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Biology  2013 

Antarctic Epilithic Lichens as Niches for Black Meristematic Fungi

DOI: 10.3390/biology2020784

Keywords: black meristematic fungi, Dothideomycetes, Eurotiomycetes, lichen-associated fungi, phylogeny

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Abstract:

Sixteen epilithic lichen samples (13 species), collected from seven locations in Northern and Southern Victoria Land in Antarctica, were investigated for the presence of black fungi. Thirteen fungal strains isolated were studied by both morphological and molecular methods. Nuclear ribosomal 18S gene sequences were used together with the most similar published and unpublished sequences of fungi from other sources, to reconstruct an ML tree. Most of the studied fungi could be grouped together with described or still unnamed rock-inhabiting species in lichen dominated Antarctic cryptoendolithic communities. At the edge of life, epilithic lichens withdraw inside the airspaces of rocks to find conditions still compatible with life; this study provides evidence, for the first time, that the same microbes associated to epilithic thalli also have the same fate and chose endolithic life. These results support the concept of lichens being complex symbiotic systems, which offer attractive and sheltered habitats for other microbes.

References

[1]  Plemenita?, A.; Gunde-Cimerman, N. Cellular responses in the halophilic black yeast Hortaea werneckii to high environmental salinity. In Adaptation to Life at High Salt Concentrations in Archaea, Bacteria, and Eukarya; Gunde-Cimerman, N., Oren, A., Plemenita?, A., Eds.; Springer: Dordrecht, The Netherlands, 2005; pp. 455–470.
[2]  Baker, B.J.; Lutz, M.A.; Dawson, S.C.; Bond, P.L.; Banfield, J.F. Metabolically active eukaryotic communities in extremely acidic mine drainage. Appl. Environ. Microbiol. 2004, 70, 6264–6271, doi:10.1128/AEM.70.10.6264-6271.2004.
[3]  Selbmann, L.; Egidi, E.; Isola, D.; Onofri, S.; Zucconi, Z.; de Hoog, G.S.; Chinaglia, S.; Testa, L.; Tosi, S.; Balestrazzi, A.; et al. Biodiversity, evolution and adaptation of fungi in extreme environments. Plant Biosyst. 2012, 147, doi:10.1080/11263504.2012.753134.
[4]  Isola, D.; Selbmann, L.; de Hoog, G.S.; Fenice, M.; Onofri, S.; Prenafeta-Boldú, F.X.; Zucconi, L. Isolation and screening of black fungi as degraders of volatile aromatic hydrocarbons. Mycopathologia 2013, doi:10.1007/s11046-013-9635-2.
[5]  Staley, J.T.; Palmer, F.; Adams, J.B. Microcolonial fungi: Common inhabitants on desert rocks? Science 1982, 215, 1093–1095.
[6]  Ruibal, C.; Gonzalo, P.; Bills, G.F. Isolation and characterization of melanized fungi from limestone formations in Mallorca. Mycol. Progress 2005, 4, 23–38, doi:10.1007/s11557-006-0107-7.
[7]  Selbmann, L.; de Hoog, G.S.; Mazzaglia, A.; Friedmann, E.I.; Onofri, S. Fungi at the edge of life: Cryptoendolithic black fungi from Antarctic desert. Stud. Mycol. 2005, 51, 1–32.
[8]  Sert, H.B.; Sümbül, H.; Sterflinger, K. Microcolonial fungi from antique marbles in Perge/Side/Termessos (Antalya/Turkey). Antonie Leeuwenhoek 2007, 91, 217–227, doi:10.1007/s10482-006-9111-9.
[9]  Sert, H.B.; Sümbül, H.; Sterflinger, K. Sarcinomyces sideticae, a new black yeast from historical marble monuments in Side (Antalya, Turkey). Bot. J. Linnean Soc. 2007, 154, 373–380, doi:10.1111/j.1095-8339.2007.00658.x.
[10]  Sert, H.B.; Sümbül, H.; Sterflinger, K. A new species of Capnobotryella from monument surfaces. Mycol. Res. 2007, 111, 1235–1241, doi:10.1016/j.mycres.2007.06.011.
[11]  Marvasi, M.; Donnarumma, F.; Frandi, A.; Mastromei, G.; Sterflinger, K.; Tiano, P.; Perito, B. Black microcolonial fungi as deteriogens of two famous marble statues in Florence, Italy. Int. Biodeterior. Biodegrad. 2012, 68, 36–44, doi:10.1016/j.ibiod.2011.10.011.
[12]  Zucconi, L.; Gagliardi, M.; Isola, D.; Onofri, S.; Andaloro, M.C.; Pelosi, C.; Pogliani, P.; Selbmann, L. Biodeteriorigenous agents dwelling the wall paintings of the Holy Saviour’s Cave (Vallerano, Italy). Int. Biodeterior. Biodegrad. 2012, 70, 40–46, doi:10.1016/j.ibiod.2011.11.018.
[13]  Onofri, S.; Selbmann, L.; Zucconi, L.; de Hoog, G.S.; de los Rios, A.; Ruisi, S.; Grube, M. Fungal associations at the cold edge of life. In Algae and Cyanobacteria in Extreme Environments; Seckbach, J., Ed.; Springer: Dordrecht, The Netherlands, 2007; pp. 735–757.
[14]  Harutyunyan, S.; Muggia, L.; Grube, M. Black fungi in lichens from seasonally arid habitats. Stud. Mycol. 2008, 61, 83–90, doi:10.3114/sim.2008.61.08.
[15]  Sterflinger, K. Black Yeast and Meristematic Fungi: Ecology, Diversity and Identification. In The Yeast Handbook. Biodiversity and Ecophysiology of Yeasts; Péter, G., Rosa, C., Eds.; Springer: Berlin, Germany, 2006; pp. 501–514.
[16]  Nienow, J.A.; Friedmann, E.I. Terrestrial Litophytic (Rock) Communities. In Antarctic Microbiology; Friedmann, E.I., Ed.; Wiley-Liss: New York, NY, USA, 1993; pp. 343–412.
[17]  Selbmann, L.; de Hoog, G.S.; Gerrits van den Ende, A.H.G.; Ruibal, C.; de Leo, F.; Zucconi, L.; Isola, D.; Ruisi, S.; Onofri, S. Drought meets acid: Three new genera in a Dothidealean clade of extremotolerant fungi. Stud. Mycol. 2008, 61, 1–20, doi:10.3114/sim.2008.61.01.
[18]  Friedmann, E.I. Endolithic microorganisms in the Antarctic Cold Desert. Science 1982, 215, 1045–1053.
[19]  De la Torre, J.R.; Goebel, B.M.; Friedmann, E.I.; Pace, N.R. Microbial diversity of cryptoendolithic communities from the McMurdo Dry Valleys, Antarctica. Appl. Environ. Microbiol. 2003, 215, 3858–3867.
[20]  Selbmann, L.; Zucconi, L.; Ruisi, S.; Grube, M.; Cardinale, M.; Onofri, S. Culturable bacteria associated with Antarctic lichens: Affiliation and psychrotolerance. Polar Biol. 2010, 33, 71–83, doi:10.1007/s00300-009-0686-2.
[21]  Cardinale, M.; Vieira de Castro, J., Jr.; Müller, H.; Berg, G.; Grube, M. In situ analysis of the bacterial community associated with the reindeer lichen Cladonia arbuscula reveals predominance of Alphaproteobacteria. FEMS Microbiol. Ecol. 2008, 66, 63–71, doi:10.1111/j.1574-6941.2008.00546.x.
[22]  Grube, M.; Cardinale, M.; Vieira de Castro, J.; Müller, H.; Berg, G. Species-specificstructural and functional diversity of bacterial communitiesin lichen symbioses. ISME J. 2009, 3, 1105–1115, doi:10.1038/ismej.2009.63.
[23]  Hodkinson, B.; Lutzoni, F. A microbiotic survey of lichen-associated bacteria reveals a new lineage from the Rhizobiales. Symbiosis 2009, 49, 163–180, doi:10.1007/s13199-009-0049-3.
[24]  Bates, S.T.; Cropsey, G.W.G.; Caporaso, J.G.; Knight, R.; Fierer, N. Bacterial communities associated with the lichen symbiosis. Appl. Environ. Microbiol. 2011, 77, 1309–1314, doi:10.1128/AEM.02257-10.
[25]  Grube, M.; Berg, G. Microbial consortia of bacteria and fungi with focus on the lichen symbiosis. Fungal Biol. Rev. 2009, 23, 72–85, doi:10.1016/j.fbr.2009.10.001.
[26]  Lawrey, J.D.; Diederich, P. Lichenicolous fungi: Interactions, evolution, and biodiversity. Bryologist 2003, 106, 80–120, doi:10.1639/0007-2745(2003)106[0080:LFIEAB]2.0.CO;2.
[27]  Lawrey, J.D.; Binder, M.; Diederich, P.; Molina, M.C.; Sikaroodi, M.; Ertz, D. Phylogenetic diversity of lichen-associated homobasidiomycetes. Mol. Phylogenetics Evol. 2007, 44, 778–789, doi:10.1016/j.ympev.2006.12.023.
[28]  Girlanda, M.; Isocrono, D.; Bianco, C.; Luppi-Mosca, A.M. Two foliose lichens as microfungal ecological niches. Mycologia 1997, 89, 531–536, doi:10.2307/3760987.
[29]  Suryanarayanan, T.S.; Thirunavukkarasu, N.; Hariharan, G.N.; Balaji, P. Occurrence of non-obligate microfungi inside lichen thalli. Sydowia 2005, 57, 120–130.
[30]  U’Ren, J.; Lutzoni, F.; Miadlikowska, J.; Arnold, A.E. Community analysis reveals close affinities between endophytic and endolichenic fungi in mosses and lichens. Microb. Ecol. 2010, 60, 340–353, doi:10.1007/s00248-010-9698-2.
[31]  Bates, S.T.; Berg-Lyons, D.; Lauber, C.L.; Walters, W.A.; Knight, R.; Fierer, N. A preliminary survey of lichen associated eukaryotes using Pyrosequencing. Lichenologist 2012, 44, 137–146, doi:10.1017/S0024282911000648.
[32]  Farrar, J.F. The Lichen as an Ecosystem: Observation and Experiment. In Lichenology: Progress and Problems; Brown, D.H., Hawksworth, D.L., Bailey, R.H., Eds.; Academic Press: London, UK, 1976; pp. 385–406.
[33]  Castello, M. Lichens of the Terra Nova Bay area, Northern Victoria Land (Continental Antactica). Stud. Geobot. 2003, 22, 3–54.
[34]  White, T.J.; Bruns, T.; Lee, S.B.; Taylor, J.W. Amplification and Direct Sequencing of Fungal Ribosomal RNA Genes for Phylogenetics. In PCR Protocols, a Guide to Methods and Applications; Innis, M.A., Gelfand, D.H., Sninsky, J.J., White, T.J., Eds.; Academic Press: San Diego, CA, USA, 1990; pp. 315–322.
[35]  Thompson, J.D.; Gibson, T.J.; Plewniak, F.; Jeanmougin, F.; Higgins, D.G. The ClustalX windows interface: Flexible strategies for multiple sequence alignment aided by quality analysis tools. Nucleic Acids Res. 1997, 24, 4876–4882.
[36]  Tamura, K.; Peterson, D.; Peterson, N.; Stecher, G.; Nei, M.; Kumar, S. MEGA5: Molecular evolutionary genetics analysis using maximum likelihood, evolutionary distance, and maximum parsimony methods. Mol. Biol. Evol. 2011, 28, 2731–2739, doi:10.1093/molbev/msr121.
[37]  Felsenstein, J. Confidence limits on phylogenies: An approach using the bootstrap. Evolution 1985, 40, 783–791, doi:10.2307/2408678.
[38]  Van Uden, N. Temperature profiles of yeasts. Adv. Microbiol. Physiol. 1984, 25, 195–251, doi:10.1016/S0065-2911(08)60293-3.
[39]  Schoch, C.L.; Shoemaker, R.A.; Seifert, K.A.; Hambleton, S.; Spatafora, J.W.; Crous, P.W. A multigene phylogeny of the Dothideomycetes using four nuclear loci. Mycologia 2006, 98, 1041–1052, doi:10.3852/mycologia.98.6.1041.
[40]  Ruibal, C.; Gueidan, C.; Selbmann, L.; Gorbushina, A.A.; Crous, P.W.; Groenewald, J.Z.; Muggia, L.; Grube, M.; Isola, D.; Schoch, C.L.; et al. Phylogeny of rock-inhabiting fungi related to Dothideomycetes. Stud. Mycol. 2009, 64, 123–133, doi:10.3114/sim.2009.64.06.
[41]  Tsuneda, A.; Hambleton, S.; Currah, R.S. The anamorph genus Knufia and its phylogenetically allied species in Coniosporium, Sarcinomyces, and Phaeococcomyces. Botany 2011, 89, 523–536, doi:10.1139/b11-041.
[42]  Muggia, L.; Hafellner, J.; Wirtz, N.; Hawksworth, D.L.; Grube, M. The sterile microfilamentous lichenized fungi Cystocoleus ebeneus and Racodium rupestre are relatives of plant pathogens and clinically important dothidealean fungi. Mycol. Res. 2008, 112, 50–56, doi:10.1016/j.mycres.2007.08.025.
[43]  Onofri, S.; Pagano, S.; Zucconi, L.; Tosi, S. Friedmanniomyces endolithicus (Fungi, Hyphomycetes), anam.-gen. and sp.nov., from continental Antarctica. Nova Hedwig. 1999, 68, 175–181.
[44]  Onofri, S.; Anastasi, A.; Del Frate, G.; di Piazza, S.; Garnero, N.; Guglielminetti, M.; Isola, D.; Panno, L.; Ripa, C.; Selbmann, L.; et al. Biodiversity of rock, beach and water fungi in Italy. Plant Biosyst. 2011, 45, 978–987.
[45]  Prenafeta-Boldú, F.X.; Summerbell, R.C.; de Hoog, G.S. Fungi growing on aromatic hydrocarbons: Biotechnology’s unexpected encounter with biohazard. FEMS Microbiol. Rev. 2006, 30, 109–130, doi:10.1111/j.1574-6976.2005.00007.x.
[46]  Diederich, P.; Lawrey, J.D. New lichenicolous, muscicolous, corticolous and lignicolous taxa of Burgoa s. l. and Marchandiomyces s. l. (anamorphic Basidiomycota), a new genus for Omphalina foliacea, and a catalogue and a key to the non-lichenized, bulbilliferous basidiomycetes. Mycol. Progress 2007, 6, 61–80, doi:10.1007/s11557-007-0523-3.
[47]  Muggia, L.; Gueidan, C.; Knudsen, K.; Perlmutter, G.; Grube, M. The lichen connections of black fungi. Mycopathologia 2012, doi:10.1007/s11046-012-9598-8.
[48]  Selbmann, L.; Isola, D.; Egidi, E.; Zucconi, L.; Gueidan, C.; de Hoog, G.S.; Onofri, S. Rock inhabiting fungi: Saxomyces gen. nov. and four new species from the Alps. Fungal Diver. 2013. in press.
[49]  Gorbushina, A.A.; Beck, A.; Shulte, A. Microcolonial rock inhabiting fungi and lichen photobionts: Evidence for mutualistic interactions. Mycol. Res. 2005, 109, 1288–1296, doi:10.1017/S0953756205003631.
[50]  Brunauer, G.; Blaha, J.; Hager, A.; Turk, R.; Stocker-Worgotter, E.; Grube, M. An isolated lichenicolous fungus forms lichenoid structures when co-cultured with various coccoid algae. Symbiosis 2007, 44, 127–136.
[51]  Gueidan, C.; Ruibal, C.; de Hoog, G.S.; Gorbushina, A.; Untereiner, W.A.; Lutzoni, F. A rock-inhabiting ancestor for mutualistic and pathogen-rich fungal lineages. Stud. Mycol. 2008, 61, 111–119, doi:10.3114/sim.2008.61.11.

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