogle Scholar
  65. Zilber-Rosenberg I, Rosenberg E (2008) Role of microorganisms in the evolution of animals and plants: the hologenome theory of evolution. FEMS Microbiol Rev 32:723–735PubMedCrossRefGoogle Scholar

Copyright information

© Springer-Verlag Berlin Heidelberg 2013

Authors and Affiliations

  • S. Domaschke
    • 1
    • 3
    Email author
  • M. Vivas
    • 2
  • L. G. Sancho
    • 2
  • C. Printzen
    • 1
    • 3
  1. 1.Department of Botany and Molecular EvolutionSenckenberg Research InstituteFrankfurt am MainGermany
  2. 2.Biología Vegetal II, Fac. de FarmaciaUniversidad ComplutenseMadridSpain
  3. 3.Biodiversity and Climate Research CenterFrankfurt am MainGermany

Personalised recommendations