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Molecular and morphological diversity in photobionts associated with Micarea s. str. (Lecanorales, Ascomycota)

  • Rebecca Yahr (a1), Anna Florence (a1), Pavel Škaloud (a2) and Anna Voytsekhovich (a3)


Lichenization is a symbiotic ecological strategy that is widely distributed among the fungi, but in which the diversity of partners is relatively poorly known. Limited morphological diversity has hindered the recognition of true diversity in many lichen fungi, and also in their algal partners. In the temperate and boreal zones, the crustose microlichens are the most speciose but arguably the least studied, particularly in terms of their photobiont partners. In this study, we sampled eight species of Micarea s. str. collected from Europe, culturing and sequencing their green-algal partners using chloroplast (rbcL) and nuclear ribosomal (nucSSU) markers. All specimens collected in Great Britain were associated with members of Coccomyxa (including Pseudococcomyxa), but in the smaller sample of Ukrainian material, both Coccomyxa and Elliptochloris were found. This study extends the known range of fungal hosts for symbionts in the genus Coccomyxa, and supports earlier findings that a separate lineage of predominantly non-symbiotic Coccomyxa exists.



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Ahmadjian, V. (1967) The Lichen Symbiosis. New York: John Wiley & Sons.
Andersen, H. L. & Ekman, S. (2005) Disintegration of the Micareaceae (lichenized Ascomycota): a molecular phylogeny based on mitochondrial rDNA sequences. Mycological Research 109: 2130.
Arnold, A. E., Miądlikowska, J., Higgins, K. L., Sarvate, S. D., Gugger, P., Way, A., Hofstetter, V., Kauff, F. & Lutzoni, F. (2009) A phylogenetic estimation of trophic transition networks for Ascomycetous fungi: are lichens cradles of symbiotrophic fungal diversification? Systematic Biology 58: 283297.
Beck, A. (1999) Photobiont inventory of a lichen community growing on heavy-metal-rich rock. Lichenologist 31: 501510.
Beck, A., Friedl, T. & Rambold, G. (1998) Selectivity of photobiont choice in a defined lichen community: inferences from cultural and molecular studies. New Phytologist 139: 709720.
Brunner, U. (1985) Ultrustructurelle und chemische Zellwanduntersuchungen an Flechten-phycobionten aus 7 Gattungen der Chlorophyceae (Chlorophytina) unter besonderer Berücksichtigung sporopollenin-ähnlicher Biopolymere. Doctoral dissertation, University of Zurich.
Casano, L. M., del Campo, E. M., Garcia-Breijo, F. J., 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? Environmental Microbiology 13: 806818.
Coppins, B. J. (1983) A taxonomic study of the lichen genus Micarea in Europe. Bulletin of the British Museum (Natural History) 11: 18214.
Czarnota, P. (2007) The lichen genus Micarea (Lecanorales, Ascomycota) in Poland. Polish Botanical Studies 23: 1199.
Darienko, T., Gustavs, L., Mudimu, O., Menendez, C. R., Schumann, R., Karsten, U., Friedl, T. & Pröschold, T. (2010) Chloroidium, a common terrestrial coccoid green alga previously assigned to Chlorella (Trebouxiophyceae, Chlorophyta). European Journal of Phycology 45: 7995.
Darienko, T., Gustavs, L., Eggert, A., Wolf, W. & Pröschold, T. (2015) Evaluating the species boundaries of green microalgae (Coccomyxa, Trebouxiophyceae, Chlorophyta) using integrative taxonomy and DNA barcoding with further implications for the species identification in environmental samples. PLoS One 10: e0127838.
Darriba, D., Taboada, G. L., Doallo, R. & Posada, D. (2012) jModelTest 2: more models, new heuristics and parallel computing. Nature Methods 9: 772.
del Campo, E. M., Catala, S., Gimeno, J., del Hoyo, A., Martinez-Alberola, F., Casano, L. M., Grube, M. & Barreno, E. (2013) The genetic structure of the cosmopolitan three-partner lichen Ramalina farinacea evidences the concerted diversification of symbionts. FEMS Microbiology Ecology 83: 310323.
Ekman, S. & Svensson, M. (2014) Brianaria (Psoraceae), a new genus to accommodate the Micarea sylvicola group. Lichenologist 46: 285294.
Eliáš, M., Neustupa, J. & Škaloud, P. (2008) Elliptochloris bilobata var. corticola var. nov. (Trebouxiophyceae, Chlorophyta), a novel subaerial coccal green alga. Biologia 63: 791798.
Ettl, H. & Gärtner, G. (1995) Syllabus der Boden-, Luft-, und Flechtenalgen . Stuttgart, Jena, New York: Gustav Fischer.
Fernández-Martínez, M. A., de los Ríos, A., Sancho, L. G. & Pérez-Ortega, S. (2013) Diversity of endosymbiotic Nostoc in Gunnera magellanica (L) from Tierra del Fuego, Chile. Microbial Ecology 66: 335350.
Fernández-Mendoza, F., Domaschke, S., García, M. A., Jordan, P., Martín, M. P. & Printzen, C. (2011) Population structure of mycobionts and photobionts of the widespread lichen Cetraria aculeata . Molecular Ecology 20: 12081232.
Grube, M. & Kroken, S. (2000) Molecular approaches and the concept of species and species complexes in lichenized fungi. Mycological Research 104: 12841294.
Hafellner, J. (2004) Notes on Scoliciosporum . Fritschiana 49: 2941.
Honegger, R. (1999) Long-term in vitro preservation of the symbiotic phenotype of lichen-forming fungi and their photobionts: the impact of different modes of storage on their viability. In Abstracts of the International Conference on Lichen Conservation Biology (Licons), 30 August–3 September, 1999, Birmensdorf, Switzerland, p. 19.
Honegger, R. (2008) Morphogenesis. In Lichen Biology, 2nd Edition (T. H. Nash III, ed.): 6993. Cambridge: Cambridge University Press.
Huelsenbeck, J. P. & Ronquist, F. (2001) MRBAYES: Bayesian inference of phylogeny. Bioinformatics 17: 754755.
Kroken, S. & Taylor, J. W. (2000) Phylogenetic species, reproductive mode, and specificity of the green alga Trebouxia forming lichens with the fungal genus Letharia . Bryologist 103: 645660.
Kroken, S. & Taylor, J. W. (2001) A gene geneological approach to determine phylogenetic species boundaries in the lichenized fungus Letharia . Mycologia 93: 3853.
Leavitt, S. D., Esslinger, T. L., Divakar, P. K. & Lumbsch, H. T. (2012) Miocene divergence, phenotypically cryptic lineages, and contrasting distribution patterns in common lichen-forming fungi (Ascomycota: Parmeliaceae). Biological Journal of the Linnean Society 107: 920937.
Leavitt, S. D., Nelsen, M. P., Lumbsch, H. T., Johnson, L. A. & St. Clair, L. L. (2013) Symbiont flexibility in subalpine rock shield lichen communities in the Southwestern USA. Bryologist 116: 149161.
Leliaert, F., Smith, D. R., Moreau, H., Herron, M. D., Verbruggen, H., Delwiche, C. F. & De Clerck, O. (2012) Phylogeny and molecular evolution of the green algae. Critical Reviews in Plant Sciences 31: 146.
Letsch, M. R. & Lewis, L. A. (2012) Chloroplast gene arrangement variation within a closely related group of green algae (Trebouxiophyceae, Chlorophyta). Molecular Phylogenetics and Evolution 64: 524532.
Letsch, M. R., Muller-Parker, G., Friedl, T. & Lewis, L. (2009) Elliptochloris marina sp. nov. (Trebouxiophyceae, Chlorophyta), symbiotic green alga of the temperate Pacific sea anemones Anthopleura xanthogrammica and A. elegantissima (Anthozoa, Cnidaria). Journal of Phycology 45: 11271135.
Lücking, R., Dal-Forno, M., Sikaroodi, M., Gillevet, P. M., Bungartz, F., Moncada, B., Yánez-Ayabaca, A., Chaves, J. L., Coca, L. F. & Lawrey, J. D. (2014) A single macrolichen constitutes hundreds of unrecognized species. Proceedings of the National Academy of Sciences of the United States of America 111: 1109111096.
Maddison, W. P. & Maddison, D. R. (2011) Mesquite: a modular system for evolutionary analysis. Version 2.75.
Mansournia, M. R., Wu, B., Matsushita, N. & Hogetsu, T. (2012) Genotypic analysis of the foliose lichen Parmotrema tinctorum using microsatellite markers: association of mycobiont and photobiont, and their reproductive modes. Lichenologist 44: 419440.
Mueller, U. G. (2012) Symbiont recruitment versus ant-symbiont co-evolution in the attine ant-microbe symbiosis. Current Opinion in Microbiology 15: 269277.
Muggia, L., Baloch, E., Stabentheiner, E., Grube, M. & Wedin, M. (2010) Photobiont association and genetic diversity of the optionally lichenized fungus Schizoxylon albescens . FEMS Microbiology Ecology 75: 255272.
Muggia, L., Pérez-Ortega, S., Kopun, T., Zellnig, G. & Grube, M. (2014) Photobiont selectivity leads to ecological tolerance and evolutionary divergence in a polymorphic complex of lichenized fungi. Annals of Botany 114: 463475.
O’Brien, H. E. (2013 a) a searchable database of photobiont sequences. Retrieved from
O’Brien, H. E. (2013 b) Symbiotic Nostoc revisited. Retrieved from
Orange, A., James, P. W. & White, F. J. (2001) Microchemical Methods for the Identification of Lichens. London: British Lichen Society.
Otálora, M. A. G., Martínez, I., O’Brien, H., Molina, M. C., Aragón, G. & Lutzoni, F. (2010) Multiple origins of high reciprocal symbiotic specificity at an intercontinental spatial scale among gelatinous lichens (Collemataceae, Lecanoromycetes). Molecular Phylogenetics and Evolution 56: 10891095.
Park, C. H., Kim, K. M., Elvebakk, A., Kim, O.-S., Jeong, G. & Hong, S. G. (2014) Algal and fungal diversity in Antarctic lichens. Journal of Eukaryotic Microbiology 62: 196205.
Piercey-Normore, M. D. (2006) The lichen-forming ascomycete Evernia mesomorpha associates with multiple genotypes of Trebouxia jamesii . New Phytologist 169: 331344.
Piercey-Normore, M. D. & DePriest, P. T. (2001) Algal switching among lichen symbioses. American Journal of Botany 88: 14901498.
Pröschold, T., Darienko, T., Silva, P. C., Reisser, W. & Krienitz, L. (2011) The systematics of Zoochlorella revisited employing an integrative approach. Environmental Microbiology 13: 350364.
Rambaut, A., Suchard, M., Xie, D. & Drummond, A. (2014) Tracer v1.6. Available from
Ruprecht, U., Brunauer, G. & Printzen, C. (2012) Genetic diversity of photobionts in Antarctic lecideoid lichens from an ecological view point. Lichenologist 44: 661678.
Sadowska-Des, A. D., Dal Grande, F., Lumbsch, H. T., Beck, A., Otte, J., Hur, J. S., Kim, J. A. & Schmitt, I. (2014) Integrating coalescent and phylogenetic approaches to delimit species in the lichen photobiont Trebouxia . Molecular Phylogenetics and Evolution 76: 202210.
Samarakoon, T., Wang, S. Y. & Alford, M. H. (2013) Enhancing PCR amplification of DNA from recalcitrant plant specimens using a trehalose-based additive. Applications in Plant Sciences 1: 1200236.
Sherwood, A. R., Garbary, D. J. & Sheath, R. G. (2000) Assessing the phylogenetic position of the Prasiolales (Chlorophyta) using rbcL and 18S rRNA gene sequence data. Phycologia 39: 139146.
Škaloud, P. & Peksa, O. (2010) Evolutionary inferences based on ITS rDNA and actin sequences reveal extensive diversity of the common lichen alga Asterochloris (Trebouxiophyceae, Chlorophyta). Molecular Phylogenetics and Evolution 54: 3646.
Smith, D. C. & Douglas, A. (1987) The Biology of Symbiosis. London: Edward Arnold.
Thompson, J. N. (2009) The coevolving web of life. American Naturalist 173: 125140.
Thüs, H., Muggia, L., Perez-Ortega, S., Favero-Longo, S. E., Joneson, S., O’Brien, H., Nelsen, M. P., Duque-Thues, R., Grube, M., Friedl, T., et al. (2011) Revisiting photobiont diversity in the lichen family Verrucariaceae (Ascomycota). European Journal of Phycology 46: 399415.
Tremouillaux-Guiller, J. & Huss, V. A. R. (2007) A cryptic intracellular green alga in Ginkgo biloba: ribosomal DNA markers reveal worldwide distribution. Planta 226: 553557.
Tsarenko, P. M. (2011) Trebouxiophyceae . In Algae of Ukraine: Diversity, Nomenclature, Taxonomy, Ecology and Geography. Volume 3: Chlorophyta (P. M. Tsarenko, S. P. Wasser & E. Nevo, eds): 61108. Ruggell: A.R.A. Gantner Verlag K.-G.
Tschermak-Woess, E. (1985) Elliptochloris bilobata - not a rare phycobiont. Herzogia 7: 105116.
Voytsekhovich, A., Dymytrova, L. & Nadyeina, O. (2011 a) Photobiont composition of some taxa of the genera Micarea and Placynthiella (Lecanoromycetes, lichenized Ascomycota) from Ukraine. Folia Cryptogamica Estonica 48: 135148.
Voytsekhovich, A., Mikhailyuk, T. I. & Darienko, T. (2011 b) Lichen photobionts 1: biodiversity, ecophysiology and co-evolution with the mycobiont. Algologia 21: 326.
Werth, S. (2012) Fungal-algal interactions in Ramalina menziesii and its associated epiphytic lichen community. Lichenologist 44: 543560.
White, T. J., Bruns, T., Lee, S. & Taylor, J. W. (1990) Amplification and direct sequencing of fungal ribosomal RNA genes for phylogenetics. In PCR Protocols: a Guide to Methods and Applications (M. A. Innis, D. H. Gelfand, J. J. Sninsky & T. J. White, eds): 315322. New York: Academic Press.
Yahr, R., Vilgalys, R. & DePriest, P. T. (2006) Geographic variation in algal partners of Cladonia subtenuis (Cladoniaceae) highlights the dynamic nature of a lichen symbiosis. New Phytologist 171: 847860.
Yahr, R., Coppins, B. J. & Ellis, C. J. (2011) Preserved epiphytes as an archaeological resource in pre-industrial vernacular buildings. Journal of Archaeological Science 38: 11911198.
Zoller, S. & Lutzoni, F. (2003) Slow algae, fast fungi: exceptionally high nucleotide substitution rate differences between lichenized fungi Omphalina and their symbiotic green algae Coccomyxa . Molecular Phylogenetics and Evolution 29: 629640.


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Molecular and morphological diversity in photobionts associated with Micarea s. str. (Lecanorales, Ascomycota)

  • Rebecca Yahr (a1), Anna Florence (a1), Pavel Škaloud (a2) and Anna Voytsekhovich (a3)


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