Abstract
We surveyed the distribution and diversity of fungi present in moss fairy rings from the South Shetland Islands. In the different islands accessed, the mosses Bartramia patens, Brachythecium austrosalebrosum, Bryum pseudotriquetrum, Pohlia nutans, Polytrichastrum alpinum, Sanionia uncinata, Syntrichia magellanica, and Syntrichia saxicola were infected with fairy rings. Among them, B. patens, B. pseudotriquetrum, P. nutans, P. alpinum, S. magellanica, and S. saxicola were reported for the first time as species susceptible to infection with fairy rings. From five different fairy ring moss species sampled, we isolated 40 fungal taxa identified as belonging to the genera Alpinaria, Cadophora, Cladosporium, Chalara, Cosmospora, Drechmera, Glarea, Gyoerffyella, Hymenoscyphus, Juncaceicola, Melanodiplodia, Mortierella, Mycosysmbioses, Pseudogymnoascus, Phoma, and Velucrispora. A high level of fungal richness was associated with the infected mosses, and Mortierella was the dominant genus. However, most of the fungi were present as minor components of the fungal assemblages. Among the mosses studied, S. uncinata harboured the greatest fungal diversity. Some fungal taxa present have previously been reported as opportunistic plant pathogens, including Cladosporium sp. and Phoma herbarum. We hypothesize that some of the fungi recovered from fairy ring mosses might represent secondary opportunistic pathogens and contribute to the reduced natural defences of the infected mosses, thus accelerating the dissemination of the pathogenic fairy rings in the Antarctic Peninsula. In addition, the presence of fairy rings on previously unreported moss species suggests that the disease may be becoming more widespread in Antarctica.
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References
Altschul SF, Madden TL, Schäffer AA et al (1997) Gapped BLAST and PSI-BLAST: a new generation of protein database search programs. Nucleic Acids Res 25:3389–3402
Amesbury MJ, Roland TP, Royles J et al (2017) Widespread biological response to rapid warming on the Antarctic Peninsula. Current Biol 27:1616–1622
Anderson LE (1954) Hoyer's Solution as a rapid mounting medium for bryophytes. Bryologist 57:242–244
Arenz BE, Blanchette RA (2011) Distribution and abundance of soil fungi in Antarctica at sites on the Peninsula, Ross Sea Region and McMurdo Dry Valleys. Soil Biol Biochem 43:308–315
Bardou P, Mariette J, Escudié F et al (2014) An interactive Venn diagram viewer. BMC Bioinformatics 15:293
Bennett A, Ponder MM, Garcia-Diaz J (2018) Phoma infections: classification, potential food sources, and their clinical impact. Microorganisms 6:58
Bradner JR, Sidhu RK, Yee B, Skotnick ML et al (2000) A new microfungal isolate, Embellisia sp., associated with the Antarctic moss Bryum argenteum. Polar Biol 23:730–732
Bridge PD, Newsham KK (2009) Soil fungal community composition at Mars Oasis, a southern maritime Antarctic site, assessed by PCR amplification and cloning. Fungal Ecol 2:66–74
Carvalho CR, Santiago IF, Coelho LC et al (2019) Fungi associated with plants and lichens of Antarctica. In: Rosa LH (ed) Fungi of Antarctica. Springer Nature, Cham, pp 165–199
Convey P (2017) Antarctic ecosystems. In: Reference module in life sciences. Elsevier, https://doi.org/10.1016/B978-0-12-809633-8.02182-8
Davey ML, Currah RS (2006a) Interactions between mosses (Bryophyta) and fungi. Can J Bot 84:1509–1519
Davey ML, Currah RS (2006b) Interactions between mosses (Bryophyta) and fungi. Botany 84:1509–1519
de Menezes GCA, Alves RP, de Carvalho VF et al (2019) Study of physiological and enzymatic properties and characterization of pathogenic activity of a fungus isolated from moss Sanionia uncinata (Hedw.) Loeske in Antarctica. Polar Biol 42:783–792
Döbbeler P (1997) Biodiversity of bryophilous ascomycetes. Biodiv Conserv 6:721–738
Döbbler P (2002) Microniches occupied by bryophillous ascomycetes. Nova Hedwigia 75:275–306
Fenton JHC (1983) Concentric fungal rings in Antarctic moss communities. Trans Brit Mycol Soc 80:415–420
Furbino LE, Godinho VM, Santiago IF et al (2014) Diversity patterns, ecology and biological activities of fungal communities associated with the endemic macroalgae across the Antarctic. Microbial Ecol 67:775–787
Gardes M, Bruns TD (1996) Community structure of ectomycorrhizal fungi in a Pinus muricata forest: above and below ground views. Can J Bot 74:1572–1583
Godinho VM, Furbino LE, Santiago IF et al (2013) Diversity and bioprospecting of fungal communities associated with endemic and cold-adapted macroalgae in Antarctica. ISME J 7:1434–1451
Gomes EC, Godinho VM, Silva DA et al (2018) Cultivable fungi present in Antarctic soils: taxonomy, phylogeny, diversity, and bioprospecting of antiparasitic and herbicidal metabolites. Extremophiles 22:381–393
Gonçalves VN, Vaz ABM, Rosa CA et al (2012) Diversity and distribution of fungal communities in lakes of Antarctica. FEMS Microbiol Ecol 82:459–471
Gonçalves VN, Carvalho CR, Johann S et al (2015) Antibacterial, antifungal and antiprotozoal activities of fungal communities present in different substrates from Antarctica. Polar Biol 38:1143–1152
Hammer Ø, Harper DAT, Ryan PD (2001) PAST: paleontological statistics software package for education and data analysis. Palaeontol Electrc 4:9
Hawksworth DL (1973) Thyronectria antarctica (Speg.) Seeler var. hyperantarctica D. Hawksw. Var. nov. Bull Br Antarct Sury 32:51–53
Kauserud H, Mathiesen C, Ohlson M (2008) High diversity of fungi associated with living parts of boreal forest bryophytes. Botany 86:1326–1333
Krishnan A, Convey P, Gonzalez-Rocha G et al (2016) Production of extracellular hydrolase enzymes by fungi from King George Island. Polar Biol 39:65–76
Kirk PM, Cannon PF, Minter DW et al (2008) Dictionary of the fungi, 10th edn. CAB International, Wallingford
Last FT, Mason PA, Ingleby K, Fleming LV (1984) Succession of fruitbodies of sheating mycorrhizal fungi with Betula pendula. For Ecol Manag 9:229–234
Li YP, You M, Khan T et al (2011) First report of Phoma herbarum on field pea (Pisum sativum) in Australia. Plant Dis 95:1590–1590
Lian C, Narimatsu M, Nara K, Hogetsu T (2006) Tricholoma matsutake in a natural Pinus densiflora forest: correspondence between above and below ground genets, association with multiple host trees and alteration of existing ectomycorrhizal communities. New Phytol 171:825–836
Longton RE (1973) The occurrence of radial infection patterns in colonies of polar bryophytes. Brit Antarc Sur Bull 32:41–49
Loque CP, Medeiros AO, Pellizzari FM et al (2010) Fungal community associated with marine macroalgae from Antarctica. Polar Biol 33:641–648
Lorch JM, Meteyer CU, Behr JM et al (2011) Experimental infection of bats with Geomyces destructans causes white-nose syndrome. Nature 480:376–378
Lorch JM, Lindner DL, Gargas A et al (2013) A culture-based survey of fungi in soil from bat hibernacula in the eastern United States and its implications for detection of Geomyces destructans, the causal agent of bat white-nose syndrome. Mycologia 105:237–252
Ma L, Cao YH, Cheng MH et al (2013) Phylogenetic diversity of bacterial endophytes of Panax notoginseng with antagonistic characteristics towards pathogens of root-rot disease complex. AntonVan Leeuw Int G J 113:299–312
Mercantini R, Marsella R, Cervellati MC (1989) Keratinophilic fungi isolated from Antarctic soil. Mycopathologia 106:47–52
Miao ZQ, Li SD, Liu XZ et al (2006) The causal microorganisms of Panax notoginseng root rot disease. Sci Agric Sin 39:1371–1378
Minnis AM, Lindner DL (2013) Phylogenetic evaluation of Geomyces and allies reveals no close relatives of Pseudogymnoascus destructans, comb. nov., in bat hibernacula of eastern North America. Fungal Biol 117:638–649
Möller C, Dreyfuss MM (1996) Microfungi from Antarctic lichens, mosses and vascular plants. Mycologia 88:922–933
Ochyra R, Lewis-Smith RI, Bednarek-Ochyra H (2008) The illustrated moss flora of Antarctica. Cambridge University Press, Cambridge
Pawłowska J, Istel L, Gorczak M et al (2017) Psychronectria hyperantarctica, gen. nov., comb. nov., epitypification and phylogenetic position of an Antarctic bryophilous ascomycete. Mycologia 109:601–607
Prather HM, Casanova-Katny A, Clements AF et al (2019) Species-specific effects of passive warming in an Antarctic moss system. R Soc Open Sci 6:190744
Putzke J, Pereira AB (2012) Fungos muscícolas na ilha elefante-Antártica. Cad Pesq Biol 24:155–164
Racovitza A (1959) É tude systematique et biologique des champignons bryophiles. Mém Mus Natl Hist nat Sér B Bot 10:1–288
Rosa LH, Vaz ABM, Caligiorne RB et al (2009) Endophytic fungi associated with the Antarctic grass Deschampsia antarctica Desv. (Poaceae). Polar Biol 32:161–167
Rosa LH, Vieira MLA, Santiago IF et al (2010) Endophytic fungi community associated with the dicotyledonous plant Colobanthus quitensis (Kunth) Bartl. (Caryophyllaceae) in Antarctica. FEMS Microbiol Ecol 73:178–189
Santiago IF, Soares MA, Rosa CA et al (2015) Lichensphere: a protected natural microhabitat of the non-lichenised fungal communities living in extreme environments of Antarctica. Extremophiles 19:1087–1097
Rosa LH, Zani CL, Cantrell CL et al (2019) Fungi in Antarctica: diversity, ecology, effects of climate change, and bioprospection for bioactive compounds. In: Rosa LH (ed) Fungi of Antarctica. Springer Nature, Cham, pp 1–17
Tojo M, West PV, Hoshino T et al (2012) Pythium polare, a new heterothallic oomycete causing brown discolouration of Sanionia uncinata in the Arctic and Antarctic. Fungal Biol 116:756–768
Tokumasu S (1998) Fungal succession on pine needles fallen at different seasons: the succession of surface colonizers. Mycoscience 39:417–423
Torres DE, Rojas-Martínez RI, Zavaleta-Mejía E et al (2017) Cladosporium cladosporioides and Cladosporium pseudocladosporioides as potential new fungal antagonists of Puccinia horiana Henn., the causal agent of chrysanthemum white rust. PLoS ONE 12:e0170782
Tosi S, Casado B, Gerdol R (2002) Fungi isolated from Antarctic mosses. Polar Biol 25:262–268
Turner J, Bindschadler RA, Convey P et al (2009) Antarctic climate change and the environment. Scientific Committee on Antarctic Research, Cambridge
Turner J, Barrand N, Bracegirdle TJ (2014) Antarctic climate change and the environment: an update. Polar Rec 50:237–259
White TJ, Bruns TD, Lee SB (1990) Amplification and direct sequencing of fungal ribosomal RNA genes for phylogenetics. In: Innis NA, Gelfand J, Sninsky J, et al. (eds) PCR protocols: a guide to methods and applications. Academic Press, San Diego, pp 315–322
Wilson JW (1951) Observations on concentric 'fairy rings' in Arctic moss mat. J Ecol 39:407–416
Wynn-Williams DD (1985) Comparative microbiology of moss-peat decomposition on the Scotia Arc and Antarctic Peninsula. In: Siefried WR, Condy PR, Laws RM (eds) Antarctic nutrient cycles and food webs. Springer, Berlin, pp 204–210
Yajima Y, Tojo M, Chen B, Hoshino T (2017) Typhula cf. subvariabilis, new snow mould in Antarctica. Mycology 8:147–152
Yu NH, Kim J, Jeong M et al (2014) Diversity of endophytic fungi associated with bryophyte in the maritime Antarctic (King George Island). Polar Biol 37:27–36
Acknowledgements
This study received financial support from CNPq, PROANTAR, FAPEMIG, Coordenação de Aperfeiçoamento de Pessoal de Nível Superior—Brasil (CAPES), INCT Criosfera 2. P. Convey is supported by NERC core funding to the British Antarctic Survey’s ‘Biodiversity, Evolution and Adaptation’ Team. We are also grateful for the generous support of the Spanish Polar Committee and its staff at Gabriel de Castilla and Juan Carlos I bases. Finally we are grateful for the comments of three anonymous reviewers for suggestions improving this manuscript.
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Rosa, L.H., de Sousa, J.R.P., de Menezes, G.C.A. et al. Opportunistic fungi found in fairy rings are present on different moss species in the Antarctic Peninsula. Polar Biol 43, 587–596 (2020). https://doi.org/10.1007/s00300-020-02663-w
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DOI: https://doi.org/10.1007/s00300-020-02663-w