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Photobiont associations in co-occurring umbilicate lichens with contrasting modes of reproduction in coastal Norway

Published online by Cambridge University Press:  27 September 2016

CEES, Center for Ecological and Evolutionary Synthesis, Department of Biosciences, University of Oslo, P.O. Box 1066 Blindern, 0316 Oslo, Norway
François LUTZONI
Department of Biology, Duke University, Durham, NC 27708-90338, USA
Department of Biology, Duke University, Durham, NC 27708-90338, USA


The identity and phylogenetic placement of photobionts associated with two lichen-forming fungi, Umbilicaria spodochroa and Lasallia pustulata were examined. These lichens commonly grow together in high abundance on coastal cliffs in Norway, Sweden and Finland. The mycobiont of U. spodochroa reproduces sexually through ascospores, and must find a suitable algal partner in the environment to re-establish the lichen symbiosis. Lasallia pustulata reproduces mainly vegetatively using symbiotic propagules (isidia) containing both symbiotic partners (photobiont and mycobiont). Based on DNA sequences of the internal transcribed spacer region (ITS) we detected seven haplotypes of the green-algal genus Trebouxia in 19 pairs of adjacent thalli of U. spodochroa and L. pustulata from five coastal localities in Norway. As expected, U. spodochroa associated with a higher diversity of photobionts (seven haplotypes) than the mostly asexually reproducing L. pustulata (four haplotypes). The latter was associated with the same haplotype in 15 of the 19 thalli sampled. Nine of the lichen pairs examined share the same algal haplotype, supporting the hypothesis that the mycobiont of U. spodochroa might associate with the photobiont ‘pirated’ from the abundant isidia produced by L. pustulata that are often scattered on the cliff surfaces. Up to six haplotypes of Trebouxia were found within a single sampling site, indicating a low level of specificity of both mycobionts for their algal partner. Most photobiont strains associated with species of Umbilicaria and Lasallia, including samples from this study, represent phylogenetically closely related taxa of Trebouxia grouped within a small number of main clades (Trebouxia sp., T. simplex/T. jamesii, and T. incrustata+T. gigantea). Three of the photobiont haplotypes were found only in U. spodochroa thalli.

© British Lichen Society, 2016 

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Abrams, P. (1983) The theory of limiting similarity. Annual Review of Ecology, Evolution, and Systematics 14: 359376.CrossRefGoogle Scholar
Abrams, P. & Rueffler, C. (2009) Coexistence and limiting similarity of consumer species competing for a linear array of resources. Ecology 90: 812822.CrossRefGoogle Scholar
Ahmadjian, V. (1988) The lichen alga Trebouxia: does it occur free-living? Plant Systematics and Evolution 158: 243247.CrossRefGoogle Scholar
Beck, A. (1999) Photobiont inventory of a lichen community growing on heavy-metal-rich rock. Lichenologist 31: 501510.CrossRefGoogle Scholar
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.CrossRefGoogle Scholar
Beck, A., Kasalicky, T. & Rambold, G. (2002) The myco-photobiontal selection in a Mediterranean cryptogam community with Fulgensia fulgida and considerations on research strategies focusing on the selectivity of lichen bionts. New Phytologist 153: 317326.CrossRefGoogle Scholar
Bowler, P. A. & Rundel, P. W. (1975) Reproductive strategies in lichens. Botanical Journal of the Linnean Society 70: 325340.CrossRefGoogle Scholar
Büdel, B. & Scheidegger, C. (2008) Thallus morphology and anatomy. In Lichen Biology, 2nd edn (T. H. Nash III, ed.): 4370. Cambridge: Cambridge University Press.Google Scholar
Dal Grande, F., Widmer, I., Wagner, H. H. & Scheidegger, C. (2012) Vertical and horizontal photobiont transmission within populations of a lichen symbiosis. Molecular Ecology 21: 31593172.CrossRefGoogle ScholarPubMed
del Campo, E. M., Hoyo, A., Casano, L. M., Martinez-Alberola, F. & Barrena, E. (2010) A rapid and cost-efficient DMSO-based method isolating DNA from cultured lichen photobionts. Taxon 59: 588591.Google Scholar
Domaschke, S., Vivas, M., Sancho, L. G. & Printzen, C. (2013) Ecophysiology and genetic structure of polar versus temperate populations of the lichen Cetraria aculeata . Oecologia 173: 699709.CrossRefGoogle ScholarPubMed
Fedrowitz, K., Kaasalainen, U. & Rikkinen, J. (2011) Genotype variability of Nostoc symbionts associated with three epiphytic Nephroma species in a boreal forest landscape. Bryologist 114: 220230.CrossRefGoogle Scholar
Fernandez-Mendoza, F., Domaschke, S., Garcia, M. A., Jordan, P., Martin, M. P. & Printzen, C. (2011) Population structure of mycobionts and photobionts of the widespread lichen Cetraria aculeata . Molecular Ecology 20: 12081232.CrossRefGoogle ScholarPubMed
Gregersen, I. K., Hegseth, M. N., Hestmark, G., Kongsbak, R. H. & Moe, T. F. (2006) The relationship between thallus mass, surface area and apothecium production in Umbilicaria rigida . Nova Hedwigia 82: 115121.CrossRefGoogle Scholar
Guzow-Krzemińska, B. (2006) Photobiont flexibility in the lichen Protoparmeliopsis muralis as revealed by ITS rDNA analyses. Lichenologist 38: 469476.CrossRefGoogle Scholar
Hauk, M., Helms, G. & Friedl, T. (2007) Photobiont selectivity in the epiphytic lichens Hypogymnia physodes and Lecanora conizaeoides . Lichenologist 39: 195204.CrossRefGoogle Scholar
Hestmark, G. (1990) Thalloconidia in the genus Umbilicaria . Nordic Journal of Botany 9: 547574.CrossRefGoogle Scholar
Hestmark, G. (1991 a) Teleomorph-anamorph relationships in Umbilicaria. I. Making the connections. Lichenologist 23: 343359.CrossRefGoogle Scholar
Hestmark, G. (1991 b) Teleomorph-anamorph relationships in Umbilicaria. II. Patterns in propagative morph production. Lichenologist 23: 361380.CrossRefGoogle Scholar
Hestmark, G. (1991 c) To sex or not to sex...structures and strategies of reproduction in the family Umbilicariaceae (Lecanorales, Ascomycetes). Sommerfeltia Supplement 3: 147.Google Scholar
Hestmark, G. (1992 a) Conidiogenesis in five species of Umbilicaria . Mycological Research 96: 10331043.CrossRefGoogle Scholar
Hestmark, G. (1992 b) Sex, size, competition and escape – strategies of reproduction and dispersal in Lasallia pustulata (Umbilicariaceae, Ascomycetes). Oecologia 92: 305312.CrossRefGoogle Scholar
Hestmark, G. (1997 a) Competitive behaviour of umbilicate lichens - an experimental approach. Oecologia 111: 523528.CrossRefGoogle ScholarPubMed
Hestmark, G. (1997 b) Gap-dynamics, recruitment and individual growth in populations of Lasallia pustulata . Mycological Research 101: 12731280.CrossRefGoogle Scholar
Hestmark, G. (1997 c) Growth from the centre in an umbilicate lichen. Lichenologist 29: 379383.CrossRefGoogle Scholar
Hestmark, G. (2000) The ecophysiology of lichen population biology. Bibliotheca Lichenologica 75: 397403.Google Scholar
Hestmark, G., Schroeter, B. & Kappen, L. (1997) Intrathalline and size-dependent patterns of activity in Lasallia pustulata and their possible consequence for competitive interactions. Functional Ecology 11: 318322.CrossRefGoogle Scholar
Hestmark, G., Skogesal, O. & Skullerud, Ø. (2004) Growth, reproduction, and population structure in four alpine lichens during 240 years of primary colonization. Canadian Journal of Botany 82: 13561362.CrossRefGoogle Scholar
Jones, T. C., Hogg, I. D., Wilkins, R. J. & Green, T. G. A. (2013) Photobiont selectivity for lichens and evidence for a possible glacial refugium in the Ross Region, Antarctica. Polar Biology 36: 767774.CrossRefGoogle Scholar
Kappen, L., Schroeter, B., Hestmark, G. & Winkler, J. B. (1996) Field measurements of photosynthesis of umbilicarious lichens in winter. Botanica Acta 109: 292298.CrossRefGoogle Scholar
Kappen, L., Schroeter, B., Scheidegger, C., Sommerkorn, M. & Hestmark, G. (1997) Cold resistance and metabolic activity of lichens below 0°C. Advances in Space Research 18: 119128.CrossRefGoogle Scholar
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.CrossRefGoogle Scholar
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.CrossRefGoogle Scholar
Leavitt, S. D., Kraichak, E., Nelsen, M. P., Altermann, S., Divakar, P. K., Alors, D., Esslinger, T. L., Crespo, A. & Lumbsch, T. (2015) Fungal specificity and selectivity for algae play a major role in determining lichen partnerships across diverse ecogeographic regions in the lichen-forming family Parmeliaceae (Ascomycota). Molecular Ecology 24: 37793797.CrossRefGoogle Scholar
Lindgren, H., Velmaala, S., Högnabba, P., Goward, T., Holien, H. & Myllys, L. (2014) High fungal selectivity for algal symbionts in the genus Bryoria . Lichenologist 46: 681695.CrossRefGoogle Scholar
Lücking, R., Hodkinson, B. P., Stamatakis, A. & Cartwright, R. A. (2011) PICS-Ord: unlimited coding of ambiguous regions by pairwise identity and cost scores ordination. BMC Bioinformatics 12: 10.CrossRefGoogle ScholarPubMed
Lutzoni, F., Wagner, F. P., Reeb, V. & Zoller, S. (2000) Integrating ambiguously aligned regions of DNA sequences in phylogenetic analyses without violating positional homology. Systematic Biology 49: 628651.CrossRefGoogle ScholarPubMed
MacArthur, R. & Levins, R. (1967) The limiting similarity, convergence, and divergence of coexisting species. American Naturalist 101: 377385.CrossRefGoogle Scholar
Maddison, D. R. & Maddison, W. P. M. (2005) McClade: Analysis of Phylogeny and Character Evolution, 4.08. Sunderland, Massachusetts: Sinauer Associates.Google Scholar
Miadlikowska, J., Kauff, F., Hofstetter, V., Fraker, E., Grube, M., Hafellner, J., Reeb, V., Hodkinson, B. P., Kukwa, M., Lücking, R. et al. (2006) New insights into classification and evolution of the Lecanoromycetes (Pezizomycotina, Ascomycota) from phylogenetic analyses of three ribosomal RNA- and two protein-coding genes. Mycologia 98: 10881103.CrossRefGoogle ScholarPubMed
Miadlikowska, J, Kauff, F., Högnabba, F., Oliver, J. C., Molnár, K., Fraker, E., Gaya, E., Hafellner, J., Hofstetter, V., Gueidan, C. et al. (2014) A multigene phylogenetic synthesis for the class Lecanoromycetes (Ascomycota): 1307 fungi representing 1139 infrageneric taxa, 317 genera and 66 families. Molecular Phylogenetics and Evolution 79: 132168.CrossRefGoogle ScholarPubMed
Miller, M. A., Pfeiffer, W. & Schwartz, T. (2010) Creating the CIPRES Science Gateway for inference of large phylogenetic trees. In Proceedings of the Gateway Computing Environments Workshop (GCE), 14 November 2010, New Orleans, Louisiana, pp. 1–8.Google Scholar
Muggia, L., Vancurova, L., Skaloud, P., Peksa, O., Wedin, M. & Grube, M. (2013) The symbiotic playground of lichen thalli – a highly flexible photobiont association in rock-inhabiting lichens. FEMS Microbiology Ecology 85: 313323.CrossRefGoogle ScholarPubMed
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.CrossRefGoogle Scholar
Nash, T. H. III (2008) Lichen Biology, 2nd edn. Cambridge: Cambridge University Press.CrossRefGoogle Scholar
Nelsen, M. P. & Gargas, A. (2008) Dissociation and horizontal transmission of codispersing lichen symbionts in the genus Lepraria (Lecanorales: Stereocaulaceae). New Phytologist 177: 264275.Google Scholar
Nyati, S., Scherrer, S., Werth, S. & Honegger, R. (2014) Green-algal photobiont diversity (Trebouxia spp.) in representatives of Teloschistaceae (Lecanoromycetes, lichen-forming ascomycetes). Lichenologist 46: 189212.CrossRefGoogle Scholar
O’Brien, H. (2014) Trebouxia update 24 October 2014. Google Scholar
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.CrossRefGoogle Scholar
Paulsrud, P., Rikkinen, J. & Lindblad, P. (2000) Spatial patterns of photobiont diversity in some Nostoc-containing lichens. New Phytologist 146: 291299.CrossRefGoogle Scholar
Pérez-Ortega, S., Ortiz-Alvarez, R., Green, T. G. A. & de los Rios, A. (2012) Lichen myco- and photobiont diversity and their relationships at the edge of life (McMurdo Dry Valleys, Antarctica). FEMS Microbiology Ecology 82: 429448.CrossRefGoogle Scholar
Piercey-Normore, M. (2005) The lichen-forming ascomycete Evernia mesomorpha associates with multiple genotypes of Trebouxia jamesii . New Phytologist 169: 331344.CrossRefGoogle Scholar
Piercey-Normore, M. (2009) Vegetatively reproducing fungi in three genera of the Parmeliaceae share divergent algal partners. Bryologist 112: 773785.CrossRefGoogle Scholar
Piercey-Normore, M. & DePriest, P. T. (2001) Algal switching among lichen symbioses. American Journal of Botany 88: 14901498.CrossRefGoogle ScholarPubMed
Ramstad, S. & Hestmark, G. (2000) Effective neighbourhoods for a saxicolous lichen. Mycological Research 104: 198204.CrossRefGoogle Scholar
Ramstad, S. & Hestmark, G. (2001) Population structure and size-dependent reproductive effort in Umbilicaria spodochroa . Mycologia 93: 453459.CrossRefGoogle Scholar
Rikkinen, J. (2003) Ecological and evolutionary role of photobiont-mediated guilds in lichens. Symbiosis 34: 99110.Google Scholar
Rikkinen, J., Oksanen, I. & Lohtander, K. (2002) Lichen guilds share related cyanobacterial photobionts. Science 297: 357.CrossRefGoogle Scholar
Rodríguez, F., Oliver, J. L., Marin, A. & Medina, J.-R. (1990) The general stochastic model of nucleotide substitution. Journal of Theoretical Biology 142: 458501.CrossRefGoogle ScholarPubMed
Romeike, J., Fridl, 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. Molecular Biology and Evolution 19: 12091217.CrossRefGoogle ScholarPubMed
Sadowska-Des, A., Balint, M., Otte, J. & Schmitt, I. (2013) Assessing intraspecific diversity in a lichen-forming fungus and its green algal symbiont: evaluation of eight molecular markers. Fungal Ecology 6: 141151.CrossRefGoogle Scholar
Sadowska-Des, A., Dal Grande, F., Lumbsch, 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.CrossRefGoogle ScholarPubMed
Simberloff, D. & Dayan, T (1991) The guild concept and the structure of ecological communities. Annual Review of Ecology and Systematics 22: 115143.CrossRefGoogle Scholar
Sletvold, N. & Hestmark, G. (1999) A comparative test of the predictive power of neighbourhood models in natural populations of Lasallia pustulata . Canadian Journal of Botany 77: 16551661.CrossRefGoogle Scholar
Stamatakis, A. (2006) RAxML-VI-HPC: maximum likelihood-based phylogenetic analyses with thousands of taxa and mixed models. Bioinformatics 22: 26882690.CrossRefGoogle ScholarPubMed
Stamatakis, A., Hoover, P. & Rougemont, J. (2008) A rapid bootstrap algorithm for the RAxML Web servers. Systematic Biology 57: 758771.CrossRefGoogle ScholarPubMed
Werth, S. (2012) Fungal-algal interactions in Ramalina menziesii and its associated epiphytic lichen community. Lichenologist 44: 543560.CrossRefGoogle Scholar
Wheeler, D. L., Barrett, T., Benson, D. A., Bryant, S. H., Canese, K., Chetvernin, V., Church, D. M., DiCuccio, M., Edgar, R., Federhen, S. et al. (2007) Database resources of the national center for biotechnology information. Nucleic Acids Research 35: D5D12.CrossRefGoogle ScholarPubMed
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.Google Scholar
Yahr, R., Vilgalys, R. & DePriest, P. (2004) Strong fungal specificity and selectivity for algal symbionts in Florida scrub Cladonia lichens. Molecular Ecology 13: 33673378.CrossRefGoogle ScholarPubMed
Yahr, R., Vilgalys, R. & DePriest, P. (2006) Geographic variation in algal partners in Cladonia subtenuis (Cladoniaceae) highlights the dynamic nature of a lichen symbiosis. New Phytologist 171: 847860.CrossRefGoogle ScholarPubMed
Zolan, M. E. & Pukkila, M. J. (1986) Inheritance of DNA methylation in Coprinus cinereus . Molecular and Cellular Biology 6: 195200.CrossRefGoogle ScholarPubMed