Abstract
Climate change may alter mycorrhizal communities, which impact ecosystem characteristics such as carbon sequestration processes. These impacts occur at a greater magnitude in Arctic ecosystems, where the climate is warming faster than in lower latitudes. Cassiope tetragona (L.) D. Don is an Arctic plant species in the Ericaceae family with a circumpolar range. C. tetragona has been reported to form ericoid mycorrhizal (ErM) as well as ectomycorrhizal (ECM) symbioses. In this study, the fungal taxa present within roots of C. tetragona plants collected from Svalbard were investigated using DNA metabarcoding. In light of ongoing climate change in the Arctic, the effects of artificial warming by open-top chambers (OTCs) on the fungal root community of C. tetragona were evaluated. We detected only a weak effect of warming by OTCs on the root-associated fungal communities that was masked by the spatial variation between sampling sites. The root fungal community of C. tetragona was dominated by fungal groups in the Basidiomycota traditionally classified as either saprotrophic or ECM symbionts, including the orders Sebacinales and Agaricales and the genera Clavaria, Cortinarius, and Mycena. Only a minor proportion of the operational taxonomic units (OTUs) could be annotated as ErM-forming fungi. This indicates that C. tetragona may be forming mycorrhizal symbioses with typically ECM-forming fungi, although no characteristic ECM root tips were observed. Previous studies have indicated that some saprophytic fungi may also be involved in biotrophic associations, but whether the saprotrophic fungi in the roots of C. tetragona are involved in biotrophic associations remains unclear. The need for more experimental and microscopy-based studies to reveal the nature of the fungal associations in C. tetragona roots is emphasized.
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References
Anisimov O, Vaughan D, Callaghan T (2007) Polar regions (Arctic and Antarctic). In: Parry M, Canziani O, Palutikof J et al (eds) Climate change 2007: impacts, adaptation and vulnerability. Contribution of working group II to the fourth assessment report of the Intergovernmental Panel on Climate Change. Cambridge University Press, Cambridge, pp 653–685
Aronesty E (2013) Comparison of sequencing utility programs. Open Bioinforma J 7:1–8. doi:10.2174/1875036201307010001
Begerow D, Nilsson H, Unterseher M, Maier W (2010) Current state and perspectives of fungal DNA barcoding and rapid identification procedures. Appl Microbiol Biotechnol 87:99–108. doi:10.1007/s00253-010-2585-4
Bellemain E, Carlsen T, Brochmann C et al (2010) ITS as an environmental DNA barcode for fungi: an in silico approach reveals potential PCR biases. BMC Microbiol 10:189. doi:10.1186/1471-2180-10-189
Birkebak JM, Mayor JR, Ryberg KM, Matheny PB (2013) A systematic, morphological and ecological overview of the Clavariaceae (Agaricales). Mycologia 105:896–911. doi:10.3852/12-070
Blaalid R, Carlsen T, Kumar S et al (2012) Changes in the root-associated fungal communities along a primary succession gradient analysed by 454 pyrosequencing. Mol Ecol 21:1897–1908. doi:10.1111/j.1365-294X.2011.05214.x
Blaalid R, Davey ML, Carlsen T et al (2014) Arctic root-associated fungal community composition reflects environmental filtering. Mol Ecol 23:649–659. doi:10.1111/mec.12622
Blok D, Weijers S, Welker JM et al (2015) Deepened winter snow increases stem growth and alters stem δ 13 C and δ 15 N in evergreen dwarf shrub Cassiope tetragona in high-arctic Svalbard tundra. Environ Res Lett 10:44008. doi:10.1088/1748-9326/10/4/044008
Bokhorst S, Huiskes A, Aerts R et al (2013) Variable temperature effects of open top chambers at polar and alpine sites explained by irradiance and snow depth. Glob Chang Biol 19:64–74. doi:10.1111/gcb.12028
Botnen S, Vik U, Carlsen T et al (2014) Low host specificity of root-associated fungi at an Arctic site. Mol Ecol 23:975–985. doi:10.1111/mec.12646
Bougoure DS, Parkin PI, Cairney JWG et al (2007) Diversity of fungi in hair roots of Ericaceae varies along a vegetation gradient. Mol Ecol 16:4624–4636. doi:10.1111/j.1365-294X.2007.03540.x
Buizer B, Weijers S, van Bodegom PM et al (2012) Range shifts and global warming: ecological responses of Empetrum nigrum L. to experimental warming at its northern (high Arctic) and southern (Atlantic) geographical range margin. Environ Res Lett 7:25501. doi:10.1088/1748-9326/7/2/025501
Cairney JWG, Meharg AA (2003) Ericoid mycorrhiza: a partnership that exploits harsh edaphic conditions. Eur J Soil Sci 54:735–740. doi:10.1046/j.1365-2389.2003.00555.x
Caporaso JG, Kuczynski J, Stombaugh J et al (2010) QIIME allows analysis of high-throughput community sequencing data. Nat Methods 7:335–336. doi:10.1038/nmeth0510-335
Clemmensen KE, Michelsen A, Jonasson S, Shaver GR (2006) Increased ectomycorrhizal fungal abundance after long-term fertilization and warming of two arctic tundra ecosystems. New Phytol 171:391–404. doi:10.1111/j.1469-8137.2006.01778.x
Davey ML, Heimdal R, Ohlson M, Kauserud H (2013) Host- and tissue-specificity of moss-associated Galerina and Mycena determined from amplicon pyrosequencing data. Fungal Ecol 6:179–186. doi:10.1016/j.funeco.2013.02.003
Davey M, Blaalid R, Vik U, et al (2015) Primary succession of Bistorta vivipara (L.) Delabre (Polygonaceae) root associated fungi mirrors plant succession in two glacial chronosequences. Environ Microbiol 17:n/a-n/a. doi:10.1111/1462–2920.12770
Deslippe JR, Hartmann M, Simard SW, Mohn WW (2012) Long-term warming alters the composition of Arctic soil microbial communities. FEMS Microbiol Ecol 82:303–315. doi:10.1111/j.1574-6941.2012.01350.x
Edgar RC (2010) Search and clustering orders of magnitude faster than BLAST. Bioinformatics 26:2460–2461. doi:10.1093/bioinformatics/btq461
Elvebakk A (1994) A survey of the plant associations and alliances from Svalbard. J Veg Sci 5:791–802
Elvebakk A (1999) Bioclimatic delimitation and subdivision of the Arctic. In: Nordal I, Razzhivin VY (eds) The species concept in the High North—a panarctic flora initiative. Norwegian Academy of Science and Letters, Oslo, pp 81–112
Englander L, Hull RJ (1980) Reciprocal transfer of nutrients between Ericaceous plants and a Clavaria sp. New Phytol 84:661–667
Feng S, Ho CH, Hu Q et al (2012) Evaluating observed and projected future climate changes for the Arctic using the Köppen-Trewartha climate classification. Clim Dyn 38:1359–1373. doi:10.1007/s00382-011-1020-6
Fujimura KE, Egger KN (2012) Host plant and environment influence community assembly of High Arctic root-associated fungal communities. Fungal Ecol 5:409–418. doi:10.1016/j.funeco.2011.12.010
Fujimura KE, Egger KN, Henry GH (2008) The effect of experimental warming on the root-associated fungal community of Salix arctica. Isme J 2:105–114. doi:10.1038/ismej.2007.89
Gardes M, Bruns TD (1993) ITS primers with enhanced specificity for basidiomycetes—application to the identification of mycorrhizae and rusts. Mol Ecol 2:113–118
Geml J, Morgado L, Semenova T et al (2015) Long-term warming alters richness and composition of taxonomic and functional groups of Arctic fungi. FEMS Microbiol Ecol 91:1–13
Grau O, Rautio P, Heikkinen J et al (2010) An ericoid shrub plays a dual role in recruiting both pines and their fungal symbionts along primary succession gradients. Oikos 119:1727–1734. doi:10.1111/j.1600-0706.2010.18511.x
Grelet GA, Johnson D, Vralstad T et al (2010) New insights into the mycorrhizal Rhizoscyphus ericae aggregate: spatial structure and co-colonization of ectomycorrhizal and ericoid roots. New Phytol 188:210–222. doi:10.1111/j.1469-8137.2010.03560.x
Hambleton S, Sigler L (2005) Meliniomyces, a new anamorph genus for root-associated fungi with phylogenetic affinities to Rhizoscyphus ericae (=Hymenoscyphus ericae), Leotiomycetes. Stud Mycol 53:1–27
Henry GHR, Molau U (1997) Tundra plants and climate change: the International Tundra Experiment (ITEX). Glob Chang Biol 3:1–9. doi:10.1111/j.1365-2486.1997.gcb132.x
Hill MO, Gauch HG Jr (1980) Detrended correspondence analysis: an improved ordination technique. Vegetatio 42:47–58
Hobbie JE, Hobbie EA (2006) 15N in symbiotic fungi and plants estimates nitrogen. Ecology 87:816–822
Ihrmark K, Bödeker ITM, Cruz-Martinez K et al (2012) New primers to amplify the fungal ITS2 region—evaluation by 454-sequencing of artificial and natural communities. FEMS Microbiol Ecol 82:666–677. doi:10.1111/j.1574-6941.2012.01437.x
Katenin A (1964) Mycorrhizae of Arctic plants. Probl Sev 8:148–154
Katenin A (1972) Mycorrhiza in tundra plants of north-east of European part of the USSR. In: Tikhomirov B (ed) The vegetation of the far north of the USSR and its utilization. Botanical Institute Ameni BL Komorova, Leningrad, pp 1–140
Kauserud H, Mathiesen C, Ohlson M (2008) High diversity of fungi associated with living parts of boreal forest bryophytes. Botany 86:1326–1333. doi:10.1139/B08-102
Kohn LM, Stasovski E (1990) The mycorrhizal status of plants at Alexandra Fjord, Ellesmere Island, Canada, a High Arctic site. Mycologia 82:23–35
Kõljalg U, Nilsson RH, Abarenkov K et al (2013) Towards a unified paradigm for sequence-based identification of fungi. Mol Ecol 22:5271–5277. doi:10.1111/mec.12481
Kruskal JB (1964a) Nonmetric multidimensional scaling: a numerical method. Psychometrika 29:115–129
Kruskal JB (1964b) Multidimensional scaling by optimizing goodness of fit to a nonmetric hypothesis. Psychometrika 29:1–27. doi:10.1007/BF02289565
Kühdorf K, Münzenberger B, Begerow D et al (2014a) Sebacina sp. is a mycorrhizal partner of Comarostaphylis arbutoides (Ericaceae). Mycol Prog 13:733–744. doi:10.1007/s11557-013-0956-9
Kühdorf K, Münzenberger B, Begerow D, et al (2014b) Leotia cf. lubrica forms arbutoid mycorrhiza with Comarostaphylis arbutoides (Ericaceae). Mycorrhiza 109–120. doi:10.1007/s00572–014–0590-7
Lindahl BD, Nilsson RH, Tedersoo L et al (2013) Fungal community analysis by high-throughput sequencing of amplified markers—a user’s guide. New Phytol 199:288–299
Liu H-Y, Økland T, Halvorsen R (2008) Gradient analyses of forests ground vegetation and it’s relationship to environmental variables in five subtropical forest areas, S and SW China. Sommerfeltia 32:3–196
Mallik AU, Wdowiak JV, Cooper EJ (2011) Growth and reproductive responses of Cassiope tetragona, a circumpolar evergreen shrub, to experimentally delayed snowmelt. Arct Antarct Alp Res 43:404–409. doi:10.1657/1938-4246-43.3.404
Marion G, Henry G, Freckman D et al (1997) Open-top designs for manipulating field temperature in high-latitude ecosystems. Glob Chang Biol 3:20–32. doi:10.1111/j.1365-2486.1997.gcb136.x
Martos F, Dulormne M, Pailler T et al (2009) Independent recruitment of saprotrophic fungi as mycorrhizal partners by tropical achlorophyllous orchids. New Phytol 184:668–681. doi:10.1111/j.1469-8137.2009.02987.x
Michelsen A, Schmidt IK, Jonasson S et al (1996) Leaf N-15 abundance of subarctic plants provides field evidence that ericoid, ectomycorrhizal and non- and arbuscular mycorrhizal species access different sources of soil nitrogen. Oecologia 105:53–63. doi:10.1007/bf00328791
Miller O Jr (1982) Higher fungi in Alaskan subarctic tundra and taiga plant communities. In: Laursen G, Ammirati J (eds) Arctic and alpine mycology, vol 1. University of Washington Press, Seattle, pp 123–149
Miller O Jr, Laursen G (1974) Belowground fungal biomass on U.S. Tundra Biome sites at Barrow, Alaska. In: Holding A, Heal O, MacLean S, Flanagan P (eds) Soil organisms and decomposition in tundra. Swedish IBP Commitee, Stockholm, pp 151–158
Minchin PR (1987) An evaluation of the relative robustness of techniques for ecological ordination. Vegetatio 69:89–107. doi:10.1007/BF00038690
Morgado LN, Semenova TA, Welker JM et al (2015) Summer temperature increase has distinct effects on the ectomycorrhizal fungal communities of moist tussock and dry tundra in Arctic Alaska. Glob Chang Biol 21:959–972. doi:10.1111/gcb.12716
Mundra S, Bahram M, Tedersoo L et al (2015a) Temporal variation of Bistorta vivipara-associated ectomycorrhizal fungal communities in the High Arctic. Mol Ecol 24:6289–6302. doi:10.1111/mec.13458
Mundra S, Halvorsen R, Kauserud H, et al (2015b) Arctic fungal communities associated with roots of Bistorta vivipara do not respond to the same fine-scale edaphic gradients as the aboveground vegetation. New Phytol 205:1587–1597
Mundra S, Halvorsen R, Kauserud H et al (2016) Ectomycorrhizal and saprotrophic fungi respond differently to long-term experimentally increased snow depth in the High Arctic. Microbiology 5:856–869. doi:10.1002/mbo3.375
Murray MG, Thompson WF (1980) Rapid isolation of high molecular weight plant DNA. Nucleic Acids Res 8:4321–4325
Newsham KK, Upson R, Read DJ (2009) Mycorrhizas and dark septate root endophytes in polar regions. Fungal Ecol 2:10–20
Nguyen NH, Smith D, Peay K, Kennedy P (2014) Parsing ecological signal from noise in next generation amplicon sequencing. New Phytol 205:1389–1393. doi:10.1111/nph.12923
Oberwinkler F, Riess K, Bauer R et al (2013) Enigmatic Sebacinales. Mycol Prog 12:1–27. doi:10.1007/s11557-012-0880-4
Oberwinkler F, Riess K, Bauer R, Garnica S (2014) Morphology and molecules: the Sebacinales, a case study. Mycol Prog 13:445–470. doi:10.1007/s11557-014-0983-1
Ogura-Tsujita Y, Gebauer G, Hashimoto T et al (2009) Evidence for novel and specialized mycorrhizal parasitism: the orchid Gastrodia confusa gains carbon from saprotrophic Mycena. Proc Biol Sci 276:761–767. doi:10.1098/rspb.2008.1225
Økland RH (1990) Vegetation ecology: theory, methods and applications with reference to Fennoscandia. In: Sommerfeltia Supplementary, 1st edn. pp 1–233
Økland RH (1999) On the variation explained by ordination and constrained ordination axes. J Veg Sci 10:131–136. doi:10.2307/3237168
Økland RH, Eilertsen O (1993) Vegetation-environment relationships of boreal coniferous forests in the Solhomfjell area. Gjerstand, S Norway Sommerfeltia:1–254
Oksanen J, Blanchet FG, Friendly M, et al (2017) vegan: Community Ecology Package.
Park EJ, Lee WY (2013) In vitro symbiotic germination of myco-heterotrophic Gastrodia elata by Mycena species. Plant Biotechnol Rep 7:185–191. doi:10.1007/s11816-012-0248-x
Perotto S, Girlanda M, Martino E (2002) Ericoid mycorrhizal fungi: some new perspectives on old acquaintances. Plant Soil 244:41–53. doi:10.1023/A:1020289401610
Peters C, Basinger JF, Kaminskyj SGW (2011) Endorhizal fungi associated with vascular plants on Truelove Lowland, Devon Island, Nunavut, Canadian High Arctic. Arctic, Antarct Alp Res 43:73–81
Peterson JH, Læssøe T (2014) MycoKey 4.1. www.mycokey.com. Accessed January 2016.
Read DJ (1996) The structure and function of the ericoid mycorrhizal root. Ann Bot 77:365–374. doi:10.1006/anbo.1996.0044
Rønning O (1996) The flora of Svalbard. Norsk Polarinstitutt
Schadt CW, Rosling A (2015) Comment on “Global diversity and geography of soil fungi”. Science 348:1438–1438. doi:10.1126/science.aaa426980-
Selosse MA, Setaro S, Glatard F et al (2007) Sebacinales are common mycorrhizal associates of Ericaceae. New Phytol 174:864–878. doi:10.1111/j.1469-8137.2007.02064.x
Semenchuk PR, Elberling B, Cooper EJ (2013) Snow cover and extreme winter warming events control flower abundance of some, but not all species in High Arctic Svalbard. Ecol Evol 3:2586–2599. doi:10.1002/ece3.648
Semenova TA, Morgado LN, Welker JM et al (2015) Long-term experimental warming alters community composition of ascomycetes in Alaskan moist and dry arctic tundra. Mol Ecol 24:424–437. doi:10.1111/mec.13045
Seviour RJ, Willing RR, Chilvers GA (1973) Basidiocarps associated with ericoid mycorrhizas. New Phytol 72:381–385. doi:10.1111/j.1469-8137.1973.tb02045.x
Smith SE, Read D (2008) Mycorrhizal symbiosis, Third edn. Academic Press
Strelkova A (1956) Mycorrhizae of plants of tundra and taiga in Taimyr. Bot Zhurnal Leningr 41:1161–1168
Sturm M, Racine C, Tape K (2001) Increasing shrub abundance in the Arctic. Nature 411:546–547. doi:10.1038/35079180
Stutz R (1972) Survey of mycorrhizal plants. In: Bliss L (ed) Devon Island IPB Project: High Arctic ecosystem. University of Alberta, Edmonton, pp 214–216
Sweet SK, Griffin KL, Steltzer H et al (2015) Greater deciduous shrub abundance extends tundra peak season and increases modeled net CO2 uptake. Glob Chang Biol 21:2394–2409. doi:10.1111/gcb.12852
Tarnocai C, Canadell JC, Schuur EAG et al (2009) Soil organic carbon pools in the northern circumpolar permafrost region. Glob Biogeochem Cycles 23:1–11. doi:10.1029/2008GB003327
Tejesvi MV, Sauvola T, Pirttilä AM, Ruotsalainen AL (2013) Neighboring Deschampsia flexuosa and Trientalis europaea harbor contrasting root fungal endophytic communities. Mycorrhiza 23:1–10. doi:10.1007/s00572-012-0444-0
Timling I, Walker DA, Nusbaum C et al (2014) Rich and cold: diversity, distribution and drivers of fungal communities in patterned-ground ecosystems of the North American Arctic. Mol Ecol 23:3258–3272
Treu R, Laursen GA, Stephenson SL et al (1996) Mycorrhizae from Denali National Park and Preserve, Alaska. Mycorrhiza 6:21–29
Ugland KI, Gray JS, Ellingsen KE (2003) The species-accumulation curve and estimation of species richness. J Anim Ecol 72:888–897
Van Son TC, Halvorsen R (2014) Multiple parallel ordinations: the importance of choice of ordination method and weighting of species abundance data. Sommerfeltia 37:1–27. doi:10.2478/som-2014-0001
Villarreal-Ruiz L, Neri-Luna C, Anderson IC, Alexander IJ (2012) In vitro interactions between ectomycorrhizal fungi and ericaceous plants. Symbiosis 56:67–75. doi:10.1007/s13199-012-0161-7
Vohnik M, Panek M, Fehrer J, Selosse M-A (2016) Experimental evidence of ericoid mycorrhizal potential within Serendipitaceae (Sebacinales). Mycorrhiza 26:831–846. doi:10.1007/s00572-016-0717-0
Vrålstad T (2004) Are ericoid and ectomycorrhizal fungi part of a common guild? New Phytol 164:7–10
Walker JF, Aldrich-Wolfe L, Riffel A et al (2011) Diverse helotiales associated with the roots of three species of arctic ericaceae provide no evidence for host specificity. New Phytol 191:515–527. doi:10.1111/j.1469-8137.2011.03703.x
Weiss M, Sykorova Z, Garnica S et al (2011) Sebacinales everywhere: previously overlooked ubiquitous fungal endophytes. PLoS One. doi:10.1371/journal.pone.0016793
White TJ, Bruns S, Lee S, Taylor J (1990) Amplification and direct sequencing of fungal ribosomal RNA genes for phylogenetics. In: PCR Protocols: A Guide to Methods and Applications. pp 315–322
Zhang T, Xiang H-B, Zhang Y-Q et al (2013) Molecular analysis of fungal diversity associated with three bryophyte species in the Fildes Region, King George Island, maritime Antarctica. Extremophiles 17:757–765. doi:10.1007/s00792-013-0558-0
Acknowledgements
The University of Oslo and UNIS are acknowledged for the financial support and for providing lab facilities, while the Research Council of Norway and Svalbard Science Forum are acknowledged for the travel support. Kevin Newsham, David Read, and Ulrik Sochting kindly provided microscopy pictures of Cassiope plant roots.
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Fig S1
Global nonmetric multidimensional scaling (GNMDS) and detrended correspondence analysis (DCA) ordinations for operational taxonomic unit (OTU) – sample matrices based on (a, b) raw read abundances (c, d) raw read abundances converted to presence/absence, and (e, f) rarefied read abundances converted to presence/absence. The DCA ordinations show clear tongue effects yet confirm the pattern seen in the GNMDS ordinations. Samples from the same location group together and the samples are not separated by warming treatment on either of the first two axes. (GIF 48 kb)
Fig S2
Micrograph of a Cassiope tetragona hair-root tip taken at 400 x magnification with a Leica DMRB microscope mounted with a Leica DFC420 digital camera. Root sample is unstained, mounted in water, and was collected from Isdammen, Svalbard in August 2014. There is a notable lack of mantle or Hartig net. Micrograph by Kelsey Lorberau. (PNG 489 kb)
Fig S3
Three Cassiope tetragona root micrographs collected from Endalen, Svalbard and stained with trypan blue. Lines indicate ErM hyphal coils. Micrographs courtesy of Kevin Newsham, David Read, and Ulrik Sochting, and taken at 400 x magnification with a Leica DMRB microscope mounted with a Leica DFC420 digital camera. (PNG 539 kb)
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Lorberau, K.E., Botnen, S.S., Mundra, S. et al. Does warming by open-top chambers induce change in the root-associated fungal community of the arctic dwarf shrub Cassiope tetragona (Ericaceae)?. Mycorrhiza 27, 513–524 (2017). https://doi.org/10.1007/s00572-017-0767-y
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DOI: https://doi.org/10.1007/s00572-017-0767-y