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Photobiont selectivity for lichens and evidence for a possible glacial refugium in the Ross Sea Region, Antarctica

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Abstract

Lichens are a symbiosis consisting of heterotrophic, fungal (mycobiont) and photosynthetic algal or cyanobacterial (photobiont) components. We examined photobiont sequences from lichens in the Ross Sea Region of Antarctica using the internal transcribed spacer region of ribosomal DNA and tested the hypothesis that lichens from this extreme environment would demonstrate low selectivity in their choice of photobionts. Sequence data from three targeted lichen species (Buellia frigida, Umbilicaria aprina and Umbilicaria decussata) showed that all three were associated with a common algal haplotype (an unnamed Trebouxia species) which was present in all taxa and at all sites, suggesting lower selectivity. However, there was also association with unique, local photobionts as well as evidence for species-specific selection. For example, the cosmopolitan U. decussata was associated with two photobiont species, Trebouxia jamesii and an unnamed species. The most commonly collected lichen (B. frigida) had its highest photobiont haplotype diversity in the Dry Valley region, which may have served as a refugium during glacial periods. We conclude that even in these extreme environments, photobiont selectivity still has an influence on the successful colonisation of lichens. However, the level of selectivity is variable among species and may be related to the ability of some (e.g. B. frigida) to colonise a wider range of habitats.

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References

  • Ahmadjian V (1993) The lichen symbiosis. Wiley, Chichester

    Google Scholar 

  • Ahmadjian V (2004) Trebouxia: reflections on a perplexing and controversial lichen photobiont. In: Seckbach J (ed) Symbiosis. Springer, Berlin, pp 373–383

    Chapter  Google Scholar 

  • Aoki M, Nakano T, Kanda H, Deguchi H (1998) Photobionts isolated from Antarctic lichens. J Mar Biotechnol 6:39–43

    Google Scholar 

  • Beck A, Kasalicky T, Rambold G (2002) Myco-photobiontal selection in a mediterranean cryptogam community with Fulgensia fulgida. New Phytol 153:317–326

    Article  Google Scholar 

  • Blaha J, Baloch E, Grube M (2006) High photobiont diversity associated with the euryoecious lichen-forming ascomycete Lecanora rupicola (Lecanoraceae, Ascomycota). Biol J Linn Soc 88:283–293

    Article  Google Scholar 

  • Chomczynski P, Rymaszewski M (2006) Alkaline polyethylene glycol-based method for direct PCR from bacteria, eukaryotic tissue samples, and whole blood. Biotechniques 40:454–458

    Article  PubMed  CAS  Google Scholar 

  • Chown SL, Lee JE, Hughes KA et al (2012) Challenges to the Future Conservation of the Antarctic. Science 337:158–159

    Article  PubMed  CAS  Google Scholar 

  • Cowan DA, Ah Tow L (2004) Endangered Antarctic environments. Annu Rev Microbiol 58:649–690

    Article  PubMed  CAS  Google Scholar 

  • Cowan DA, Chown SL, Convey P, Tuffin M, Hughes K, Pointing S, Vincent WF (2011) Non-indigenous microorganisms in the Antarctic: assessing the risks. Trends Microbiol 19:540–548

    Article  PubMed  CAS  Google Scholar 

  • Dahlkild A, Kallersjo M, Lohtander K, Tehler A (2001) Photobiont diversity in the Physciaceae (Lecanorales). Bryologist 104:527–536

    Article  Google Scholar 

  • Des Los Rios A, Sancho LG, Grube M, Wierzchos J, Ascaso C (2005) Endolithic growth of two Lecidea lichens in granite from continental Antarctica detected by molecular and microscopy techniques. New Phytol 165:181–190

    Article  Google Scholar 

  • Domaschke S, Fernãndez-Mendoza F, Garcia MA, Martãn MP, Printzen C (2012) Low genetic diversity in Antarctic populations of the lichen forming ascomycete Cetraria aculeata and its photobiont. Polar Res 31:17353

  • Drummond AJ, Ashton B, Buxton S, Cheung M, Cooper A, Duran C, Field M, Heled J, Kearse M, Markowitz S, Moir R, Stones-Havas S, Sturrock S, Thierer T, Wilson A (2011) Geneious v5.4. http://www.geneious.com/. Accessed 3 June 2011

  • Fernãndez-Mendoza F, Domaschke S, Garcãa MA, Jordan P, Martãn MP, Printzen C (2011) Population structure of mycobionts and photobionts of the widespread lichen Cetraria aculeata. Mol Ecol 20:1208–1232

    Article  PubMed  Google Scholar 

  • Freifelder D, Better M (1982) Dialysis of small samples in agarose gels. Anal Biochem 123:83–85

    Article  PubMed  CAS  Google 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. Mol Phylogenet Evol 14:342–352

    Article  PubMed  CAS  Google Scholar 

  • Green TGA, Sancho LG, Pintado A, Schroeter B (2011) Functional and spatial pressures on terrestrial vegetation in Antarctica forced by global warming. Polar Biol 34:1643–1656

    Article  Google Scholar 

  • Greuter W, McNeill J, Hawksworth DL et al (2000) Report on botanical nomenclature: Saint Louis 1999. XVI international botanical congress, Saint Louis: nomenclature section, 26–30 July 1999. Englera. Botanischer Garten und Botanisches Museum, Berlin-Dahlem, pp 3–253

  • Guzow-Krzeminska B (2006) Photobiont flexibility in the lichen Protoparmeliopsis muralis as revealed by ITS rDNA analyses. Lichenologist 38:469–476

    Article  Google Scholar 

  • Hauck M, Helms G, Friedl T (2007) Photobiont selectivity in the epiphytic lichens Hypogymnia physodes and Lecanora conizaeoide. Lichenologist 39:195–204

    Article  Google 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

    Article  Google Scholar 

  • Honegger R (2009) Lichen-forming fungi and their photobionts. In: Deising HB (ed) Plant relationships, 2nd edn. Springer, Berlin, pp 305–333

    Google Scholar 

  • Jukes TH, Cantor CR (1969) Evolution of protein molecules. In: Munro HN (ed) Mammalian protein metabolism, vol 3. Academic, New York, pp 21–132

    Google Scholar 

  • Jump AS, Marchant R, Penuelas J (2009) Environmental change and the option value of genetic diversity. Trends Plant Sci 14:51–58

    Article  PubMed  CAS  Google Scholar 

  • Librado P, Rozas J (2009) DnaSP v5: a software for comprehensive analysis of DNA polymorphism data. Bioinformatics 25:1451–1452

    Article  PubMed  CAS  Google Scholar 

  • Lindsay DC (1978) The role of lichens in Antarctic ecosystems. Bryologist 81:268–276

    Article  Google Scholar 

  • McGaughran A, Hogg ID, Stevens MI (2008) Patterns of population genetic structure for springtails and mites in southern Victoria Land, Antarctica. Mol Phylogenet Evol 46:606–618

    Article  PubMed  CAS  Google Scholar 

  • Nash TH (2007) Lichen biology. Cambridge University Press, Cambridge

    Google Scholar 

  • Nelsen MP, Gargas A (2009) Symbiont flexibility in Thamnolia vermicularis (Pertusariales: Icmadophilaceae). Bryologist 112:404–417

    Article  Google Scholar 

  • Nyati S, Scherrer S, Honegger R (2004) Photobiont diversity in the genus Xanthoria. In: Randlane T, Saag A (eds) Book of abstracts of the 5th IAL symposium, lichens in focus. Tartu University Press, p 65

  • Peksa O, Škaloud P (2011) Do photobionts influence the ecology of lichens? A case study of environmental preferences in symbiotic green alga Asterochloris (Trebouxiophyceae). Mol Ecol 20:3936–3948

    Article  PubMed  Google Scholar 

  • Pérez-Ortega S, Ortiz-Álvarez R, Green TGA, de los Rios A (2012) Lichen myco- and photo-biont diversity and their relationships at the edge of life (McMurdo Dry Valleys, Antarctica). FEMS Microbiol Ecol 82:429–448

    Article  PubMed  Google Scholar 

  • Piercy-Normore MD, DePriest PT (2001) Algal switching among lichen symbioses. Am J Bot 88:1490–1498

    Article  Google Scholar 

  • Posada D (2008) jModelTest: phylogenetic model averaging. Mol Biol Evol 25:1253–1256

    Article  PubMed  CAS  Google Scholar 

  • Rambaut A (2008) FigTree v111: tree figure drawing tool. Available http://treebioedacuk/software/figtree/. Accessed Feb–April 2012

  • Romeike J, Friedl T, Helms G, Ott S (2002) Genetic diversity of algal and fungal partners in four species of Umbilicaria (Lichenised Ascomycetes) along a transect of the Antarctic Peninsula. Mol Biol Evol 19:1209–1217

    Article  PubMed  CAS  Google Scholar 

  • Ruprecht U, Lumbsch HT, Brunauer G, Green TGA, Turk R (2012) Insights into the diversity of Lecanoraceae (Lecanorales, Ascomycota) in continental Antarctica (Ross Sea region). Nova Hedwigia 94:287–306

    Google Scholar 

  • Sanders WB (2005) Observing microscopic phases of lichen life cycles on transparent substrata placed in situ. Lichenologist 37:373–382

    Article  Google Scholar 

  • Seymour FA, Crittenden PD, Dyer P (2005) Sex in the extremes: lichen forming fungi. Mycologist 19:51–58

    Article  Google Scholar 

  • Stevens MI, Hogg ID (2003) Long-term isolation and recent range expansion from glacial refugia revealed for the endemic springtail Gomphiocephalus hodgsoni from Victoria Land, Antarctica. Mol Ecol 12:2357–2369

    Article  PubMed  CAS  Google Scholar 

  • Stevens MI, Frati F, Mcgaughran A, Spinsanti G, Hogg ID (2007) Phylogeographic structure suggests multiple glacial refugia in northern Victoria Land for the endemic Antarctic springtail Desoria klovstadi (Collembola, Isotomidae). Zool Scr 36:201–212

    Article  Google Scholar 

  • Swofford DL (2002) PAUP* phylogenetic analysis using parsimony (*and other methods) version 4. Sinauer Associates, Sunderland

    Google Scholar 

  • Tamura K, Nei M (1993) Estimation of the number of nucleotide substitutions in the control region of mitochondrial DNA in humans and chimpanzees. Mol Biol Evol 10:512–526

    PubMed  CAS  Google Scholar 

  • Wall DH, Lyons WB, Convey P, Howard-Williams C, Quesada A, Vincent WF (2011) Long term ecosystem networks to record change: an international imperative. Antarct Sci 23:209

    Article  Google Scholar 

  • White TJ, Bruns T, Lee S, Taylor J (1990) Amplification and direct sequencing of fungal ribosomal RNA genes for phylogenetics. In: Innis MA, Gelfand GH, Sninsky JJ, White TJ (eds) PCR protocols: a guide to methods and applications, vol 18. Academic Press, pp 315–322

  • Wirtz N, Lumbsch HT, Green TGA, Türk R, Pintado A, Sancho L, Schroeter B (2003) Lichen fungi have low cyanobiont selectivity in maritime Antarctica. New Phytol 160:177–183

    Article  Google Scholar 

  • Yahr R, Vilgalys R, Depriest PT (2004) Strong fungal specificity and selectivity for algal symbionts in Florida scrub Cladonia lichens. Mol Ecol 13:3367–3378

    Article  PubMed  CAS  Google Scholar 

  • Zwickl DJ (2006) Genetic algorithm approaches for the phylogenetic analysis of large biological sequence datasets under the maximum likelihood criterion. PhD dissertation, The University of Texas at Austin

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Acknowledgments

We are extremely grateful for the valuable and constructive comments provided by three anonymous reviewers. We also thank C. Gemmill for advice on PAUP* and phylogenetic analyses, and R. Cursons and O. Patty for helpful advice in the laboratory. Antarctica New Zealand provided logistic support and Helicopters New Zealand, FRST grant UOWX0505 and the University of Waikato provided financial support. C. Beard, L. Sancho, J. Banks, S. Fitzsimmons, R. Seppelt, R. Türk and Thorsten Lumbsch, Beata Guzow-Krzeminska provided valuable help in the field and laboratory, respectively. Lichen samples were transported into New Zealand under MAF permit number 2007032514.

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Jones, T.C., Hogg, I.D., Wilkins, R.J. et al. Photobiont selectivity for lichens and evidence for a possible glacial refugium in the Ross Sea Region, Antarctica. Polar Biol 36, 767–774 (2013). https://doi.org/10.1007/s00300-013-1295-7

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