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A preliminary survey of lichen associated eukaryotes using pyrosequencing

Published online by Cambridge University Press:  12 December 2011

Scott T. BATES ,
Donna BERG-LYONS ,
Christian L. LAUBER ,
William A. WALTERS ,
Rob KNIGHT  and
Noah FIERER
Scott T. BATES
Affiliation:
Cooperative Institute for Research in Environmental Sciences, University of Colorado, Boulder, Colorado 80309, USA. Email: scott.bates@colorado.edu
Donna BERG-LYONS
Affiliation:
Cooperative Institute for Research in Environmental Sciences, University of Colorado, Boulder, Colorado 80309, USA. Email: scott.bates@colorado.edu
Christian L. LAUBER
Affiliation:
Cooperative Institute for Research in Environmental Sciences, University of Colorado, Boulder, Colorado 80309, USA. Email: scott.bates@colorado.edu
William A. WALTERS
Affiliation:
Department of Cellular, Molecular, and Developmental Biology, University of Colorado, Boulder, Colorado 80309, USA.
Rob KNIGHT
Affiliation:
Department of Chemistry and Biochemistry, University of Colorado, Boulder, Colorado 80309 and Howard Hughes Medical Institute, Boulder, Colorado 80309, USA.
Noah FIERER
Affiliation:
Cooperative Institute for Research in Environmental Sciences, University of Colorado, Boulder, Colorado 80309, USA. Email: scott.bates@colorado.edu Department of Ecology and Evolutionary Biology, University of Colorado, Boulder, Colorado 80309, USA.
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Abstract

Although various eukaryotic organisms, such as arthropods, endolichenic/lichenicolous fungi, and nematodes, have been isolated from lichens, the diversity and structure of eukaryotic communities associated with lichen thalli has not been well studied. In addressing this knowledge gap, we used bar-coded pyrosequencing of 18S rRNA genes to survey eukaryotes associated with thalli of three different lichen species. In addition to revealing an expected high abundance of lichen biont-related 18S genes, sequences recovered in our survey showed non-biont fungi from the Ascomycota also have a substantial presence in these thalli. Our samples additionally harboured fungi representing phyla (Blastocladiomycota, Chytridiomycota) that have not been isolated previously from lichens; however, their very low abundance indicates an incidental presence. The recovery of Alveolata, Metazoa, and Rhizaria sequences, along with recent work revealing the considerable bacterial diversity in these same samples, suggests lichens function as minute ecosystems in addition to being symbiotic organisms.

Keywords

Ascomycotabacteriaendolichenic/lichenicolous fungiinvertebrates
Type
Research Article
Information
The Lichenologist , Volume 44 , Issue 1 , January 2012 , pp. 137 - 146
Copyright
Copyright © British Lichen Society 2011

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References

Altschul, S. F., Madden, T. J., 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.Google Scholar
Arnold, A. E., Miądlikowska, J., Higgins, K. L., Sarvate, S. D., Gugger, P., Way, A., Hofstetter, V., Kauff, F. & Lutzoni, F. (2009) A phylogenetic estimation of trophic transition networks for ascomycetous fungi: are lichens cradles of symbiotrophic fungal diversification? Systematic Biology 58: 283–297.Google Scholar
Bartels, P. J. & Nelson, D. R. (2007) An evaluation of species richness estimators for tardigrades in the Great Smoky Mountains National Park. Journal of Limnology 66 (Supplement 1): 104–110.Google Scholar
Bates, S. T., Cropsey, G. W. G., Caporaso, J. G., Knight, R. & Fierer, N. (2011) Bacterial communities associated with the lichen symbiosis. Applied and Environmental Microbiology 77: 1309–1314.Google Scholar
Caporaso, J. G., Kuczynski, J., Stombaugh, J., Bittinger, K., Bushman, F. D., Costello, E. K., Fierer, N., Gonzalez Peña, A., Goodrich, J. K., Gordon, J. I. et al. (2010) QIIME allows integration and analysis of high-throughput community sequencing data. Nature Methods 7: 335–336.CrossRefGoogle Scholar
Cardinale, M., Vieira de Castro, J. Jr., Müller, H., Berg, G. & Grube, M. (2008) In situ analysis of the bacterial community associated with the reindeer lichen Cladonia arbuscula reveals predominance of Alphaproteobacteria. FEMS Microbiology Ecology 66: 63–71.Google Scholar
Engelbrektson, A., Kunin, V., Wrighton, K. C., Zvenigorodsky, N., Chen, F., Ochman, H. & Hugenholtz, P. (2010) Experimental factors affecting PCR-based estimates of microbial species richness and evenness. ISME Journal 4: 642–647.Google Scholar
Farrar, J. F. (1976) The lichen as an ecosystem: observation and experiment. In Lichenology: Progress and Problems (Brown, D. H., Hawksworth, D. L. & Bailey, R.H., eds): 385–406. London: Academic Press.Google Scholar
Fierer, N., Hamady, M., Lauber, C. L. & Knight, R. (2008) The influence of sex, handedness, and washing on the diversity of hand surface bacteria. Proceedings of the National Academy of Sciences 105: 17994–17999.CrossRefGoogle ScholarPubMed
Fuhrman, J. A. (2009) Microbial community structure and its functional implications. Nature 459: 193–199.Google Scholar
Gerson, U. (1973) Lichen-arthropod associations. Lichenologist 5: 434–443.Google Scholar
Girlanda, M., Isocrono, D., Bianco, C. & Luppi-Mosca, A. M. (1997) Two foliose lichens as microfungal ecological niches. Mycologia 89: 531–536.Google Scholar
Grandjean, F. (1950) Sur deux espèces du genre Dometorina n. g. et les mœurs de D. plantivaga (Berl.) (Acariens, Oribates). Bulletin de la Société Zoologique de France 75: 224–242.Google Scholar
Grube, M. & Berg, G. (2009) Microbial consortia of bacteria and fungi with focus on the lichen symbiosis. Fungal Biology Reviews 23: 72–85.Google Scholar
Grube, M., Cardinale, M., Vieira de Castro, J. Jr., Müller, H. & Berg, G. (2009) Species-specific structural and functional diversity of bacterial communities in lichen symbioses. ISME Journal 3: 1105–1115.CrossRefGoogle Scholar
Henckel, P. A. & Yuzhakova, L. A. (1936) On the role of Azotobacter in the lichen symbiosis. Izvestiia Permskogo Biologicheskogo Nauchno-Issle-dovatel'skogo Instituta 10: 9–10.Google Scholar
Hodkinson, B. & Lutzoni, F. (2009) A microbiotic survey of lichen-associated bacteria reveals a new lineage from the Rhizobiales. Symbiosis 49: 163–180.Google Scholar
Hodkinson, B. P., Gottel, N. R., Schadt, C. W. & Lutzoni, F. (in press) Photoautotrophic symbiont and geography are major factors affecting highly structured and diverse bacterial communities in the lichen microbiome. Environmental Microbiology.Google Scholar
Honegger, R. (2000) Great discoveries in bryology and lichenology: Simon Schwendener (1829–1919) and the dual hypothesis in lichens. Bryologist 103: 307–713.Google Scholar
Lawrey, J. D. & Diederich, P. (2003) Lichenicolous fungi: interactions, evolution, and biodiversity. Bryologist 106: 80–120.Google Scholar
Lawrey, J. D., Binder, M., Diederich, P., Molina, M. C., Sikaroodi, M. & Ertz, D. (2007) Phylogenetic diversity of lichen-associated homobasidiomycetes. Molecular Phylogenetics and Evolution 44: 778–789.Google Scholar
Liu, Z., Lozupone, C., Hamady, M., Bushman, F. D. & Knight, R. (2007) Short pyrosequencing reads suffice for accurate microbial community analysis. Nucleic Acids Research 35: e120.CrossRefGoogle Scholar
Meininger, C. A. & Spatt, P. D. (1988) Variations of tardigrade assemblages in dust-impacted Arctic mosses. Artic and Alpine Research 20: 24–30.Google Scholar
Nash, T. H. III (ed.). (2008) Lichen Biology, 2nd edn. Cambridge: Cambridge University Press.Google Scholar
Pfister, D. H & Liftik, M. E. (1995) Arthrobotrys anamorphs from Orbilia auricolor. Mycologia 87: 684–688.Google Scholar
Schwendener, S. (1868) Ueber die Beziehungen zwischen Algen und Flechtengonidien. Botanische Zeitung 26: 289–292.Google Scholar
Stubbs, C. S. (1989) Patterns of distribution and abundance of corticolous lichens and their invertebrate associates on Quercus rubra in Maine. Bryologist 92: 453–460.Google Scholar
Suryanarayanan, T. S., Thirunavukkarasu, N., Hariharan, G. N. & Balaji, P. (2005) Occurrence of non-obligate microfungi inside lichen thalli. Sydowia 57: 120–130.Google Scholar
Thompson, M. G. (1958) Egg sampling for the western hemlock looper. Forestry Chronicle 34: 248–256.Google Scholar
U'Ren, J., Lutzoni, F., Miądlikowska, J. & Arnold, A. E. (2010) Community analysis reveals close affinities between endophytic and endolichenic fungi in mosses and lichens. Microbial Ecology 60: 340–353.Google Scholar
Wilson, C. G. & Sherman, P.W. (2010) Anciently asexual bdelloid rotifers escape lethal fungal parasites by drying up and blowing away. Science 327: 574–576.Google Scholar