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Contrasting pattern of photobiont diversity in the Atlantic and Pacific populations of Erioderma pedicellatum (Pannariaceae)

Published online by Cambridge University Press:  28 July 2016

Carolina CORNEJO ,
Peter R. NELSON ,
Irina STEPANCHIKOVA ,
Dmitry HIMELBRANT ,
Per-Magnus JØRGENSEN  and
Christoph SCHEIDEGGER
Carolina CORNEJO*
Affiliation:
Swiss Federal Research Institute WSL, Zuercherstrasse 111, 8903 Birmensdorf, Switzerland
Peter R. NELSON
Affiliation:
University of Maine-Fort Kent, 23 University Drive, Fort Kent, Maine 04743, USA
Irina STEPANCHIKOVA
Affiliation:
St. Petersburg State University, Universitetskaya emb. 7–9, 199034 St. Petersburg, Russia; Komarov Botanical Institute RAS, Professor Popov St. 2, 197376 St. Petersburg, Russia
Dmitry HIMELBRANT
Affiliation:
St. Petersburg State University, Universitetskaya emb. 7–9, 199034 St. Petersburg, Russia; Komarov Botanical Institute RAS, Professor Popov St. 2, 197376 St. Petersburg, Russia
Per-Magnus JØRGENSEN
Affiliation:
Department of Natural History, Bergen University Museum, Allégt. 41, Box 7800, 5020 Bergen, Norway
Christoph SCHEIDEGGER
Affiliation:
Swiss Federal Research Institute WSL, Zuercherstrasse 111, 8903 Birmensdorf, Switzerland
*
Email: carolina.cornejo@wsl.ch
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Abstract

The present study investigates the photobiont diversity of the boreal felt lichen, Erioderma pedicellatum. Previously sampled genetic data from Newfoundland were reanalyzed and new sequence data (16S rDNA, rbcLX) of the boreal felt lichen from Alaska (USA), Kamchatka (Russia), and North Trøndelag (Norway) were generated. The highest genetic diversity of the photobiont is found in Alaska and Kamchatka, indicating that these may be the primary sources of the species in the Northern Hemisphere. In Newfoundland, the photobiont of E. pedicellatum was screened on leaves of the symbiotic liverwort Frullania asagrayana and it was found to occur on trees where no other lichens were present, demonstrating that the geographical distribution, and possibly also the ecological requirement of the photobiont of E. pedicellatum, is wider than that of the lichen phenotype. Finally, a postulated association between the occurrence of the vegetatively reproducing Coccocarpia palmicola and the occurrence of the compatible photobiont of E. pedicellatum on the same tree could not be established.

Keywords

cyanobacteriaFrullania asagrayanaphotobiont-mediated lichen guildRhizonemaRuBisCotripartite interaction16S rDNA
Type
Articles
Information
The Lichenologist , Volume 48 , Issue 4 , July 2016 , pp. 275 - 291
Copyright
© British Lichen Society, 2016 

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References

Adams, D., Bergman, B., Nierzwicki-Bauer, S., Duggan, P., Rai, A. & Schüßler, A. (2013) Cyanobacterial-plant symbioses. In The Prokaryotes (E. Rosenberg, E. Delong, S. Lory, E. Stackebrandt & F. Thompson, eds): 359–400. Berlin, Heidelberg: Springer.CrossRefGoogle Scholar
Ahlner, S. (1954) Värmlands märkligaste lav. I. In Natur I Värmland (N. H. Magnusson & K. Curry-Lindahl, eds): 99–102. Stockholm: Bokförlaget Svensk Natur.Google Scholar
Bruen, T. C., Philippe, H. & Bryant, D. (2006) A simple and robust statistical test for detecting the presence of recombination. Genetics 172: 2665–2681.CrossRefGoogle ScholarPubMed
Cameron, R., Neily, T. & Anderson, F. (2010) Observations of mortality in a small population of the endangered lichen Erioderma pedicellatum . Opuscula Philolichenum 8: 67–70.Google Scholar
Cameron, R., Goudie, I. & Richardson, D. (2013 a) Habitat loss exceeds habitat regeneration for an IUCN flagship lichen epiphyte: Erioderma pedicellatum . Canadian Journal of Forest Research 43: 1075–1080.CrossRefGoogle Scholar
Cameron, R. P., Neily, T. & Clapp, H. (2013 b) Forest harvesting impacts on mortality of an endangered lichen at the landscape and stand scales. Canadian Journal of Forest Research 43: 507–511.CrossRefGoogle Scholar
Castresana, J. (2000) Selection of conserved blocks from multiple alignments for their use in phylogenetic analysis. Molecular Biology and Evolution 17: 540–552.CrossRefGoogle ScholarPubMed
Clement, M., Posada, D. & Crandall, K. A. (2000) TCS: a computer program to estimate gene genealogies. Molecular Ecology 9: 1657–1659.CrossRefGoogle ScholarPubMed
Cornejo, C. & Scheidegger, C. (2016) Cyanobacterial gardens: the liverwort Frullania asagrayana acts as a reservoir of lichen photobionts. Environmental Microbiology Reports 8: 352–357.CrossRefGoogle ScholarPubMed
Dal-Forno, M., Lawrey, J. D., Sikaroodi, M., Bhattarai, S., Gillevet, P. M., Sulzbacher, M. & Lücking, R. (2013) Starting from scratch: evolution of the lichen thallus in the basidiolichen Dictyonema (Agaricales: Hygrophoraceae). Fungal Biology 117: 584–598.CrossRefGoogle ScholarPubMed
Dal-Forno, M., Lücking, R., Bungartz, F., Yánez-Ayabaca, A., Marcelli, M. P., Spielmann, A. A., Coca, L. F., Chaves, J. L., Aptroot, A. & Sipman, H. (2016) From one to six: unrecognized species diversity in the genus Acantholichen (lichenized Basidiomycota: Hygrophoraceae). Mycologia 108: 38–55.CrossRefGoogle ScholarPubMed
Dal Grande, F., Widmer, I., Wagner, H. & Scheidegger, C. (2012) Vertical and horizontal photobiont transmission within populations of a lichen symbiosis. Molecular Ecology 21: 3159–3172.CrossRefGoogle ScholarPubMed
Dal Grande, F., Beck, A., Cornejo, C., Singh, G., Cheenacharoen, S., Nelsen, M. P. & Scheidegger, C. (2014) Molecular phylogeny and symbiotic selectivity of the green algal genus Dictyochloropsis s.l. (Trebouxiophyceae): a polyphyletic and widespread group forming photobiont-mediated guilds in the lichen family Lobariaceae . New Phytologist 202: 455–470.CrossRefGoogle ScholarPubMed
Dereeper, A., Guignon, V., Blanc, G., Audic, S., Buffet, S., Chevenet, F., Dufayard, J. F., Guindon, S., Lefort, V., Lescot, M., et al. (2008) Phylogeny.fr: robust phylogenetic analysis for the non-specialist. Nucleic Acids Research 36: W465–W469.CrossRefGoogle ScholarPubMed
Dereeper, A., Audic, S., Claverie, J.-M. & Blanc, G. (2010) BLAST-EXPLORER helps you building datasets for phylogenetic analysis. BMC Evolutionary Biology 10: 8.CrossRefGoogle ScholarPubMed
Fedrowitz, K., Kaasalainen, U. & Rikkinen, J. (2012) Geographic mosaic of symbiont selectivity in a genus of epiphytic cyanolichens. Ecology and Evolution 2: 2291–2303.CrossRefGoogle Scholar
Fernández-Mendoza, F., Domaschke, S., García, M., Jordan, P., Martín, M. P. & Printzen, C. (2011) Population structure of mycobionts and photobionts of the widespread lichen Cetraria aculeata . Molecular Ecology 20: 1208–1232.CrossRefGoogle ScholarPubMed
Gomulkiewicz, R., Drown, D. M., Dybdahl, M. F., Godsoe, W., Nuismer, S. L., Pepin, K. M., Ridenhour, B. J., Smith, C. I. & Yoder, J. B. (2007) Dos and don’ts of testing the geographic mosaic theory of coevolution. Heredity 98: 249–258.CrossRefGoogle ScholarPubMed
Hart, M. W. & Sunday, J. (2007) Things fall apart: biological species form unconnected parsimony networks. Biology Letters 3: 509–512.CrossRefGoogle ScholarPubMed
Holien, H., Gaarder, G. & Håpnes, A. (1995) Erioderma pedicellatum still present, but highly endangered in Europe. Graphis scripta 7: 79–84.Google Scholar
Honegger, R. (2012) The symbiotic phenotype of lichen-forming ascomycetes and their endo- and epibionts. In Fungal Associations IX (B. Hock, ed.): 287–339. Berlin: Springer-Verlag.CrossRefGoogle Scholar
Huson, D. H. & Bryant, D. (2006) Application of phylogenetic networks in evolutionary studies. Molecular Biology and Evolution 23: 254–267.CrossRefGoogle ScholarPubMed
Joly, S., Stevens, M. I. & van Vuuren, B. J. (2007) Haplotype networks can be misleading in the presence of missing data. Systematic Biology 56: 857–862.CrossRefGoogle ScholarPubMed
Jørgensen, P. M. (1990) Trønderlav (Erioderma pedicellatum) – Norges mest gåtefulle plante. Blyttia 48: 119–123.Google Scholar
Jørgensen, P. M. (2001) The present status of the names applicable to species and infraspecific taxa of Erioderma (lichenised ascomycetes) included in Zahlbruckner’s Catalogus. Taxon 50: 525–541.CrossRefGoogle Scholar
Jørgensen, P. M. (2006) Conspectus familiae Pannariaceae (Ascomycetes lichenosae). Ilicifolia 4: 1–78.Google Scholar
Jørgensen, P. M. & Arvidsson, L. (2002) The lichen genus Erioderma (Pannariaceae) in Ecuador and neighbouring countries. Nordic Journal of Botany 22: 87–114.CrossRefGoogle Scholar
Jørgensen, P. M. & Sipman, H. J. M. (2002) The lichen genus Erioderma in Southeast Asia. Annales Botanici Fennici 39: 201–211.Google Scholar
Jørgensen, P. M., Clayden, S. R., Hanel, C. & Elix, J. A. (2009) Erioderma mollissimum (Pannariaceae) found with certainty in Newfoundland, Canada. Bryologist 112: 572–575.CrossRefGoogle Scholar
Jukes, T. H. & Cantor, C. R. (1969) Evolution of protein molecules. In Mammalian Protein Metabolism, Vol. 3 (H. N. Munro, ed.): 21–132. New York: Academic Press.CrossRefGoogle Scholar
Lawrey, J. D., Lücking, R., Sipman, H. J. M., Chaves, J. L., Redhead, S. A., Bungartz, F., Sikaroodi, M. & Gillevet, P. M. (2009) High concentration of basidiolichens in a single family of agaricoid mushrooms (Basidiomycota: Agaricales: Hygrophoraceae). Mycological Research 113: 1154–1171.CrossRefGoogle Scholar
Librado, P. & Rozas, J. (2009) DnaSP v5: a software for comprehensive analysis of DNA polymorphism data. Bioinformatics 25: 1451–1452.CrossRefGoogle ScholarPubMed
Lücking, R., Lawrey, J. D., Sikaroodi, M., Gillevet, P. M., Chaves, J. L., Sipman, H. J. M. & Bungartz, F. (2009) Do lichens domesticate photobionts like farmers domesticate crops? Evidence from a previously unrecognized lineage of filamentous cyanobacteria. American Journal of Botany 96: 1409–1418.CrossRefGoogle ScholarPubMed
Lücking, R., Barrie, F. R. & Genney, D. (2014) Dictyonema coppinsii, a new name for the European species known as Dictyonema interruptum (Basidiomycota: Agaricales: Hygrophoraceae), with a validation of its photobiont Rhizonema (Cyanoprokaryota: Nostocales: Rhizonemataceae). Lichenologist 46: 261–267.CrossRefGoogle Scholar
Maass, W. S. G. & Yetman, D. J. (2002) COSEWIC Assessment and Status Report on the Boreal Felt Lichen Erioderma pedicellatum. Ottawa: COSEWIC Canadian Wildlife Service.Google Scholar
Miadlikowska, J. & Lutzoni, F. (2000) Phylogenetic revision of the genus Peltigera (lichen-forming Ascomycota) based on morphological, chemical, and large subunit nuclear ribosomal DNA data. International Journal of Plant Sciences 161: 925–958.CrossRefGoogle Scholar
Muggia, L., Nelson, P., Wheeler, T., Yakovchenko, L. S., Tønsberg, T. & Spribille, T. (2011) Convergent evolution of a symbiotic duet: the case of the lichen genus Polychidium (Peltigerales, Ascomycota). American Journal of Botany 98: 1647–1656.CrossRefGoogle ScholarPubMed
Muggia, L., Vancurova, L., Škaloud, 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: 313–323.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: 463–475.CrossRefGoogle Scholar
Nei, M. & Tajima, F. (1983) Maximum likelihood estimation of the number of nucleotide substitutions from restriction sites data. Genetics 105: 207–217.CrossRefGoogle ScholarPubMed
Nelsen, M. P. & Gargas, A. (2008) Dissociation and horizontal transmission of codispersing lichen symbionts in the genus Lepraria (Lecanorales: Stereocaulaceae). New Phytologist 177: 264–275.CrossRefGoogle ScholarPubMed
Nelson, P., Walton, J. & Roland, C. (2009) Erioderma pedicellatum (Hue) P.M. Jørg., new to the United States and western North America, discovered in Denali National Park and Preserve and Denali State Park, Alaska. Evansia 26: 19–23.Google Scholar
Nübel, U., Garciapichel, F. & Muyzer, G. (1997) PCR primers to amplify 16S rRNA genes from cyanobacteria. Applied and Environmental Microbiology 63: 3327–3332.CrossRefGoogle ScholarPubMed
O’Brien, H. E., Miadlikowska, J. & Lutzoni, F. (2013) Assessing population structure and host specialization in lichenized cyanobacteria. New Phytologist 198: 557–566.CrossRefGoogle ScholarPubMed
Otálora, M. A., 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: 1089–1095.CrossRefGoogle ScholarPubMed
Otálora, M. A., Salvador, C., Martínez, I. & Aragón, G. (2013) Does the reproductive strategy affect the transmission and genetic diversity of bionts in cyanolichens? A case study using two closely related species. Microbial Ecology 65: 517–530.CrossRefGoogle ScholarPubMed
R Core Team (2014) R: A Language and Environment for Statistical Computing. R Foundation for Statistical Computing, Vienna, Austria (2012). http://www.R-project.org/ Google Scholar
Reiso, S. & Hofton, T. (2006) Tronderlav Erioderma pedicellatum og fossefiltlav Fuscopannaria confusa funnet i Hedmark. Blyttia 64: 83–88.Google Scholar
Richardson, D. H. S. & Cameron, R. P. (2004) Cyanolichens: their response to pollution and possible management strategies for their conservation in northeastern North America. Northeastern Naturalist 11: 1–22.CrossRefGoogle Scholar
Rikkinen, J. (2002) Cyanolichens: an evolutionary overview. In Cyanobacteria in Symbiosis (A. N. Rai, B. Bergman & U. Rasmussen, eds): 31–72. Dordrecht: Kluwer Academic Publishers.Google Scholar
Rikkinen, J. (2003) Ecological and evolutionary role of photobiont-mediated guilds in lichens. Symbiosis 34: 99–110.Google Scholar
Rikkinen, J. (2009) Relations between cyanobacterial symbionts in lichens and plants. In Prokaryotic Symbionts in Plants (K. Pawlowski, ed.): 265–270. Berlin, Heidelberg: Springer.Google Scholar
Rikkinen, J. (2013) Molecular studies on cyanobacterial diversity in lichen symbioses. MycoKeys 6: 3–32.CrossRefGoogle Scholar
Rikkinen, J. (2015) Cyanolichens. Biodiversity and Conservation 24: 973–993.CrossRefGoogle Scholar
Rudi, K., Skulberg, O. M. & Jakobsen, K. S. (1998) Evolution of cyanobacteria by exchange of genetic material among phyletically related strains. Journal of Bacteriology 180: 3453–3461.CrossRefGoogle ScholarPubMed
Scheidegger, C. (2003) Erioderma pedicellatum - critically endangered. In The IUCN Red List of threatened species. www.iucnredlist.org/details/43995/0 Google Scholar
Stehn, S. E., Nelson, P. R., Roland, C. A. & Jones, J. R. (2013) Patterns in the occupancy and abundance of the globally rare lichen Erioderma pedicellatum in Denali National Park and Preserve, Alaska. Bryologist 116: 2–4.CrossRefGoogle Scholar
Stenroos, S., Stocker-Wörgötter, E., Yoshimura, I., Myllys, L., Thell, A. & Hyvonen, J. (2003) Culture experiments and DNA sequence data confirm the identity of Lobaria photomorphs. Canadian Journal of Botany 81: 232–247.CrossRefGoogle Scholar
Stepanchikova, I. & Himelbrant, D. (2012) Lichen diversity hot spot in Kronotsky Nature Reserve, Kamchatka. In Poster Session at the 7th International Association for Lichenology Symposium, 9–13 January, 2012, Bangkok, Thailand, p. 140.Google Scholar
Tajima, F. (1989) Statistical method for testing the neutral mutation hypothesis by DNA polymorphism. Genetics 123: 585–595.CrossRefGoogle ScholarPubMed
Talavera, G. & Castresana, J. (2007) Improvement of phylogenies after removing divergent and ambiguously aligned blocks from protein sequence alignments. Systematic Biology 56: 564–577.CrossRefGoogle ScholarPubMed
Thompson, J. N. (1999 a) Specific hypotheses on the geographic mosaic of coevolution. American Naturalist 153: S1–S14.CrossRefGoogle Scholar
Thompson, J. N. (1999 b) The evolution of species interactions. Science 284: 2116–2118.CrossRefGoogle ScholarPubMed
Thompson, J. N. (2005) The Geographic Mosaic of Coevolution. Chicago: University of Chicago Press.CrossRefGoogle Scholar
Wedin, M., Wiklund, E., Jorgensen, P. M. & Ekman, S. (2009) Slippery when wet: phylogeny and character evolution in the gelatinous cyanobacterial lichens (Peltigerales, Ascomycetes). Molecular Phylogenetics and Evolution 53: 862–871.CrossRefGoogle ScholarPubMed
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: 847–860.CrossRefGoogle ScholarPubMed
Yánez, A., Dal-Forno, M., Bungartz, F., Lücking, R. & Lawrey, J. D. (2012) A first assessment of Galapagos basidiolichens. Fungal Diversity 52: 225–244.CrossRefGoogle Scholar