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Microbial Ecology

, Volume 78, Issue 3, pp 764–780 | Cite as

Different Degrees of Niche Differentiation for Bacteria, Fungi, and Myxomycetes Within an Elevational Transect in the German Alps

  • Mathilde Borg DahlEmail author
  • Asker Daniel Brejnrod
  • Jakob Russel
  • Søren Johannes Sørensen
  • Martin Schnittler
Soil Microbiology

Abstract

We used direct DNA amplification from soil extracts to analyze microbial communities from an elevational transect in the German Alps by parallel metabarcoding of bacteria (16S rRNA), fungi (ITS2), and myxomycetes (18S rRNA). For the three microbial groups, 5710, 6133, and 261 operational taxonomic units (OTU) were found. For the latter group, we can relate OTUs to barcodes from fruit bodies sampled over a 4-year period. The alpha diversity of myxomycetes was positively correlated with that of bacteria. Vegetation type was found to be the main explanatory parameter for the community composition of all three groups and a substantial species turnover with elevation was observed. Bacteria and fungi display similar community responses, driven by symbiont species and plant substrate quality. Myxamoebae show a more patchy distribution, though still clearly stratified between taxa, which seems to be a response to both structural properties of the habitat and interaction with specific bacterial and fungal taxa. Finally, we report a high number of myxomycete OTUs not represented in a reference database from fructifications, which might represent novel species.

Keywords

16S rRNA 18S rRNA DNA barcoding Environmental PCR (ePCR) ITS Myxomycetes Natural gradient 

Notes

Acknowledgments

MD thanks Dr. Martin Steen Mortensen for assistance with the robot soil extraction and Luma George Odish for laboratorial assistance in the preparation of the Illumina library. Dr. Samuel Jacquiod helped with advice and assistance for the statistical calculations. We also thank Stefan Kellerer and Klaus Kellner, the wardens of the Tröglhütte of the DAV (Deutscher Alpenverein), for making our stay at the field site pleasant. We wish to express general gratitude to researchers for sharing their data and programming codes as well as engaging in online discussion forums (particularly Stack Overflow), which has benefited the analysis in this study.

Funding Information

Funding for this study was provided in the frame of a Ph.D. position for MD within the Research Training Group RESPONSE (RTG 2010), supported by the Deutsche Forschungsgemeinschaft (DFG).

Compliance with Ethical Standards

Conflict of Interest

The authors declare that they have no conflict of interest.

Supplementary material

248_2019_1347_MOESM1_ESM.xlsx (10 kb)
ESM 1 List of primers used to amplify the three target communities. (XLSX 9 kb)
248_2019_1347_MOESM2_ESM.xlsx (32 kb)
ESM 2 DNA reads of mock samples. (XLSX 32 kb)
248_2019_1347_MOESM3_ESM.pdf (2.1 mb)
ESM 3 Sample quality: Illumina quality statistics, OTU accumulation curves, and overview of significant relations between the numbers of DNA reads and the numbers of OTUs. (PDF 2149 kb)
248_2019_1347_MOESM4_ESM.xlsx (2.4 mb)
ESM 4 OTU tables. (XLSX 2472 kb)
248_2019_1347_MOESM5_ESM.pdf (1.4 mb)
ESM 5 Maximum-likelihood phylogenetic tree of the most abundant myxomycete OTUs. (PDF 1432 kb)
248_2019_1347_MOESM6_ESM.pdf (99 kb)
ESM 6 Analysis script. (PDF 98 kb)
248_2019_1347_MOESM7_ESM.pdf (116 kb)
ESM 7 Result script. (PDF 115 kb)
248_2019_1347_MOESM8_ESM.xlsx (15 kb)
ESM 8 Functional classification. (XLSX 14 kb)

References

  1. 1.
    Abarenkov K, Henrik Nilsson R, Larsson K-H, Alexander IJ, Eberhardt U, Erland S, Høiland K, Kjøller R, Larsson E, Pennanen T, Sen R, Taylor AFS, Tedersoo L, Ursing BM, Vrålstad T, Liimatainen K, Peintner U, Kõljalg U (2010) The UNITE database for molecular identification of fungi – recent updates and future perspectives. New Phytol 186:281–285Google Scholar
  2. 2.
    Adl MS, Gupta VVSR (2006) Protists in soil ecology and forest nutrient cycling. Can J For Res 36:1805–1817Google Scholar
  3. 3.
    Adl SM, Simpson AGB, Lane CE et al (2012) The revised classification of eukaryotes. J Eukaryot Microbiol 59:1–45Google Scholar
  4. 4.
    Anderson MJ (2001) A new method for non parametric multivariate analysis of variance. Austral Ecol 26:32–46Google Scholar
  5. 5.
    Bahram M, Kohout P, Anslan S, Harend H, Abarenkov K, Tedersoo L (2016) Stochastic distribution of small soil eukaryotes resulting from high dispersal and drift in a local environment. ISME J 10:885–896Google Scholar
  6. 6.
    Bailey VL, Fansler SJ, Stegen JC, McCue LA (2013) Linking microbial community structure to β-glucosidic function in soil aggregates. ISME J 7:2044–2053Google Scholar
  7. 7.
    Benjamini Y, Hochberg Y (1995) Controlling the false discovery rate: a practical and powerful approach to multiple testing. J R Stat Soc Ser B 57:289–300Google Scholar
  8. 8.
    Bjørnlund L, Rønn R (2008) “David and Goliath” of the soil food web – flagellates that kill nematodes. Soil Biol Biochem 40:2032–2039Google Scholar
  9. 9.
    Bjørnlund L, Mørk S, Vestergård M, Rønn R (2006) Trophic interactions between rhizosphere bacteria and bacterial feeders influenced by phosphate and aphids in barley. Biol Fertil Soils 43:1–11Google Scholar
  10. 10.
    Boenigk J, Ereshefsky M, Hoef-Emden K, Mallet J, Bass D (2012) Concepts in protistology: species definitions and boundaries. Eur J Protistol 48:96–102Google Scholar
  11. 11.
    Bonkowski M (2002) Protozoa and plant growth: trophic links and mutualism. Eur J Protistol 37:363–365Google Scholar
  12. 12.
    Bonkowski M (2004) Protozoa and plant growth: the microbial loop in soil revisited. New Phytol 162:617–631Google Scholar
  13. 13.
    Borg Dahl M, Priemé A, Brejnrod A et al (2017) Warming, shading and a moth outbreak reduce tundra carbon sink strength dramatically by changing plant cover and soil microbial activity. Sci Rep 7:16035Google Scholar
  14. 14.
    Borg Dahl M, Brejnrod AD, Unterseher M, Hoppe T, Feng Y, Novozhilov Y, Sørensen SJ, Schnittler M (2018a) Genetic barcoding of dark-spored myxomycetes (Amoebozoa) – identification, evaluation and application of a sequence similarity threshold for species differentiation in NGS studies. Mol Ecol Resour 18:306–318Google Scholar
  15. 15.
    Borg Dahl M, Shchepin ON, Schunk C et al (2018b) A four year survey reveals a coherent pattern between occurrence of fruit bodies and soil amoebae populations for nivicolous myxomycetes. Sci Rep 8:11662Google Scholar
  16. 16.
    Brundrett MC (2002) Coevolution of roots and mycorrhizas of land plants. New Phytol 154:275–304Google Scholar
  17. 17.
    Chagnon PL, Bradley RL, Maherali H, Klironomos JN (2013) A trait-based framework to understand life history of mycorrhizal fungi. Trends Plant Sci 18:484–491Google Scholar
  18. 18.
    Chase JM, Kraft NJB, Smith KG et al (2011) Using null models to disentangle variation in community dissimilarity from variation in α-diversity. Ecosphere 2:art24Google Scholar
  19. 19.
    Choma M, Bárta J, Šantrůčková H, Urich T (2016) Low abundance of Archaeorhizomycetes among fungi in soil metatranscriptomes. Sci Rep 6:38455Google Scholar
  20. 20.
    Churchman K (2015) Brock Biology of Microorganisms14th edn. Pearson Higher Education, New YorkGoogle Scholar
  21. 21.
    Crump BC, Amaral-Zettler LA, Kling GW (2012) Microbial diversity in arctic freshwaters is structured by inoculation of microbes from soils. ISME J 6:1629–1639Google Scholar
  22. 22.
    Dagamac NHA, Rojas C, Novozhilov YK et al (2017) Speciation in progress? A phylogeographic study among populations of Hemitrichia serpula (Myxomycetes). PLoS One 12:1–22Google Scholar
  23. 23.
    Day A (2012) Heatmap.plus: Heatmap with more sensible behavior. R package version 1.3Google Scholar
  24. 24.
    de Boer W, Folman LB, Summerbell RC et al (2005) Living in a fungal world: impact of fungi on soil bacterial niche development. FEMS Microbiol Rev 29:795–811Google Scholar
  25. 25.
    de Vries FT, Manning P, Tallowin JRB, Mortimer SR, Pilgrim ES, Harrison KA, Hobbs PJ, Quirk H, Shipley B, Cornelissen JHC, Kattge J, Bardgett RD (2012) Abiotic drivers and plant traits explain landscape-scale patterns in soil microbial communities. Ecol Lett 15:1230–1239Google Scholar
  26. 26.
    Deslippe JR, Hartmann M, Simard SW, Mohn WW (2012) Long-term warming alters the composition of Arctic soil microbial communities. FEMS Microbiol Ecol 82:303–315Google Scholar
  27. 27.
    Edgar R (2010) Search and clustering orders of magnitude faster than BLAST. Bioinformatics 26:2460–2461Google Scholar
  28. 28.
    Edgar R (2016) SINTAX: a simple non-Bayesian taxonomy classifier for 16S and ITS sequences. bioRxiv. 074161Google Scholar
  29. 29.
    Edgar R, Flyvbjerg H (2014) Error filtering, pair assembly and error correction for next-generation sequencing reads. Bioinformatics 31:3476–3482Google Scholar
  30. 30.
    Feng Y, Schnittler M (2015) Sex or no sex? Group I introns and independent marker genes reveal the existence of three sexual but reproductively isolated biospecies in Trichia varia (Myxomycetes). Org Divers Evol 15:631–650Google Scholar
  31. 31.
    Feng Y, Klahr A, Janik P, Ronikier A, Hoppe T, Novozhilov YK, Schnittler M (2016) What an intron may tell: several sexual biospecies coexist in Meriderma spp. (Myxomycetes). Protist 167:234–253Google Scholar
  32. 32.
    Fierer N, Bradford MA, Jackson RB (2007) Toward an ecological classification of soil bacteria. Ecology 88:1354–1364Google Scholar
  33. 33.
    Finlay RD (2008) Ecological aspects of mycorrhizal symbiosis: with special emphasis on the functional diversity of interactions involving the extraradical mycelium. J Exp Bot 59:1115–1126Google Scholar
  34. 34.
    Finlay RD, Read DJ (1986) The structure and function of the vegetative mycelium of ectomycorrhizal plants: I. Translocation of 14C-labelled carbon between plants interconnected by a common mycelium. New Phytol 103:143–156Google Scholar
  35. 35.
    Fiore-Donno AM, Kamono A, Meyer M, Schnittler M, Fukui M, Cavalier-Smith T (2012) 18S rDNA phylogeny of Lamproderma and allied genera (Stemonitales, myxomycetes, Amoebozoa). PLoS One 7:e35359Google Scholar
  36. 36.
    Fiore-Donno AM, Clissmann F, Meyer M, Schnittler M, Cavalier-Smith T (2013) Two-gene phylogeny of bright-spored myxomycetes (slime-moulds, superorder Lucisporidia). PLoS One 8:e62586Google Scholar
  37. 37.
    Fiore-Donno AM, Weinert J, Wubet T, Bonkowski M (2016) Metacommunity analysis of amoeboid protists in grassland soils. Sci Rep 6:19068Google Scholar
  38. 38.
    Franklin RB, Mills AL (2003) Multi-scale variation in spatial heterogeneity for microbial community structure in an eastern Virginia agricultural field. FEMS Microbiol Ecol 44:335–346Google Scholar
  39. 39.
    Fukasawa Y, Hyodo F, Kawakami S (2018) Foraging association between myxomycetes and fungal communities on coarse woody debris. Soil Biol Biochem 121:95–102Google Scholar
  40. 40.
    Geisen S, Bonkowski M (2017) Methodological advances to study the diversity of soil protists and their functioning in soil food webs. Appl Soil Ecol.  https://doi.org/10.1016/j.apsoil.2017.05.021
  41. 41.
    Geisen S, Cornelia B, Jörg R et al (2014) Soil water availability strongly alters the community composition of soil protists. Pedobiologia 57:205–213Google Scholar
  42. 42.
    Geisen S, Laros I, Vizcaíno A, Bonkowski M, de Groot GA (2015a) Not all are free-living: high-throughput DNA metabarcoding reveals a diverse community of protists parasitizing soil metazoa. Mol Ecol 24:4556–4569Google Scholar
  43. 43.
    Geisen S, Tveit AT, Clark IM, Richter A, Svenning MM, Bonkowski M, Urich T (2015b) Metatranscriptomic census of active protists in soils. ISME J 9:2178–2190Google Scholar
  44. 44.
    Geisen S, Mitchell EAD, Wilkinson DM, Adl S, Bonkowski M, Brown MW, Fiore-Donno AM, Heger TJ, Jassey VEJ, Krashevska V, Lahr DJG, Marcisz K, Mulot M, Payne R, Singer D, Anderson OR, Charman DJ, Ekelund F, Griffiths BS, Rønn R, Smirnov A, Bass D, Belbahri L, Berney C, Blandenier Q, Chatzinotas A, Clarholm M, Dunthorn M, Feest A, Fernández LD, Foissner W, Fournier B, Gentekaki E, Hájek M, Helder J, Jousset A, Koller R, Kumar S, la Terza A, Lamentowicz M, Mazei Y, Santos SS, Seppey CVW, Spiegel FW, Walochnik J, Winding A, Lara E (2017) Soil protistology rebooted: 30 fundamental questions to start with. Soil Biol Biochem 111:94–103Google Scholar
  45. 45.
    Glücksman E, Bell T, Griffiths RI, Bass D (2010) Closely related protist strains have different grazing impacts on natural bacterial communities. Environ Microbiol 12:3105–3113Google Scholar
  46. 46.
    Goodfellow M, Williams ST (1983) Ecology of actinomycetes. Annu Rev Microbiol 37:189–216Google Scholar
  47. 47.
    Goslee SC, Urban DL (2007) The ecodist package for dissimilarity-based analysis of ecological data. J Stat Softw 22:1–19Google Scholar
  48. 48.
    Harris JK, Sahl JW, Castoe TA, Wagner BD, Pollock DD, Spear JR (2010) Comparison of normalization methods for construction of large, multiplex amplicon pools for next-generation sequencing. Appl Environ Microbiol 76:3863–3868Google Scholar
  49. 49.
    Hess S, Sausen N, Melkonian M (2012) Shedding light on vampires: the phylogeny of vampyrellid amoebae revisited. PLoS One 7:e31165Google Scholar
  50. 50.
    Högberg P, Read DJ (2006) Towards a more plant physiological perspective on soil ecology. Trends Ecol Evol 21:548–554Google Scholar
  51. 51.
    Högberg P, Nordgren A, Buchmann N, Taylor AFS, Ekblad A, Högberg MN, Nyberg G, Ottosson-Löfvenius M, Read DJ (2001) Large-scale forest girdling shows that current photosynthesis drives soil respiration. Nature 411:789–792Google Scholar
  52. 52.
    Hünninghaus M, Koller R, Kramer S, Marhan S, Kandeler E, Bonkowski M (2017) Changes in bacterial community composition and soil respiration indicate rapid successions of protist grazers during mineralization of maize crop residues. Pedobiologia 62:1–8Google Scholar
  53. 53.
    Iriberri J, Azúa I, Labirua-Iturburu A, Artolozaga I, Barcina I (1994) Differential elimination of enteric bacteria by protists in a freshwater system. J Appl Bacteriol 77:476–483Google Scholar
  54. 54.
    Jacquiod S, Stenbæk J, Santos SS, Winding A, Sørensen SJ, Priemé A (2016) Metagenomes provide valuable comparative information on soil microeukaryotes. Res Microbiol 167:436–450Google Scholar
  55. 55.
    Kamono A, Kojima H, Matsumoto J, Kawamura K, Fukui M (2009) Airborne myxomycete spores: detection using molecular techniques. Naturwissenschaften 96:147–151Google Scholar
  56. 56.
    Kamono A, Meyer M, Cavalier-Smith T et al (2012) Exploring slime mould diversity in high-altitude forests and grasslands by environmental RNA analysis. FEMS Microbiol Ecol 84:98–109Google Scholar
  57. 57.
    Katoh K, Misawa K, Kuma K et al (2002) MAFFT: a novel method for rapid multiple sequence alignment based on fast Fourier transform. Nucleic Acids Res 30:3059–3066Google Scholar
  58. 58.
    King AJ, Freeman KR, McCormick KF et al (2010) Biogeography and habitat modelling of high-alpine bacteria. Nat Commun 1:1–6Google Scholar
  59. 59.
    Kohler A, Kuo A, Nagy LG et al (2015) Convergent losses of decay mechanisms and rapid turnover of symbiosis genes in mycorrhizal mutualists. Nat Genet 47:410–415Google Scholar
  60. 60.
    Kowalski DT (1975) The myxomycete taxa described by Charles Meylan. Mycologia 67:448–494Google Scholar
  61. 61.
    Krashevska V, Bonkowski M, Maraun M, Ruess L, Kandeler E, Scheu S (2008) Microorganisms as driving factors for the community structure of testate amoebae along an altitudinal transect in tropical mountain rain forests. Soil Biol Biochem 40:2427–2433Google Scholar
  62. 62.
    Lado C (2004) Nivicolous myxomycetes of the Iberian Peninsula: considerations on species richness and ecological requirements. Syst Geogr Plants 74:143–157Google Scholar
  63. 63.
    Lado C (2005-2019). An on line nomenclatural information system of Eumycetozoa. www.nomen.eumycetozoa.com. Accessed Nov 2017
  64. 64.
    Lanzén A, Epelde L, Blanco F, Martín I, Artetxe U, Garbisu C (2016) Multi-targeted metagenetic analysis of the influence of climate and environmental parameters on soil microbial communities along an elevational gradient. Sci Rep 6:28257Google Scholar
  65. 65.
    Lazzaro A, Hilfiker D, Zeyer J (2015) Structures of microbial communities in alpine soils: seasonal and elevational effects. Front Microbiol 6:1–13Google Scholar
  66. 66.
    Liu QS, Yan SZ, Chen SL (2015) Species diversity of myxomycetes associated with different terrestrial ecosystems, substrata (microhabitats) and environmental factors. Mycol Prog 14:27Google Scholar
  67. 67.
    Margesin R, Jud M, Tscherko D, Schinner F (2009) Microbial communities and activities in alpine and subalpine soils. FEMS Microbiol Ecol 67:208–218Google Scholar
  68. 68.
    Martiny JBH, Jones SE, Lennon JT, Martiny AC (2015) Microbiomes in light of traits: a phylogenetic perspective. Science 350:aac9323.  https://doi.org/10.1126/science.aac9323 Google Scholar
  69. 69.
    McMurdie JP, Holmes S (2013) phyloseq: an R package for reproducible interactive analysis and graphics of microbiome census data. PLoS One 8:e61217Google Scholar
  70. 70.
    Metzing D, Garve E, Matzke-Hajek G et al (2018) Rote Liste und Gesamtartenliste der Farn- und Blütenpflanzen (Tracheophyta) Deutschlands. Natursch Biol Vielfalt 70:313–358Google Scholar
  71. 71.
    Mueller RC, Paula FS, Mirza BS, Rodrigues JLM, Nüsslein K, Bohannan BJM (2014) Links between plant and fungal communities across a deforestation chronosequence in the Amazon rainforest. ISME J 8:1548–1550Google Scholar
  72. 72.
    Murase J, Noll M, Frenzel P (2006) Impact of protists on the activity and structure of the bacterial community in a rice field soil. Appl Environ Microbiol 72:5436–5444Google Scholar
  73. 73.
    Naether A, Foesel BU, Naegele V, Wüst PK, Weinert J, Bonkowski M, Alt F, Oelmann Y, Polle A, Lohaus G, Gockel S, Hemp A, Kalko EKV, Linsenmair KE, Pfeiffer S, Renner S, Schöning I, Weisser WW, Wells K, Fischer M, Overmann J, Friedrich MW (2012) Environmental factors affect acidobacterial communities below the subgroup level in grassland and forest soils. Appl Environ Microbiol 78:7398–7406Google Scholar
  74. 74.
    Nguyen NH, Song Z, Bates ST, Branco S, Tedersoo L, Menke J, Schilling JS, Kennedy PG (2016) FUNGuild: an open annotation tool for parsing fungal community datasets by ecological guild. Fungal Ecol 20:241–248Google Scholar
  75. 75.
    Novozhilov YK, Schnittler M, Erastova DA, Okun MV, Schepin ON, Heinrich E (2013) Diversity of nivicolous myxomycetes of the Teberda State Biosphere Reserve (Northwestern Caucasus, Russia). Fungal Divers 59:109–130Google Scholar
  76. 76.
    Novozhilov YK, Rollins AW, Schnittler M (2017) Ecology and distribution of myxomycetes. In: Stephenson SL, Rojas C (eds) Myxomycetes – biology, systematics, biogeography and ecology. Elsevier, Academic, pp 253–298Google Scholar
  77. 77.
    Oksanen J, Guillaume FB, Friendly M et al. (2013) R package vegan: ecological diversity. R package version 2.4-2Google Scholar
  78. 78.
    Osono T, Takeda H (2002) Comparison of litter decomposing ability among diverse fungi in a cool temperate deciduous forest in Japan. Mycologia 94:421–427Google Scholar
  79. 79.
    Pawlowski J, Burki F (2009) Untangling the phylogeny of amoeboid protists. J Eukaryot Microbiol 56:16–25Google Scholar
  80. 80.
    Peay KG, Baraloto C, Fine PVA (2013) Strong coupling of plant and fungal community structure across western Amazonian rainforests. ISME J 7:1852–1861Google Scholar
  81. 81.
    Philippot L, Bru D, Saby NPA, Čuhel J, Arrouays D, Šimek M, Hallin S (2009) Spatial patterns of bacterial taxa in nature reflect ecological traits of deep branches of the 16S rRNA bacterial tree. Environ Microbiol 11:3096–3104Google Scholar
  82. 82.
    Portillo MC, Leff JW, Lauber CL et al. (2013) Cell size distributions of soil bacterial and archaeal taxa. Appl Environ Microbiol 79:7610–7617Google Scholar
  83. 83.
    Pruesse E, Quast C, Knittel K, Fuchs BM, Ludwig W, Peplies J, Glockner FO (2007) SILVA: a comprehensive online resource for quality checked and aligned ribosomal RNA sequence data compatible with ARB. Nucleic Acids Res 35:7188–7196Google Scholar
  84. 84.
    Rahanandeh H, Khodakaramian G, Hassanzadeh N et al (2013) Evaluation of antagonistic Pseudomonas against root lesion nematode of tea. Int J Biosci 3:32–40Google Scholar
  85. 85.
    R Core Team (2013) R: A language and environment for statistical computing. R Found Stat ComputGoogle Scholar
  86. 86.
    Rixen C, Stoeckli V, Ammann W (2003) Does artificial snow production affect soil and vegetation of ski pistes? A review. Perspect Plant Ecol Evol Syst 5:219–230Google Scholar
  87. 87.
    Robeson MS, King AJ, Freeman KR, Birky CW, Martin AP, Schmidt SK (2011) Soil rotifer communities are extremely diverse globally but spatially autocorrelated locally. PNAS 108:4406–4410Google Scholar
  88. 88.
    Rohlfs M, Albert M, Keller NP, Kempken F (2007) Secondary chemicals protect mould from fungivory. Biol Lett 3:523–525Google Scholar
  89. 89.
    Ronikier A, Ronikier M (2009) How “alpine” are nivicolous myxomycetes? A worldwide assessment of altitudinal distribution. Mycologia 101:1–16Google Scholar
  90. 90.
    Rønn R, Mccaig AE, Griffiths BS et al (2002) Impact of protozoan grazing on bacterial community structure in soil microcosms. Appl Environ Microbiol 68:6094–6105Google Scholar
  91. 91.
    Rosenberg K, Bertaux J, Krome K, Hartmann A, Scheu S, Bonkowski M (2009) Soil amoebae rapidly change bacterial community composition in the rhizosphere of Arabidopsis thaliana. ISME J 3:675–684Google Scholar
  92. 92.
    Rosling A, Cox F, Cruz-Martinez K, Ihrmark K, Grelet GA, Lindahl BD, Menkis A, James TY (2011) Archaeorhizomycetes: unearthing an ancient class of ubiquitous soil fungi. Science 333:876–879Google Scholar
  93. 93.
    Roux-Fouillet P, Wipf S, Rixen C (2011) Long-term impacts of ski piste management on alpine vegetation and soils. J Appl Ecol 48:906–915Google Scholar
  94. 94.
    Ruggiero MA, Gordon DP, Orrell TM et al (2015) A higher level classification of all living organisms. PLoS One 10:1–60Google Scholar
  95. 95.
    Russel J (2016) MicEco: various functions for analysis for microbial community data. Available from: www.github.com/Russel88/MicEco
  96. 96.
    Schadt CW, Martin AP, Lipson DA et al (2003) Seasonal dynamics of previously unknown fungal lineages in tundra soils. Science 301:1359–1361Google Scholar
  97. 97.
    Schmidt SK, Lipson DA (2004) Microbial growth under the snow: implications for nutrient and allelochemical availability in temperate soils. Plant Soil 259:1–7Google Scholar
  98. 98.
    Schnittler M, Tesmer JA (2008) A habitat colonisation model for spore-dispersed organisms – does it work with eumycetozoans? Mycol Res 112:697–707Google Scholar
  99. 99.
    Schnittler M, Novozhilov YK, Romeralo M et al (2012) Myxomycetes and myxomycete-like organisms. In: Frey W (ed) Englers syllabus of plant families, vol 4. Bornträger, Stuttgart, pp 40–88Google Scholar
  100. 100.
    Schnittler M, Erastova DA, Shchepin ON, Heinrich E, Novozhilov YK (2015) Four years in the Caucasus – observations on the ecology of nivicolous myxomycetes. Fungal Ecol 14:105–115Google Scholar
  101. 101.
    Shang Y, Sikorski J, Bonkowski M et al (2017) Inferring interactions in complex microbial communities from nucleotide sequence data and environmental parameters. PLoS One 12:e173765Google Scholar
  102. 102.
    Shchepin O, Novozhilov Y, Schnittler M (2014) Protistology Nivicolous myxomycetes in agar culture: some results and open problems. Potistology 8:53–61Google Scholar
  103. 103.
    Shchepin ON, Novozhilov YK, Schnittler M (2016) Disentangling the taxonomic structure of the Lepidoderma chailletii-carestianum species complex (Myxogastria, Amoebozoa): genetic and morphological aspects. Protistology 10:120–129Google Scholar
  104. 104.
    Shchepin ON, Schnittler M, Erastva DA et al (2019) Community of dark-spored myxomycetes in ground litter and soil of taiga forest (Nizhne-Svirskiy Reserve, Russia) revealed by DNA metabarcoding. Fungal Ecol 39:80–93.  https://doi.org/10.1016/j.funeco.2018.11.006
  105. 105.
    Stephenson SL, Feest A (2012) Ecology of soil eumycetozoans. Acta Protozool 51:201–208Google Scholar
  106. 106.
    Stephenson SL, Schnittler M (2017) Myxomycetes. In: Archibald JM, Simpson AGB, Slamovits CH et al (eds) Handbook of the Protists. Springer, Berlin, pp 1405–1432Google Scholar
  107. 107.
    Stephenson SL, Novozhilov YK, Schnittler M (2000) Distribution and ecology of myxomycetes in high-latitude regions of the northern hemisphere. J Biogeogr 27:741–754Google Scholar
  108. 108.
    Stephenson SL, Schnittler M, Novozhilov YK (2008) Myxomycete diversity and distribution from the fossil record to the present. Biodivers Conserv 17:285–301Google Scholar
  109. 109.
    Tamura K, Stecher G, Peterson D, Filipski A, Kumar S (2013) MEGA6: molecular evolutionary genetics analysis version 6.0. Mol Biol Evol 30:2725–2729Google Scholar
  110. 110.
    Tansley IB (1994) Review no. 62. The phytosociology of myxomycetes. New Phytol 126:175–201Google Scholar
  111. 111.
    Taylor AFS, Alexander I (2005) The ectomycorrhizal symbiosis: life in the real world. Mycologist 19:102–112Google Scholar
  112. 112.
    Taylor WD, Berger J (1976) Growth responses of cohabiting ciliate protozoa to various prey bacteria. Can J Zool 54:1111–1114Google Scholar
  113. 113.
    Taylor KM, Feest A, Stephenson SL (2015) The occurrence of myxomycetes in wood. Fungal Ecol 17:179–182Google Scholar
  114. 114.
    Tedersoo L, Pärtel K, Jairus T, Gates G, Põldmaa K, Tamm H (2009) Ascomycetes associated with ectomycorrhizas: molecular diversity and ecology with particular reference to the Helotiales. Environ Microbiol 11:3166–3178Google Scholar
  115. 115.
    Tedersoo L, Bahram M, Polme S, Koljalg U, Yorou NS, Wijesundera R, Ruiz LV, Vasco-Palacios AM, Thu PQ, Suija A, Smith ME, Sharp C, Saluveer E, Saitta A, Rosas M, Riit T, Ratkowsky D, Pritsch K, Poldmaa K, Piepenbring M, Phosri C, Peterson M, Parts K, Partel K, Otsing E, Nouhra E, Njouonkou AL, Nilsson RH, Morgado LN, Mayor J, May TW, Majuakim L, Lodge DJ, Lee SS, Larsson KH, Kohout P, Hosaka K, Hiiesalu I, Henkel TW, Harend H, Guo LD, Greslebin A, Grelet G, Geml J, Gates G, Dunstan W, Dunk C, Drenkhan R, Dearnaley J, de Kesel A, Dang T, Chen X, Buegger F, Brearley FQ, Bonito G, Anslan S, Abell S, Abarenkov K (2014) Global diversity and geography of soil fungi. Science 346:1256688–1256689Google Scholar
  116. 116.
    Tiunov AV, Semenina EE, Aleksandrova AV et al (2015) Stable isotope composition (δ13 C and δ15 N values) of slime molds: placing bacterivorous soil protozoans in the food web context. Rapid Commun Mass Spectrom 29:1465–1472Google Scholar
  117. 117.
    Treseder KK, Kivlin SN, Hawkes CV (2011) Evolutionary trade-offs among decomposers determine responses to nitrogen enrichment. Ecol Lett 14:933–938Google Scholar
  118. 118.
    Urich T, Lanzén A, Qi J, Huson DH, Schleper C, Schuster SC (2008) Simultaneous assessment of soil microbial community structure and function through analysis of the meta-transcriptome. PLoS One 3:e2527Google Scholar
  119. 119.
    van der Heijden MGA, Bardgett RD, van Straalen NM (2008) The unseen majority: soil microbes as drivers of plant diversity and productivity in terrestrial ecosystems. Ecol Lett 11:296–310Google Scholar
  120. 120.
    van der Putten WH, Bardgett RD, Bever JD, Bezemer TM, Casper BB, Fukami T, Kardol P, Klironomos JN, Kulmatiski A, Schweitzer JA, Suding KN, van de Voorde TFJ, Wardle DA (2013) Plant-soil feedbacks: the past, the present and future challenges. J Ecol 101:265–276Google Scholar
  121. 121.
    von Mering C, Hugenholtz P, Raes J et al (2007) Quantitative phylogenetic assessment of microbial communities in diverse environments. Science 315:126–130Google Scholar
  122. 122.
    Wardle DA, Bardgett RD, Klironomos JN, Setälä H, van der Putten W, Wall DH (2004) Ecological linkages between aboveground and belowground biota. Science 304:1629–1633Google Scholar
  123. 123.
    Whitaker J, Ostle N, Nottingham AT, Ccahuana A, Salinas N, Bardgett RD, Meir P, McNamara N, Austin A (2014) Microbial community composition explains soil respiration responses to changing carbon inputs along an Andes-to-Amazon elevation gradient. J Ecol 102:1058–1071Google Scholar
  124. 124.
    Wickham H (2010) Ggplot2: elegant graphics for data analysis. Springer-Verlag, New YorkGoogle Scholar
  125. 125.
    Xiong W, Jousset A, Guo S et al (2017) Soil protist communities form a dynamic hub in the soil microbiome. ISME J:1–5Google Scholar
  126. 126.
    Yashiro E, Pinto-figueroa E, Buri A et al (2016) Local environmental factors drive divergent grassland soil bacterial communities in the western Swiss Alps. Appl Environ Microbiol 82:6303–6316Google Scholar
  127. 127.
    Zinger L, Lejon DPH, Baptist F, Bouasria A, Aubert S, Geremia RA, Choler P (2011) Contrasting diversity patterns of crenarchaeal, bacterial and fungal soil communities in an alpine landscape. PLoS One 6:e19950Google Scholar

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© Springer Science+Business Media, LLC, part of Springer Nature 2019

Authors and Affiliations

  1. 1.Institute of Botany and Landscape EcologyUniversity of GreifswaldGreifswaldGermany
  2. 2.Section of Microbiology, Department of BiologyUniversity of CopenhagenCopenhagenDenmark

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