Hostname: page-component-586b7cd67f-r5fsc Total loading time: 0 Render date: 2024-12-06T21:38:48.609Z Has data issue: false hasContentIssue false

Genetic diversity of photobionts in Antarctic lecideoid lichens from an ecological view point

Published online by Cambridge University Press:  24 August 2012

Ulrike RUPRECHT
Affiliation:
University of Salzburg, Organismic Biology, Hellbrunnerstr. 34, 5020 Salzburg, Austria. Email: ulrike.ruprecht@sbg.ac.at
Georg BRUNAUER
Affiliation:
University of Salzburg, Organismic Biology, Hellbrunnerstr. 34, 5020 Salzburg, Austria. Email: ulrike.ruprecht@sbg.ac.at
Christian PRINTZEN
Affiliation:
Senckenberg Forschungsinstitut und Naturmuseum Frankfurt, Abteilung Botanik und Molekulare Evolutionsforschung, Biodiversität und Klima Forschungszentrum (LOEWE BiK-F), Senckenberganlage 25, 60325 Frankfurt, Germany.

Abstract

As part of a comprehensive study on lecideoid lichens in Antarctica, we investigated the photobiont diversity and abundance in 119 specimens of lecideoid lichens from 11 localities in the continental and maritime Antarctic. A phylogeny of these photobiont ITS sequences, including samples from arctic, alpine and temperate lowland regions, reveals the presence of five major Trebouxia clades in Antarctic lecideoid lichens. Two clades are formed by members of the T. jamesii and T. impressa aggregates but for all other clades no close match to any known Trebouxia species could be found in sequence databases. One genetically uniform and well-supported Trebouxia clade was found only in the climatically unique cold desert regions of the Antarctic (preliminarily called Trebouxia sp.URa1), where it is preferentially associated with the highly adapted Antarctic endemic lichen Lecidea cancriformis. Levels of genetic photobiont diversity differ slightly, but insignificantly among ecological regions of the Antarctic and do not decrease towards regions with more unfavourable ecological conditions. The genetic diversity of photobionts varies among mycobiont species. Most pairwise comparisons reveal that these differences are insignificant, probably due to the small sample size for most species. The Antarctic lichens studied here are predominantly not specific for a single photobiont species or lineage, except for Lecidella greenii and L. siplei. These two species are preferably associated with Trebouxia sp. URa2, although in the sampling areas of both species, a pool of several other photobionts is available. Lecidea cancriformis associates with the highest diversity of photobionts followed by L. andersonii.

Type
Research Article
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

REFERENCES

Adams, B. J., Bardgett, R. D., Ayres, E., Wall, D. H., Aislabie, J., Bamforth, S., Bargagli, R., Cary, C., Cavacini, P., Connell, L. et al. (2006) Diversity and distribution of Victoria Land Biota. Soil Biology & Biochemistry 38: 30033018.CrossRefGoogle Scholar
Aoki, M., Nakano, T., Kanda, H. & Deguchi, H. (1998) Photobionts isolated from Antarctic lichens. Journal of Marine Biotechnology 6: 3943.Google Scholar
Barták, M., Váczi, P., Hájek, J. & Smykla, J. (2007) Low-temperature limitation of primary photosynthetic processes in Antarctic lichens Umbilicaria Antarctica and Xanthoria elegans . Polar Biology 31: 4751.CrossRefGoogle Scholar
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: 709720.CrossRefGoogle Scholar
Beck, A., Kasalicky, T. & Rambold, G. (2002) Myco-photobiontal selection in a Mediterranean cryptogam community with Fulgensia fulgida . New Phytologist 153: 317326.CrossRefGoogle Scholar
Blaha, J., Baloch, E. & Grube, M. (2006) High photobiont diversity in symbioses of the euryoecious lichen Lecanora rupicola (Lecanoraceae, Ascomycota). Biological Journal of the Linnean Society 88: 283293.CrossRefGoogle Scholar
Broady, P. & Weinstein, R. N. (1998) Algae, lichens and fungi in La Gorce Mountains, Antarctica. Antarctic Science 10: 376385.CrossRefGoogle Scholar
Casano, L. M., del Campo, E. M., García-Breijo, F. J., Reig-Armiñana, J., Gasulla, F., del Hoyo, A., Guéra, 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.CrossRefGoogle ScholarPubMed
Castresana, J. (2000) Selection of conserved blocks from multiple alignments for their use in phylogenetic analysis. Molecular Biology and Evolution 17: 540552.CrossRefGoogle ScholarPubMed
Clement, M., Posada, D. & Crandall, K. A. (2000) TCS: a computer program to estimate gene genealogies. Molecular Ecology 9: 16571660.CrossRefGoogle ScholarPubMed
Convey, P. & McInnes, S. J. (2005) Exceptional Tardigrade-dominated ecosystem in Ellsworth Land, Antarctica. Ecology 86: 519527.CrossRefGoogle Scholar
Domaschke, S., Fernández Mendoza, F., García, M. A., Martín, M. P. & Printzen, C. (2012) Low genetic diversity in Antarctic populations of the lichen-forming ascomycete Cetraria aculeata and its photobiont. Polar Research 31: 17353.CrossRefGoogle Scholar
Doran, P. T., Priscu, J. C., Lyons, W. B., Walsch, J. E., Fountain, A. G., McKnight, D. M., Moorhead, D. L., Virginia, R. A., Wall, D. H., Clow, G. D. et al. (2002) Antarctic climate cooling and terrestrial ecosystem response. Nature 415: 517520.CrossRefGoogle ScholarPubMed
Ettl, H. & Gärtner, G. (1995) Syllabus der Boden-, Luft- und Flechtenalgen. Stuttgart: Gustav Fischer.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: 12081232.CrossRefGoogle ScholarPubMed
Friedl, T. (1989) Systematik und Biologie von Trebouxia (Microthamniales, Chlorophyta) als Phycobiont der Parmeliaceae (Lichenisierte Ascomyceten). Ph.D. thesis, University of Bayreuth.Google Scholar
Green, T. G. A. (2009) Lichens in arctic, antarctic and alpine ecosystems. Rundgespräche der Kommission für Ökologie, Ökologische Rolle der Flechten. 36: 4565.Google Scholar
Green, T. G. A., Schroeter, B. & Sancho, L. G. (1999) Plant life in Antarctica. In Handbook of Functional Plant Ecology (Pugnaire, F. I. & Valladares, F., eds): 495543. New York, Basel: Marcel Dekker Inc. Google Scholar
Green, T. G. A., Schroeter, B. & Sancho, L. (2007) Plant life in Antarctica. In Functional Plant Ecology, 2nd Edn. (Pugnaire, F. I. & Valladares, F., eds): 389433. Boca Raton, Florida: CRC Press.CrossRefGoogle Scholar
Green, T. G. A., Sancho, L. G., Türk, R., Seppelt, R. D. & Hogg, I. D. (2011) High diversity of lichens at 84°S, Queen Maud Mountains, suggests preglacial survival of species in the Ross Sea region, Antarctica. Polar Biology 34: 12111220.CrossRefGoogle Scholar
Guzow-Krzeminska, B. (2006) Photobiont flexibility in the lichen Protoparmeliopsis muralis as revealed by ITS rDNA analyses. Lichenologist 38: 469476.CrossRefGoogle Scholar
Hauck, M., Helms, G. & Friedl, T. (2007) Photobiont selectivity in the lichens Hypogymnia physodes and Lecanora conizeaoides . Lichenologist 39: 195204.CrossRefGoogle Scholar
Helms, G. W. F. (2003) Taxonomy and symbiosis in associations of Physciaceae and Trebouxia. Ph.D. thesis, Georg-August Universität, Göttingen.Google Scholar
Hertel, H. (1984) Über saxicole, lecideoide Flechten der Subantarktis. Beih . Nova Hedwigia 79: 399499.Google Scholar
Hertel, H. (2007) Notes on and records of Southern Hemisphere lecideoid lichens. Bibliotheca Lichenologica 95: 267296.Google Scholar
Hildreth, K. C. & Ahmadjian, V. (1981) A study of Trebouxia and Pseudotrebouxia isolates from different lichens. Lichenologist 13: 6586.CrossRefGoogle Scholar
Honegger, R. (1996) Morphogenesis. In Lichen Biology (Nash, T. H. III, ed.): 6587. Cambridge: Cambridge University Press.Google Scholar
Huelsenbeck, J. P. & Ronquist, F. (2001) MRBAYES: Bayesian inference of phylogenetic trees. Bioinformatics 17: 754755.CrossRefGoogle ScholarPubMed
Kappen, L. (1993) Plant activity under snow and ice, with particular reference to lichens. Arctic 46: 297302.CrossRefGoogle Scholar
Kappen, L. (2000) Some aspects of the great success of lichens in Antarctica. Antarctic Science 12: 314324.CrossRefGoogle Scholar
Kappen, L. & Valladares, F. (2007) Opportunistic growth and desiccation tolerance: the ecological success of poikilohydrous autothrophs. In Functional Plant Ecology (Pugnaire, F. I. & Valladares, F., eds): 766. Boca Raton, Florida: CRC Press.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
Lange, O. L., Kilian, E. & Ziegler, H. (1986) Water vapor uptake and photosynthesis of lichens: performance differences in species with green and blue-green algae as phycobiont. Oecologia 71: 104110.CrossRefGoogle Scholar
Librado, P. & Rozas, J. (2009) DnaSP v.5 A software for comprehensive analysis of DNA polymorphism data. Bioinformatics 15: 14511452.CrossRefGoogle Scholar
McKay, C. P., Nienow, J. A., Meyer, M. A. & Friedmann, E. I. (1993) Continuous nanoclimate data (1985–1988) from the Ross Desert (McMurdo Dry Valleys) cryptoendolithic microbial ecosystem. In Antarctic Research Series, Vol. 61: Antarctic Meteorology and Climatology: Studies Based on Automatic Weather Stations (Bromwich, D. H. and Stearns, C. R., eds): 201207. Washington, DC: American Geophysical Union.CrossRefGoogle Scholar
Monaghan, A. J. & Bromwich, D. H. (2008) Advances in describing recent Antarctic climate variability. Bulletin of the American Meteorological Society 9: 12951306.CrossRefGoogle Scholar
Nelsen, M. P. & Gargas, A. (2009) Symbiont flexibility in Thamnolia vermicularis (Pertusariales: Icmadophilaceae). Bryologist 112: 404417.CrossRefGoogle 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 ScholarPubMed
Øvstedal, D. O. & Lewis Smith, R. I. (2001) Lichens of Antarctica and South Georgia: A Guide to Their Identification and Ecology. Cambridge: Cambridge University Press.Google Scholar
Pannewitz, S., Green, T. G. A., Maysek, K., Schlensog, M., Seppelt, R., Sancho, L. G., Türk, R. & Schröter, B. (2005) Photosynthetic responses of three common mosses from continental Antarctica. Antarctic Science 17: 341352.CrossRefGoogle Scholar
Pannewitz, S., Green, T. G. A., Schlensog, M., Seppelt, R., Sancho, L. & Schroeter, B. (2006) Photosynthetic performance of Xanthoria mawsonii C. W. Dodge in coastal habitats, Ross Sea region, continental Antarctica. Lichenologist 38: 6781.CrossRefGoogle Scholar
Peat, H. J., Clarke, A. & Convey, P. (2007) Diversity and biogeography of the Antarctic flora. Journal of Biogeography 34: 132146.CrossRefGoogle Scholar
Peksa, O. & Škaloud, P. (2011) Do photobionts influence the ecology of lichens? A case study of environmental preferences in symbiotic green alga Asterochloris (Trebouxiophyceae). Molecular Ecology 20: 39363948.CrossRefGoogle ScholarPubMed
Piercey-Normore, M. D. (2006) The lichen-forming ascomycete Evernia mesomorpha associates with multiple genotypes of Trebouxia jamesii . New Phytologist 169: 331344.CrossRefGoogle ScholarPubMed
Piercey-Normore, M. D. & DePriest, P. T. (2001) Algal switching among lichen symbioses. American Journal of Botany 88: 14901498.CrossRefGoogle ScholarPubMed
Posada, D. & Crandall, K. A. (1998) Modeltest: testing the model of DNA substitution. Bioinformatics 14: 817818.CrossRefGoogle ScholarPubMed
Posada, D. & Crandall, K. A. (2001) Selecting models of nucleotide substitution: an application to Human Immunodeficiency Virus 1 (HIV-1). Molecular Biology and Evolution 18: 897906.CrossRefGoogle ScholarPubMed
Rambold, G., Friedl, T. & Beck, A. (1998) Photobionts in lichens: possible indicators of phylogenetic relationships? Bryologist 101: 392397.CrossRefGoogle Scholar
Reijmer, C. H. & van den Broeke, M. R. (2001) Moisture source of precipitation in Western Dronning Maud Land, Antarctica. Antarctic Science 13: 210220.CrossRefGoogle Scholar
Rodriguez, F., Oliver, J. L., Marin, A. & Medina, J. R. (1990) The general stochastic model of nucleotide substitution. Journal of Theoretical Biology 142: 485501.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: 12091217.CrossRefGoogle ScholarPubMed
Ruprecht, U., Lumbsch, H. T., Brunauer, G., Green, T. G. A. & Türk, R. (2010) Diversity of Lecidea (Lecideaceae, Ascomycota) species revealed by molecular data and morphological characters. Antarctic Science 22: 721726.CrossRefGoogle Scholar
Ruprecht, U., Lumbsch, H. T., Brunauer, G., Green, T. G. A. & Türk, R. (2012) Insights into the diversity of Lecanoraceae (Lecanorales, Ascomyceta) in continental Antarctica (Ross Sea region). Nova Hedwigia 94: 287306.CrossRefGoogle Scholar
Seppelt, R. D., Nimis, P. L. & Castello, M. (1998) The genus Sarcogyne (Acarosporaceae) in Antarctica. Lichenologist 30: 249258.CrossRefGoogle Scholar
Simpson, A. L. & Cooper, A. F. (2002) Geochemistry of the Darwin Glacier region granitoids, southern Victoria Land. Antarctic Science 14: 425426.CrossRefGoogle Scholar
Stickley, C. E., Pike, J., Leventer, A., Dunbar, R., Domack, E. W., Brachfeld, S., Manley, P. & McClennan, C. (2005) Deglacial ocean and climate seasonality in laminated diatom sediments, Mac.Robertson Shelf, Antarctica. Palaeogeography, Palaeoclimatology, Palaeoecology 227: 290310.CrossRefGoogle Scholar
Swofford, D. L. (2003) PAUP*. Phylogenetic Analysis Using Parsimony (*and Other Methods). Sunderland, Massachusetts: Sinauer Associates.Google Scholar
Tschermak-Woess, E. (1988) The algal partner. In CRC Handbook of Lichenology, Vol. I. (Galun, M., ed.): 3992. Boca Raton, Florida: CRC Press.Google Scholar
Thompson, J. D., Higgins, D. G. & Gibson, T. J. (1994) CLUSTAL W: improving the sensitivity of progressive sequence alignment through sequence weighting, position-specific gap penalties and weight matrix choice. Nucleic Acids Research 22: 46734680.CrossRefGoogle ScholarPubMed
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 95: 821830.CrossRefGoogle Scholar
White, T. J., Bruns, T. D., Lee, S. B. & Taylor, J. W. (1990) Amplification and direct sequencing of fungal ribosomal genes for phylogenies. In PCR Protocols: A Guide to Methods and Applications (Innis, M. A., Gelfand, D. H., Sninsky, J. J. & White, T. J., eds): 315322. San Diego: Academic Press.Google Scholar
Wirtz, N., Lumbsch, H. T., Green, T. G. A., Türk, R., Pintado, A., Sancho, L. & Schroeter, B. (2003) Lichen fungi have low cyanobionts selectivity in maritime Antarcica. New Phytologist 160: 177183.CrossRefGoogle Scholar
Wornik, S. & Grube, M. (2010) Joint dispersal does not imply maintenance of partnerships in lichen symbioses. Microbial Ecology 59: 150157.CrossRefGoogle Scholar
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.CrossRefGoogle ScholarPubMed
Zahlbruckner, A. (1925) Catalogus Lichenum Universalis. Vol III. Leipzig: Gebrüder Borntraeger.Google Scholar