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

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 conclusionsOur 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.

Recent advances in population genetics of ectomycorrhizal mushroomsRussulaspp.

“…Plants as well as ECM fungi from glacial refugia would be the sources of organisms for these communities. Therefore, measuring the ECM fungal community structure in the Northern Hemisphere can help identify the refugia and better understand species dispersal, species survival, speciation, and the history of ecological niche transitions (Geml et al 2010, 2012). In this aspect, due to their ubiquity in natural ecosystems, species in the genus Russula should be able to provide excellent information from which to understand these issues.…”

Enigmatic Sebacinales

“…Bahram et al (2012) found evidence for host range expansions of local symbionts, including sebacinoids, to distantly related host taxa in exotic Pinus sylvestris plantations in relation to native host trees, Carpinus betulus, Fagus orientalis, and Quercus castaneifolia, in the Hyrcanian forests of Iran. Based on molecular evidence, Geml et al (2012) concluded that longdistance dispersal of some ECM fungi, including Sebacina species in the Northern Hemisphere, may have played a major role in their phylogeographic history. Human-caused introductions of ECMs are common and widespread, and may exceed 200 species (Vellinga et al 2009).…”

The genus Hebeloma in the alpine belt of the Carpathians including two new species

“…In addition to these traditional studies European Arctic-alpine fungal communities have been studied by high throughput sequencing (e.g. Bjorbaekmo et al 2010, Fujiyoshi et al 2011, Lentendu et al 2011, Geml et al 2012, Botnen et al 2014. Also the Arctic region of Greenland has been relatively well studied mycologically (Borgen et al 2006).…”