Hostname: page-component-586b7cd67f-2brh9 Total loading time: 0 Render date: 2024-11-29T17:02:56.481Z Has data issue: false hasContentIssue false
  • English
  • Français

Fungal-algal interactions in Ramalina menziesii and its associated epiphytic lichen community

Published online by Cambridge University Press:  08 June 2012

Silke WERTH
Silke WERTH
Affiliation:
Department of Ecology and Evolutionary Biology, University of California Los Angeles, Box 951606, Los Angeles, California 90095-1606, USA and Biodiversity and Conservation Biology, Swiss Federal Research Institute for Forest, Snow and Landscape Research WSL, Zürcherstrasse 111, CH-8903 Birmensdorf, Switzerland. Email: [email protected]
Get access Rights & Permissions [Opens in a new window]

Abstract

Lichens are a fascinating example of a symbiotic mutualism. It is still uncertain which processes guide fungal-photobiont interactions, and whether they are random or of a more complex nature. Here, the fungal-algal interactions in Ramalina menziesii and co-occurring taxa are analyzed by using DNA sequences of the algal Internal Transcribed Spacer region (ITS), to investigate fungal-algal associations in juvenile R. menziesii and allied species. Algal species were identified by a combination of BLAST searches, median-joining network analysis, and Bayesian phylogenetics. Fungal-algal networks were analyzed for nestedness, both at the species and haplotype level (fungal species vs. algal haplotypes), and the networks were inspected for evidence of compartmentalization. Bayesian phylogenetic trees indicated that the widespread green alga Trebouxia decolorans associated with R. menziesii, as well as six other fungal species. Four additional fungal species interacted with four different species of Trebouxia. Only in one out of ten samples were algal haplotypes shared with the nearest neighbours of juvenile R. menziesii. Fungal-algal species interactions were compartmentalized, while at the level of algal haplotypes, nestedness was found. This pattern is similar to the compartmentalization found in other intimately interacting mutualists.

Keywords

compartmentalizationlichen-forming funginestednessphotobiontspecies interactionsspecificitysymbiosis
Type
Research Article
Information
The Lichenologist , Volume 44 , Issue 4 , July 2012 , pp. 543 - 560
Copyright
Copyright © British Lichen Society 2012

Access options

Get access to the full version of this content by using one of the access options below. (Log in options will check for institutional or personal access. Content may require purchase if you do not have access.)

References

Ahmadjian, V. (1988) The lichen alga Trebouxia – does it occur free-living? Plant Systematics and Evolution 158: 243–247.CrossRefGoogle Scholar
Altschul, S. F., Madden, T. L., Schäffer, A. A., Zhang, J., Zhang, Z., Miller, W. & Lipman, D. J. (1997) Gapped BLAST and PSI-BLAST: a new generation of protein database search programs. Nucleic Acids Research 25: 3389–3402.CrossRefGoogle ScholarPubMed
Atmar, W. & Patterson, B. D. (1993) The measure of order and disorder in the distribution of species in fragmented habitat. Oecologia 96: 373–382.CrossRefGoogle ScholarPubMed
Bandelt, H. J., Forster, P., Sykes, B. C. & Richards, M. B. (1995) Mitochondrial portraits of human populations using median networks. Genetics 141: 743–753.CrossRefGoogle ScholarPubMed
Bandelt, H. J., Forster, P. & Röhl, A. (1999) Median-joining networks for inferring intraspecific phylogenies. Molecular Biology and Evolution 16: 37–48.CrossRefGoogle ScholarPubMed
Bascompte, J. & Jordano, P. (2007) Plant-animal mutualistic networks: the architecture of biodiversity. Annual Review of Ecology Evolution and Systematics 38: 567–593.CrossRefGoogle Scholar
Bascompte, J., Jordano, P., Melian, C. J. & Olesen, J. M. (2003) The nested assembly of plant-animal mutualistic networks. Proceedings of the National Academy of Sciences of the United States of America 100: 9383–9387.CrossRefGoogle ScholarPubMed
Beck, A. (1999) Photobiont inventory of a lichen community growing on heavy-metal-rich rock. Lichenologist 31: 501–510.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: 709–720.CrossRefGoogle Scholar
Beck, A., Kasalicky, T. & Rambold, G. (2002) Myco-photobiontal selection in a Mediterranean cryptogam community with Fulgensia fulgida. New Phytologist 153: 317–326.CrossRefGoogle Scholar
Bhattacharya, D., Friedl, T. & Damberger, S. (1996) Nuclear-encoded rDNA group I introns: origin and phylogenetic relationships of insertion site lineages in the green algae. Molecular Biology and Evolution 13: 978–989.CrossRefGoogle Scholar
Blaha, J., Baloch, E. & Grube, M. (2006) High photobiont diversity associated with the euryoecious lichen-forming ascomycete Lecanora rupicola (Lecanoraceae, Ascomycota). Biological Journal of the Linnean Society 88: 283–293.CrossRefGoogle Scholar
Brodo, I. M., Sharnoff, S. D. & Sharnoff, S. (2001) Lichens of North America. New Haven: Yale University Press.Google Scholar
Bubrick, P., Galun, M. & Frensdorff, A. (1984) Observations on free-living Trebouxia Depuymaly and Pseudotrebouxia Archibald, and evidence that both symbionts from Xanthoria parientina (L.) Th. Fr. can be found free-living in nature. New Phytologist 97: 455–462.CrossRefGoogle Scholar
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: 806–818.CrossRefGoogle ScholarPubMed
Dahlkild, A., Kallersjo, M., Lohtander, K. & Tehler, A. (2001) Photobiont diversity in the Physciaceae (Lecanorales). Bryologist 104: 527–536.CrossRefGoogle Scholar
Doering, M. & Piercey-Normore, M. D. (2009) Genetically divergent algae shape an epiphytic lichen community on Jack Pine in Manitoba. Lichenologist 41: 69–80.CrossRefGoogle Scholar
Fahselt, D. (1994) Secondary biochemistry of lichens. Symbiosis 16: 117–165.Google Scholar
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: 1208–1232.CrossRefGoogle ScholarPubMed
Friedl, T. (1987) Thallus development and phycobionts of the parasitic lichen Diploschistes muscorum. Lichenologist 19: 183–191.CrossRefGoogle Scholar
Friedl, T., Besendahl, A., Pfeiffer, P. & Bhattacharya, D. (2000) The distribution of group I introns in lichen algae suggests that lichenization facilitates intron lateral transfer. Molecular Phylogenetics and Evolution 14: 342–352.CrossRefGoogle Scholar
Goffinet, B. & Bayer, R. J. (1997) Characterization of mycobionts of photomorph pairs in the Peltigerineae (lichenized ascomycetes) based on internal transcribed spacer sequences of the nuclear ribosomal DNA. Fungal Genetics and Biology 21: 228–237.CrossRefGoogle ScholarPubMed
Guimarães, P. R. & Guimarães, P. (2006) Improving the analyses of nestedness for large sets of matrices. Environmental Modelling and Software 21: 1512–1513.CrossRefGoogle Scholar
Guimarães, P. R., Rico-Gray, V., Oliveira, P. S., Izzo, T. J., dos Reis, S. F. & Thompson, J. N. (2007) Interaction intimacy affects structure and coevolutionary dynamics in mutualistic networks. Current Biology 17: 1797–1803.CrossRefGoogle ScholarPubMed
Hauck, M., Helms, G. & Friedl, T. (2007) Photobiont selectivity in the epiphytic lichens Hypogymnia physodes and Lecanora conizaeoides. Lichenologist 39: 195–204.CrossRefGoogle Scholar
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.CrossRefGoogle Scholar
Hilmo, O. & Ott, S. (2002) Juvenile development of the cyanolichen Lobaria scrobiculata and the green algal lichens Platismatia glauca and Platismatia norvegica in a boreal Picea abies forest. Plant Biology 4: 273–280.CrossRefGoogle Scholar
Hilmo, O. & Såstad, S. M. (2001) Colonization of old-forest lichens in a young and an old boreal Picea abies forest: an experimental approach. Biological Conservation 102: 251–259.CrossRefGoogle Scholar
Honegger, R. (2008) Mycobionts. In Lichen Biology (Nash, T. H. III, ed.): 27–39. Cambridge: Cambridge University Press.CrossRefGoogle Scholar
Jordano, P., Bascompte, J. & Olesen, J. M. (2003) Invariant properties in coevolutionary networks of plant-animal interactions. Ecology Letters 6: 69–81.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: 645–660.CrossRefGoogle Scholar
Kumar, S., Tamura, K. & Nei, M. (2004) MEGA3: Integrated software for molecular evolutionary genetics analysis and sequence alignment. Briefings in Bioinformatics 5: 150–163.CrossRefGoogle ScholarPubMed
Margulis, L. & Fester, R. (1991) Symbiosis as a Source of Evolutionary Innovation: Speciation and Morphogenesis. Cambridge, Massachusetts: MIT Press.Google ScholarPubMed
Mukhtar, A., Garty, J. & Galun, M. (1994) Does the lichen alga Trebouxia occur free-living in nature – further immunological evidence. Symbiosis 17: 247–253.Google Scholar
Myllys, L., Stenroos, S., Thell, A. & Kuusinen, M. (2007) High cyanobiont selectivity of epiphytic lichens in old growth boreal forest of Finland. New Phytologist 173: 621–629.CrossRefGoogle ScholarPubMed
Nash, T. H. III (1996) Lichen Biology. Cambridge: Cambridge University Press.Google Scholar
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
Nelsen, M. P. & Gargas, A. (2009) Symbiont flexibility in Thamnolia vermicularis (Pertusariales: Icmadophilaceae). Bryologist 112: 404–417.CrossRefGoogle Scholar
Nylander, J. A. A. (2004) MrModeltest v2. Program distributed by the author. Available from http://www.abc.se/~nylander/. Evolutionary Biology Centre, Uppsala University.Google Scholar
Ohmura, Y., Kawachi, M., Kasai, F., Watanabe, M. M. & Takeshita, S. (2006) Genetic combinations of symbionts in a vegetatively reproducing lichen, Parmotrema tinctorum, based on ITS rDNA sequences. Bryologist 109: 43–59.CrossRefGoogle Scholar
Ott, S. (1987 a) The juvenile development of lichen thalli from vegetative diaspores. Symbiosis 3: 57–74.Google Scholar
Ott, S. (1987 b) Sexual reproduction and developmental adaptations in Xanthoria parietina. Nordic Journal of Botany 7: 219–228.CrossRefGoogle Scholar
Ott, S., Schröder, T. & Jahns, H. M. (2000) Colonization strategies and interactions of lichens on twigs. Bibliotheca Lichenologica 75: 445–455.Google Scholar
Peksa, O. & Skaloud, P. (2011) Do photobionts influence the ecology of lichens? A case study of environmental preferences in symbiotic green alga Asterochloris (Trebouxiophyceae). Molecular Ecology 20: 3936–3948.CrossRefGoogle ScholarPubMed
Piercey-Normore, M. D. (2004) Selection of algal genotypes by three species of lichen fungi in the genus Cladonia. Canadian Journal of Botany 82: 947–961.CrossRefGoogle Scholar
Piercey-Normore, M. D. (2006) The lichen-forming ascomycete Evernia mesomorpha associates with multiple genotypes of Trebouxia jamesii. New Phytologist 169: 331–344.CrossRefGoogle ScholarPubMed
Piercey-Normore, M. D. & DePriest, P. T. (2001) Algal switching among lichen symbioses. American Journal of Botany 88: 1490–1498.CrossRefGoogle ScholarPubMed
Posada, D. & Crandall, K. A. (1998) Modeltest: testing the model of DNA substitution. Bioinformatics 14: 817–818.CrossRefGoogle ScholarPubMed
Rambold, G., Friedl, T. & Beck, A. (1998) Photobionts in lichens: possible indicators of phylogenetic relationships? Bryologist 101: 392–397.CrossRefGoogle Scholar
Richardson, D. H. S. (1999) War in the world of lichens: parasitism and symbiosis as exemplified by lichens and lichenicolous fungi. Mycological Research 103: 641–650.CrossRefGoogle Scholar
Rikkinen, J. (2003) Ecological and evolutionary role of photobiont-mediated guilds in lichens. Symbiosis 34: 99–110.Google Scholar
Rikkinen, J., Oksanen, I. & Lohtander, K. (2002) Lichen guilds share related cyanobacterial symbionts. Science 297: 357.CrossRefGoogle ScholarPubMed
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. Molecular Biology and Evolution 19: 1209–1217.CrossRefGoogle ScholarPubMed
Ronquist, F. & Huelsenbeck, J. P. (2003) MrBayes 3: Bayesian phylogenetic inference under mixed models. Bioinformatics 19: 1572–1574.CrossRefGoogle ScholarPubMed
Sanders, W. B. & Lücking, R. (2002) Reproductive strategies, relichenization and thallus development observed in situ in leaf-dwelling lichen communities. New Phytologist 155: 425–435.CrossRefGoogle ScholarPubMed
Scheidegger, C. (1995) Early development of transplanted isidioid soredia of Lobaria pulmonaria in an endangered population. Lichenologist 27: 361–374.CrossRefGoogle Scholar
Scheidegger, C. & Werth, S. (2009) Conservation strategies for lichens: insights from population biology. Fungal Biology Reviews 23: 55–66.CrossRefGoogle Scholar
Schuster, G. (1985) Die Jugendentwicklung von Flechten: ein Indikator für Klimabedingungen und Umweltbelastung. Bibliotheca Lichenologica 20: 1–206.Google Scholar
Sillett, S. C., McCune, B., Peck, J. E. & Rambo, T. R. (2000 a) Four years of epiphyte colonization in Douglas-fir forest canopies. Bryologist 103: 661–669.CrossRefGoogle Scholar
Sillett, S. C., McCune, B., Peck, J. E., Rambo, T. R. & Ruchty, A. (2000 b) Dispersal limitations of epiphytic lichens result in species dependent on old-growth forests. Ecological Applications 10: 789–799.CrossRefGoogle Scholar
Smith, D. C. & Douglas, A. E. (1987) The Biology of Symbiosis. London: Edward Arnold (Publishers) Ltd.Google Scholar
Sork, V. L., Davis, F. W., Dyer, R. J. & Smouse, P. E. (2002 a) Mating patterns in a savanna population of valley oak (Quercus lobata Nee). In Fifth Symposium on Oak Woodlands: Oaks in California's Changing Landscape (Standiford, D. M. R. B. & Purcell, K. L., eds.): 427–439. USDA Forest Service Gen. Tech. Rep. PSW-GTR-184. San Diego, California: US Department of Agriculture.Google Scholar
Sork, V. L., Davis, F. W., Smouse, P. E., Apsit, V. J., Dyer, R. J., Fernandez, J. F. & Kuhn, B. (2002 b) Pollen movement in declining populations of California valley oak, Quercus lobata: where have all the fathers gone? Molecular Ecology 11: 1657–1668.CrossRefGoogle ScholarPubMed
Stenroos, S., Högnabba, F., Myllys, L., Hyvönen, J. & Thell, A. (2006) High selectivity in symbiotic associations of lichenized ascomycetes and cyanobacteria. Cladistics 22: 230–238.CrossRefGoogle Scholar
Summerfield, T. C., Galloway, D. J. & Eaton-Rye, J. J. (2002) Species of cyanolichens from Pseudocyphellaria with indistinguishable ITS sequences have different photobionts. New Phytologist 155: 121–129.CrossRefGoogle ScholarPubMed
Swofford, D. L. (1998) PAUP*. Phylogenetic Analysis Using Parsimony (*and Other Methods), version 4. Sunderland, Massachusetts: Sinauer Associates Inc.Google Scholar
Tamura, K., Dudley, J., Nei, M. & Kumar, S. (2007) MEGA4: Molecular evolutionary genetics analysis (MEGA) software version 4.0. Molecular Biology and Evolution 24: 1596–1599.CrossRefGoogle ScholarPubMed
Thompson, J. D., Higgins, D. G. & Gibson, T. J. (1994) CLUSTAL W: improving the sensitivity of progressive multiple sequence alignment through sequence weighting, position-specific gap penalties and weight matrix choice. Nucleic Acids Research 22: 4673–4680.CrossRefGoogle ScholarPubMed
Tønsberg, T. & Goward, T. (2001) Sticta oroborealis sp. nov., and other Pacific North American lichens forming dendriscocauloid cyanotypes. Bryologist 104: 12–23.CrossRefGoogle Scholar
Werth, S. (2010) Population genetics of lichen-forming fungi – a review. Lichenologist 42: 499–519.CrossRefGoogle Scholar
Werth, S. (2011) Biogeography and phylogeography of lichen fungi and their photobionts. In Biogeography of Micro-organisms. Is Everything Small Everywhere? (Fontaneto, D., ed.): 191–208. Cambridge: Cambridge University Press.CrossRefGoogle Scholar
Werth, S. & Scheidegger, C. (2012) Congruent genetic structure in the lichen-forming fungus Lobaria pulmonaria and its green-algal photobiont. Molecular Plant-Microbe Interactions 25: 220–230.CrossRefGoogle ScholarPubMed
Werth, S. & Sork, V. L. (2008) Local genetic structure in a North American epiphytic lichen, Ramalina menziesii (Ramalinaceae). American Journal of Botany 95: 568–576.CrossRefGoogle Scholar
Werth, S. & Sork, V. L. (2010) Identity and genetic structure of the photobiont of the epiphytic lichen Ramalina menziesii on three oak species in southern California. American Journal of Botany 97: 821–830.CrossRefGoogle ScholarPubMed
Werth, S., Wagner, H. H., Gugerli, F., Holderegger, R., Csencsics, D., Kalwij, J. M. & Scheidegger, C. (2006 a) Quantifying dispersal and establishment limitation in a population of an epiphytic lichen. Ecology 87: 2037–2046.CrossRefGoogle Scholar
Werth, S., Wagner, H. H., Holderegger, R., Kalwij, J. M. & Scheidegger, C. (2006 b) Effect of disturbances on the genetic diversity of an old-forest associated lichen. Molecular Ecology 15: 911–921.CrossRefGoogle ScholarPubMed
Wirtz, N., Lumbsch, H. T., Green, T. G. A., Türk, R., Pintado, A., Sancho, L. & Schroeter, B. (2003) Lichen fungi have low cyanobiont selectivity in maritime Antarctica. New Phytologist 160: 177–183.CrossRefGoogle ScholarPubMed
Wornik, S. & Grube, M. (2010) Joint dispersal does not imply maintenance of partnerships in lichen symbioses. Microbial Ecology 59: 150–157.CrossRefGoogle Scholar
Yahr, R., Vilgalys, R. & DePriest, P. T. (2004) Strong fungal specificity and selectivity for algal symbionts in Florida scrub Cladonia lichens. Molecular Ecology 13: 3367–3378.CrossRefGoogle ScholarPubMed
Zoller, S., Frey, B. & Scheidegger, C. (2000) Juvenile development and diaspore survival in the threatened epiphytic lichen species Sticta fuliginosa, Leptogium saturninum and Menegazzia terebrata: Conclusions for in situ conservation. Plant Biology 2: 496–504.CrossRefGoogle Scholar