An arctic community of symbiotic fungi assembled by long-distance dispersers: phylogenetic diversity of ectomycorrhizal basidiomycetes in Svalbard based on soil and sporocarp DNA

Authors

  • József Geml,

    Corresponding author
    1. National Herbarium of the Netherlands, Netherlands Centre for Biodiversity Naturalis, Leiden University, PO Box 9514, Einsteinweg 2, 2300 RA Leiden, The Netherlands
    2. Institute of Arctic Biology, University of Alaska Fairbanks, PO Box 757000, Fairbanks, AK 99775-7000, USA
      József Geml, National Herbarium of the Netherlands, Netherlands Centre for Biodiversity Naturalis, Leiden University, P.O. Box 9514, Einsteinweg 2, 2300 RA Leiden, The Netherlands.
      E-mail: geml@nhn.leidenuniv.nl
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  • Ina Timling,

    1. Institute of Arctic Biology, University of Alaska Fairbanks, PO Box 757000, Fairbanks, AK 99775-7000, USA
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  • Clare H. Robinson,

    1. School of Earth, Atmospheric and Environmental Sciences, The University of Manchester, Williamson Building, Oxford Road, Manchester, M13 9PL, UK
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  • Niall Lennon,

    1. Genome Sequence and Analysis Program, Broad Institute of MIT and Harvard, Cambridge, MA 02141, USA
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  • H. Chad Nusbaum,

    1. Genome Sequence and Analysis Program, Broad Institute of MIT and Harvard, Cambridge, MA 02141, USA
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  • Christian Brochmann,

    1. National Centre for Biosystematics, Natural History Museum, University of Oslo, PO Box 1172 Blindern, NO-0318 Oslo, Norway
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  • Machiel E. Noordeloos,

    1. National Herbarium of the Netherlands, Netherlands Centre for Biodiversity Naturalis, Leiden University, PO Box 9514, Einsteinweg 2, 2300 RA Leiden, The Netherlands
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  • D. Lee Taylor

    1. Institute of Arctic Biology, University of Alaska Fairbanks, PO Box 757000, Fairbanks, AK 99775-7000, USA
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József Geml, National Herbarium of the Netherlands, Netherlands Centre for Biodiversity Naturalis, Leiden University, P.O. Box 9514, Einsteinweg 2, 2300 RA Leiden, The Netherlands.
E-mail: geml@nhn.leidenuniv.nl

Abstract

Aim  Current evidence from temperate studies suggests that ectomycorrhizal (ECM) fungi require overland routes for migration because of their obligate symbiotic associations with woody plants. Despite their key roles in arctic ecosystems, the phylogenetic diversity and phylogeography of arctic ECM fungi remains little known. Here we assess the phylogenetic diversity of ECM communities in an isolated, formerly glaciated, high arctic archipelago, and provide explanations for their phylogeographic origins.

Location  Svalbard.

Methods  We generated and analysed internal transcribed spacer (ITS) nuclear ribosomal DNA sequences from both curated sporocarp collections (from Svalbard) and soil polymerase chain reaction (PCR) clone libraries (from Svalbard and the North American Arctic), compared these with publicly available sequences in GenBank, and estimated the phylogenetic diversity of ECM fungi in Svalbard. In addition, we conducted coalescent analyses to estimate migration rates in selected species.

Results  Despite Svalbard’s geographic isolation and arctic climate, its ECM fungi are surprisingly diverse, with at least 72 non-singleton operational taxonomic units (soil) and 109 phylogroups (soil + sporocarp). The most species-rich genera are Thelephora/Tomentella, Cortinarius and Inocybe, followed by Hebeloma, Russula, Lactarius, Entoloma, Sebacina, Clavulina, Laccaria, Leccinum and Alnicola. Despite the scarcity of available reference data from other arctic regions, the majority of the phylogroups (73.4%) were also found outside Svalbard. At the same time, all putative Svalbard ‘endemics’ were newly sequenced taxa from diverse genera with massive undocumented diversity. Overall, our results support long-distance dispersal more strongly than vicariance and glacial survival. However, because of the high variation in nucleotide substitution rates among fungi, allopatric persistence since the Pliocene, although unlikely, cannot be statistically rejected. Results from the coalescent analyses suggest recent gene flow among different arctic areas.

Main conclusions  Our results indicate numerous recent colonization events and suggest that long-distance, transoceanic dispersal is widespread in arctic ECM fungi, which differs markedly from the currently prevailing view on the dispersal capabilities of ECM fungi. Our molecular evidence indicates that long-distance dispersal has probably played a major role in the phylogeographic history of some ECM fungi in the Northern Hemisphere. Our results may have implications for studies on the biodiversity, ecology and conservation of arctic fungi in general.

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