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Morphological and phylogenetic study of algal partners associated with the lichen-forming fungus Tephromela atra from the Mediterranean region

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Abstract

Recent DNA sequence analyses have revealed the diversity of algal partners in lichen symbioses. Although morphologically similar, different genetic lineages of photobionts are detected in wide geographic ranges of the same lichen fungal species. We studied the photobiont of the genus Trebouxia, which are known as partners of diverse lichen-forming fungal species in the Mediterranean region. We studied the phylogeny of these algae with a multilocus dataset including three loci: ITS, rbcL, and actin type I gene. The two lineages found, informally named Trebouxia sp. 1 and Trebouxia sp. 2, are related to Trebouxia arboricola/decolorans. The cultivation under axenic conditions succeeded only for one of them so far. We used light microscopy, confocal laser scanning microscopy and transmission electron microscopy for phenotypic characterisation. The ultrastructural characters currently used to describe species in the genus do not support the segregation of Trebouxia sp.1 from Trebouxia arboricola. The preferential presence in Mediterranean climates of these strains suggests eco-physiological adaptation. Despite their asexuality in long living lichen symbioses, coccoid algal lichen partners have apparently diversified genetically and physiologically.

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References

  • Ahmadjian V (1967) The lichen symbiosis. Blaisdell Publishing Company, Massachusetts

    Google Scholar 

  • Ahmadjian V (1995) Lichens are more important than you think. Bioscience 45:123–124

    Google Scholar 

  • Ascaso C, Valladares F, De Los Rios A (1995) New ultrastructural aspects of pyrenoids of the lichen photobiont Trebouxia (Microthamniale, Chlorophyta). J Phycol 31:114–119

    Article  Google Scholar 

  • Beck A, Friedl T, Rambold G (1998) Selectivity of photobiont choice in a defined lichen community: inferences from cultural and molecular studies. New Phytol 139:709–720

    Article  CAS  Google Scholar 

  • Beck A, Kasalicky T, Rambold G (2002) Myco-photobiontal selection in a Mediterranean cryptogam community with Fulgensia fulgida. New Phytol 153:317–326

    Article  Google Scholar 

  • Blaha J, Baloch E, Grube M (2006) High photobiont diversity associated with the euryoecious lichen-forming ascomycete Lecanora. Biol J Linn Soc 88:283–293

    Article  Google Scholar 

  • Casano L, Gasulla F, del Campo E, Guera A, Zapata JM, Esteban A, del Hoyo A, Barreno E (2009) Ramalina farinacea specifically associates with three different Trebouxia algae, regardless of habitat and geographical location: physiological characterization of the photobionts. Notiziario della Società Lichenologica Italiana 22:24

    Google Scholar 

  • Cordeiro LMC, Reis RA, Cruz LM, Stocker-Wörgötter E, Grube M, Iacomini M (2005) Molecular studies of photobionts of selected lichens from coastal vegetation of Brazil. FEMS Microbiol Immunol 54:381–390

    CAS  Google Scholar 

  • Cubero OF, Crespo A, Fatehi J, Bridge PD (1999) DNA extraction and PCR amplification method suitable for fresh, herbarium stored and lichenized fungi. Plant Syst Evol 217:243–249

    Article  Google Scholar 

  • Doering M, Piercey-Normore MD (2009) Genetically divergent algae shape an epiphytic lichen community on Jack Pine in Manitoba. Lichenologist 41:69–80

    Article  Google Scholar 

  • Ettl H, Gärtner G (1984) Über die Bedeutung der Cytologie für die Algentaxonomie, dargestellt an Trebouxia (Chlorellales, Chlorophyceae). Plant Syst Evol 148:135–147

    Article  Google Scholar 

  • Felsenstein J (1985) Confidence limits on phylogenies: an approach using the bootstrap. Evolution 39:783–791

    Article  Google Scholar 

  • Feuerer T, Hawksworth DL (2007) Biodiversity of lichens, including a world-wide analysis of checklist data based on Takhtajan’s floristic regions. Biodivers Conserv 16:85–98

    Article  Google Scholar 

  • Friedl T (1989) Comparative ultrastructure of pyrenoids in Trebouxia (Microthamniales, Chlorophyta). Plant Syst Evol 164:145–159

    Article  Google Scholar 

  • Friedl T (1993) New aspects of the reproduction by autospores in the lichen alga Trebouxia (Microthamniales, Chlorophyta). Arch Protistenk 143:153–161

    Google Scholar 

  • Gärtner G (1985) Die Gattung Trebouxia Puymaly (Chlorellales, Chlorophyceae). Archiv fur Hydrobiologie, Supplement. Algol Stud 41:495–548

    Google Scholar 

  • Guzow-Krzemińska B (2006) Photobiont flexibility in the lichen Protoparmeliopsis muralis as revealed by ITS rDNA analysis. Lichenologist 38:469–476

    Article  Google Scholar 

  • Hall TA (1999) BioEdit: a user friendly biological sequence alignment editor and analysis program for Windows 95/98/NT. Nucl Acids Symp Ser 41:95–98

    CAS  Google Scholar 

  • Helms G (2003) Taxonomy and symbiosis in association of Physiaceae and Trebouxia. Dissertation zur Erlangung des Doktorandes der Biologischen Fakultät der Georg-August Universität Göttingen

  • 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, Kutasi V, Ruffner HP (1993) Polyol patterns in eleven species of aposymbiotically cultured lichen mycobionts. Mycol Res 97:35–39

    Article  CAS  Google Scholar 

  • Huelsenbeck JP, Ronquist F (2003) MRBAYES 3: Bayesian phylogenetic inference under mixed models. Bioinformatics 19:1572–1574

    Article  PubMed  Google Scholar 

  • Kroken S, Taylor JW (2000) Phylogenetic species, reproductive mode, and specificity of the green alga Trebouxia forming lichens with the fungal genus Letharia. Bryologist 103:645–660

    Article  CAS  Google Scholar 

  • Muggia L, Grube M, Tretiach M (2008a) A combined molecular and morphological approach to species delimitation in black-fruited, endolithic Caloplaca: high genetic and low morphological diversity. Mycol Res 112:36–49

    Article  Google Scholar 

  • Muggia L, Grube M, Tretiach M (2008b) Genetic diversity and photobiont association in selected taxa of the Tephromela atra group (Lecanorales, lichenized Ascomycota). Mycol Prog 7:147–160

    Article  Google Scholar 

  • Nozaki H, Ito M, Sano R, Uchida H, Watanabe MM, Kuroiwa T (1995) Phylogenetic relationships within the colonial Volvocales (Chlorophyta) inferred from rbcL gene sequence data. J Phycol 31:970–979

    Article  CAS  Google Scholar 

  • Nyati S (2006) Phototbiont diversity in Teloschistaceae (Lecanoromycetes). Dissertation zur Erlangung der naturwissenschaftlichen Doktorwürde, vorgelegt der Mathematisch-naturwissenschaftlichen Fakultät der Universität Zürich

  • Nyquist H (2002) Certain topics in telegraph transmission theory. Proceeding of the Idee 90:280–305

    Article  Google Scholar 

  • Piercey-Normore MD (2006) The lichen-forming ascomycete Evernia mesomorpha associates with multiple genotypes of Trebouxia jamesii. New Phytol 169:331–344

    Article  CAS  PubMed  Google Scholar 

  • Posada D, Crandall KA (1998) Modeltest—testing the model of DNA substitution. Bioinformatics 14:817–818

    Article  CAS  PubMed  Google Scholar 

  • Rambold G, Triebel D (1992) The inter-lecanoralean associations. Bibliotheca Lichenologica, 48, J. Cramer, Berlin, Stuttgart. 201 pp

  • Rodriguez F, Oliver JL, Marin A, Medina JR (1990) The general stochastic model of nucleotide substitution. J Theor Biol 142:485–501

    Article  CAS  PubMed  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

    CAS  PubMed  Google Scholar 

  • Stocker-Wörgötter E (2002) Investigating the production of secondary compounds in cultured lichen mycobionts. In: Kanner I, Beckett RP, Varma AK (eds) Protocol in lichenology, culturing biochemistry, ecophysiology and use in biomonitoring. Springer, Berlin, pp 296–306

    Google Scholar 

  • Swofford DL (2002) PAUP*, Phylogenetic Analysis Using Parsimony (and other methods), Version 4.01b, Illinois Natural History Survey, Champaign, Illinois

  • Tschermak-Woess E (1988) The algal partner. In: Galun M (ed) Handbook of Lichenology, Volume I. CRC, Boca Raton, pp 39–91

    Google Scholar 

  • Tschermak-Woess E (1989) Developmental studies in trebouxioid algae and taxonomical consequences. Plant Syst Evol 164:161–195

    Article  Google Scholar 

  • Yamamoto Y, Kinoshita Y, Yoshimura I (2002) Culture of thallus fragments and re-differentiation of lichens. In: Kanner I, Beckett RP, Varma AK (eds) Protocol in lichenology, culturing biochemistry, ecophysiology and use in biomonitoring. Springer, Berlin, pp 34–46

    Google Scholar 

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Acknowledgments

We acknowledge Andreas Beck and Ondrej Peska for sending algal material, Gerhard Graggaber and Theodora Kopun are thanked for technical help.

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Correspondence to Lucia Muggia.

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Muggia, L., Zellnig, G., Rabensteiner, J. et al. Morphological and phylogenetic study of algal partners associated with the lichen-forming fungus Tephromela atra from the Mediterranean region. Symbiosis 51, 149–160 (2010). https://doi.org/10.1007/s13199-010-0060-8

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  • DOI: https://doi.org/10.1007/s13199-010-0060-8

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