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Fungal Growth and Biomass Development is Boosted by Plants in Snow-Covered Soil

  • Fungal Microbiology
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Abstract

Soil microbial communities follow distinct seasonal cycles which result in drastic changes in processes involving soil nutrient availability. The biomass of fungi has been reported to be highest during winter, but is fungal growth really occurring in frozen soil? And what is the effect of plant cover on biomass formation and on the composition of fungal communities? To answer these questions, we monitored microbial biomass N, ergosterol, and the amount of fungal hyphae during summer and winter in vegetated and unvegetated soils of an alpine primary successional habitat. The winter fungal communities were identified by rDNA ITS clone libraries. Winter soil temperatures ranged between −0.6°C and −0.1°C in snow-covered soil. We found distinct seasonal patterns for all biomass parameters, with highest biomass concentrations during winter in snow-covered soil. The presence of plant cover had a significant positive effect on the amount of biomass in the soil, but the type of plant cover (plant species) was not a significant factor. A mean hyphal ingrowth of 5.6 m g−1 soil was detected in snow-covered soil during winter, thus clearly proving fungal growth during winter in snow-covered soil. Winter fungal communities had a typical species composition: saprobial fungi were dominating, among them many basidiomycete yeasts. Plant cover had no influence on the composition of winter fungal communities.

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References

  1. Amato M, Ladd JN (1988) Assay for microbial biomass based on ninhydrin reactive nitrogen in extracts of fumigated soils. Soil Biol Biochem 20:107–114

    Article  CAS  Google Scholar 

  2. Bakermans C, Skidmore M (2011) Microbial metabolism in ice and brine at −5°C. Environ Microbio 13:2269–2278

    Article  Google Scholar 

  3. Bardgett RD, Whittaker JB, Frankland JC (1993) The effect of collembolan grazing on fungal activity in differently managed upland pastures: a microcosm study. Biol Fert Soils 16:255–262

    Article  Google Scholar 

  4. Bardgett RD, Whittaker JB, Frankland JC (1993) The diet and food preferences of Onychiurus procampatus (Collembola) from upland grassland soils. Biol Fert Soils 16:296–298

    Article  Google Scholar 

  5. Bardgett RD, Bowman WD, Kaufmann R, Schmidt SK (2005) A temporal approach to linking aboveground and belowground ecology. Trends Ecol Evolut 20:634–641

    Article  Google Scholar 

  6. Bell C, McIntyre N, Cox S, Tissue D, Zak J (2008) Soil microbial responses to temporal variations of moisture and temperature in a Chihuahuan desert grassland. Microb Ecol 56:153–167

    Article  PubMed  Google Scholar 

  7. Boddy L, Wood J, Redman E, Hynes J, Fricker MD (2010) Fungal network responses to grazing. Fungal Genet Biol 47:522–530

    Article  PubMed  Google Scholar 

  8. Bonkowski M, Griffiths BS, Ritz K (2000) Food preferences of earthworms for soil fungi. Pedobiologia 44:666–676

    Article  Google Scholar 

  9. Buckeridge KM, Jefferies RL (2007) Vegetation loss alters soil nitrogen dynamics in an Arctic salt marsh. J Ecol 95:283–293

    Article  CAS  Google Scholar 

  10. Buckeridge KM, Grogan P (2008) Deepened snow alters soil microbial nutrient limitations in arctic birch hummock tundra. Appl Soil Ecol 39:210–222

    Article  Google Scholar 

  11. Butinar L, Spencer-Martins I, Gunde-Cimerman N (2007) Yeasts in high Arctic glaciers: the discovery of a new habitat for eukaryotic microorganisms. Antonie Leeuwenhoek 91:277–289

    Article  PubMed  Google Scholar 

  12. Buzzini P, Martini A (2000) Biodiversity of killer activity in yeasts isolated from the Brazilian rain forest. Can J Microbiol 46:607–611

    Article  PubMed  CAS  Google Scholar 

  13. Clein JS, Schimel JP (1995) Microbial activity of tundra and taiga soils at sub-zero temperatures. Soil Biol Biochem 27:1231–1234

    Article  CAS  Google Scholar 

  14. Cline D (1995) Snow surface energy exchanges and snowmelt at a continental alpine site. Proc. Symp. on Biogeochemistry of Seasonally Snow-Covered Catchments, Boulder, CO, Int Assoc Hydrol Sci, pp 157–166

  15. De García V, Brizzio S, Libkind D, Buzzini P, Van Broock M (2007) Biodiversity of cold-adapted yeasts from glacial meltwater rivers in Patagonia, Argentina. FEMS Microbiol Ecol 59:331–341

    Article  PubMed  Google Scholar 

  16. Erschbaumer B, Bitterlich W, Raffl C (1999) Die Vegetation als Indikator für die Bodenbildung im Gletschervorfeld des Rotmoosferners (Obergurgl, Ötztal). Ber nat-med Verein Innsbruck 86:107–122

    Google Scholar 

  17. 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

    Article  PubMed  CAS  Google Scholar 

  18. Gessner MO (2001) Mass loss, fungal colonisation and nutrient dynamics of Phragmites australis leaves during senescence and early aerial decay. Aquatic Bot 69:325–339

    Article  Google Scholar 

  19. Grant WD, West AW (1986) Measurement of ergosterol, diaminopimelic acid and glucosamine in soil: evaluation as indicators of microbial biomass. J Microbiol Meth 6:47–53

    Article  CAS  Google Scholar 

  20. Guevara R, Rayner ADM, Reynolds SE (2000) Effects of fungivory by two specialist ciid beetles (Octotemnus glabriculus and Cis boleti) on the reproductive fitness of their host fungus, Coriolus versicolor. New Phytol 145:137–144

    Article  Google Scholar 

  21. Hansen JF, Thingstad TF, Goksoyr J (1974) Evaluation of hyphal lengths and fungal biomass in soil by a membran filter technique. Oikos 25:102–107

    Article  Google Scholar 

  22. Hoinkes G, Thöni M (1993) Evolution of the Ötztal-Stubai, Scarl-Campo and Ulten basement units. In: Raumer JF, Neubauer M (eds) Pre-mesozoic geology in the Alps. Springer, Berlin

    Google Scholar 

  23. Jaeger CH, Monson RK, Fisk MC, Schmidt SK (1999) Seasonal partitioning of nitrogen by plants and soil microorganisms in an alpine ecosystem. Ecology 80:1883–1891

    Article  Google Scholar 

  24. Joergensen RG, Brookes PC (1990) Ninhydrin-reactive nitrogen measurements of microbial biomass in 0.5 M K2SO4 soil extracts. Soil Biol Biochem 22:1023–1027

    Article  CAS  Google Scholar 

  25. Kaiser C, Fuchslueger L, Koranda M, Gorfer M, Stange CF, Kitzler B, Rasche F, Strauss J, Sessitsch A, Zechmeister-Boltenstern S, Richter A (2011) Plants control the seasonal dynamics of microbial N cycling in a beech forest soil by belowground C allocation. Ecology 92:1036–1051

    Article  PubMed  Google Scholar 

  26. Kaufmann R (2001) Invertebrate succession on an Alpine glacier foreland. Ecology 82:2261–2278

    Article  Google Scholar 

  27. Kaufmann R (2002) Glacier foreland colonisation: distinguishing between short-term and long-term effects of climate change. Oecologia 130:470–475

    Article  Google Scholar 

  28. Kaufmann R, Raffl C (2002) Diversity in primary succession: the chronosequence of a glacier foreland. In: Körner C, Spehn E (eds) Global mountain biodiversity: a global assessment. Parthenon, London, pp 179–192

    Google Scholar 

  29. Kaufmann R, Fuchs M, Gosterxeier N (2002) The soil fauna of an Alpine glacier foreland: colonization and succession. Arctic Antarctic Alpine Research 34:242–250

    Article  Google Scholar 

  30. King AJ, Karki D, Nagy L, Racoviteanu A, Schimidt SK (2010) Microbial biomass and activity in high elevation (>5100 meters) soils from the Annapurna and Sagarmatha regions of the Nepalese Himalayas. Himalayan J Sci 6:11–18

    Google Scholar 

  31. Kõljalg U, Larsson K-H, Abarenkov K, Nilsson RH, Alexander IJ, Eberhardt U, Erland S, Hoiland K, Kjoller R, Larsson E, Pennanen T, Sen R, Taylor AFS, Tedersoo L, Vralstad T, Ursing BM (2005) UNITE: a database providing web-based methods for the molecular identification of ectomycorrhizal fungi. New Phytol 166:1063–1068

    Article  PubMed  Google Scholar 

  32. Lee RE (2010) A primer on insect cold tolerance. In: Denlinger DL, Lee RE (eds) Low temperature biology of insects. Cambridge University Press, Cambridge

    Google Scholar 

  33. Ley RE, Schmidt SK (2002) Fungal and bacterial responses to phenolic compounds and amino acids in high altitude barren soils. Soil Biol Biochem 34:989–995

    Article  CAS  Google Scholar 

  34. Lipson DA, Schmidt SK, Monson RK (1999) Links between microbial population dynamics and plant N availability in an alpine ecosystem. Ecology 80:1623–1631

    Article  Google Scholar 

  35. Löffler UCM, Cypionka H, Löffler J (2008) Soil microbial activity along an arctic-alpine altitudinal gradient from a seasonal perspective. Eur J Soil Sci 59:842–854

    Article  Google Scholar 

  36. Margesin R, Zacke G, Schinner F (2002) Characterization of heterotrophic microorganisms in alpine glacier cryoconite. Arctic Antarctic Alpine Res 34:88–93

    Article  Google Scholar 

  37. Margesin R, Jud M, Tscherko D, Schinner F (2009) Microbial communities and activities in alpine and subalpine soils. FEMS Microbiol Ecol 67:208–218

    Article  PubMed  CAS  Google Scholar 

  38. Matsumoto N (1992) Evolutionary ecology of the pathogenic species of Typhula. Trans Myc Soc Japan 33:269–285

    Google Scholar 

  39. McCune B, Mefford MJ (1999) PC-ORD. Multivariate analysis of ecological data. Version 5.0. MjM Software, Gleneden Beach, Oregon, USA

  40. Mille-Lindblom C, von Wachenfeldt E, Tranvik LJ (2004) Ergosterol as a measure of living fungal biomass: persistence in environmental samples after fungal death. J Microbiol Meth 59:253–262

    Article  CAS  Google Scholar 

  41. Monson RK, Lipson DL, Burns SP, Turnipseed AA, Delany AC, Williams MW, Schmidt SK (2006) Winter forest soil respiration controlled by climate and microbial community composition. Nature 439:711–714

    Article  PubMed  CAS  Google Scholar 

  42. Mühlmann O, Peintner U (2008) Ectomycorrhiza of Kobresia myosuroides at a primary successional glacier forefront. Mycorrhiza 18:355–362

    Article  PubMed  Google Scholar 

  43. Mühlmann O, Peintner U (2008) Mycobionts of Salix herbacea on a glacier forefront in the Austrian Alps. Mycorrhiza 18:171–180

    Article  PubMed  Google Scholar 

  44. Mühlmann O, Bacher M, Peintner U (2008) Polygonum viviparum mycobionts on an alpine primary successional glacier forefront. Mycorrhiza 18:87–95

    Article  PubMed  Google Scholar 

  45. Nemergut DR, Costello EK, Meyer AF, Pescador MY, Weintraub MN, Schmidt SK (2005) Structure and function of alpine and arctic soil microbial communities. Res Microbiol 156:775–784

    Article  PubMed  Google Scholar 

  46. Newell SY, Miller JD, Fallon RD (1987) Ergosterol content of salt-marsh fungi: effect of growth conditions and mycelial age. Mycologia 79:688–695

    Article  CAS  Google Scholar 

  47. O’Donnell K (1993) Fusarium and its near relatives. In: Reynolds DR, Taylor JW (eds) The fungal holomorph: mitotic, meiotic and pleomorphic speciation in fungal systematics. CAB International, Wallingford, pp 225–233

    Google Scholar 

  48. Oberkofler I, Peintner U (2008) Detection of soil fungal communities in an alpine primary successional habitat: does pooling of DNA extracts affect investigations? Ann Microbiol 58:585–595

    Article  Google Scholar 

  49. Peintner U, Iotti M, Klotz P, Bonuso E, Zambonelli A (2007) Soil fungal communities in a Castanea sativa (chestnut) forest producing large quantities of Boletus edulis sensu lato (porcini): where is the mycelium of porcini? Environ Microbio 9:880–889

    Article  CAS  Google Scholar 

  50. Pietikåinen J, Pettersson M, Baath E (2005) Comparison of temperature effects on soil respiration and bacterial and fungal growth rates. FEMS Microbiol Ecol 52:49–58

    Article  PubMed  Google Scholar 

  51. Raffl C (1999) Vegetationsgradienten und Sukzessionsmuster in einem zentralalpinen Gletschervorfeld (Ötztaler Alpen, Tirol). Diploma thesis, Department of Botany, University of Innsbruck, Austria

  52. Raffl C, Erschbamer B (2004) Comparative vegetation analyses of two transects crossing a characteristic glacier valley in the Central Alps. Phytocoenologia 34:225–240

    Article  Google Scholar 

  53. Raffl C, Mallaun M, Mayer R, Erschbamer B (2006) Vegetation succession pattern and diversity changes in a glacier valley, Central Alps, Austria. Arctic Antarctic Alpine Res 38:421–428

    Article  Google Scholar 

  54. Robinson CH (2001) Cold adaptation in Arctic and Antarctic fungi. New Phytol 151:341–353

    Article  CAS  Google Scholar 

  55. Rotheray TD, Jones TH, Fricker MD, Boddy L (2008) Grazing alters network architecture during interspecific mycelial interactions. Fungal Ecol 1:124–132

    Article  Google Scholar 

  56. Schadt CW, Martin AP, Lipson DA, Schmidt SK (2003) Seasonal dynamics of previously unknown fungal lineages in tundra soils. Science 301:1359–1361

    Article  PubMed  CAS  Google Scholar 

  57. Schimel JP, Bilbrough C, Welker JM (2004) Increased snow depth affects microbial activity and nitrogen mineralization in two Arctic tundra communities. Soil Biol Biochem 36:217–227

    Article  CAS  Google Scholar 

  58. Schinner F, Öhlinger R, Kandeler E, Margesin R (eds) (1996) Methods in soil biology. Springer, Berlin

    Google Scholar 

  59. Schlichtling E, Blume H-P, Stahr K (1995) Bodenkundliches Praktikum. Blackwell Wissenschafts-Verlag Berlin, Wien

    Google Scholar 

  60. Schmidt SK, Lipson DA (2004) Microbial growth under the snow: implications for nutrient and allelochemical availability in temperate soils. Plant Soil 259:1–7

    Article  CAS  Google Scholar 

  61. Schmidt SK, Wilson KL, Meyer AF, Gebauer MM, King AJ (2008) Phylogeny and ecophysiology of opportunistic snow molds from a subalpine forest ecosystem. Microb Ecol 56:681–687

    Article  PubMed  CAS  Google Scholar 

  62. Selosse M-A, Vohník M, Chauvet E (2008) Out of the rivers: are some aquatic hyphomycetes plant endophytes? New Phytol 178:3–7

    Article  PubMed  Google Scholar 

  63. Simms HR (1967) On the ecology of Herpotricha nigra. Mycologia 59:902–909

    Article  Google Scholar 

  64. Sømme L (1993) Living in the cold. Insects and other terrestrial arthropods in alpine and polar areas. Biologist 40:14–17

    Google Scholar 

  65. Sømme L, Block W (1982) Cold hardiness of Collembola at Signy Island, maritime Antarctic. Oikos 38:168–176

    Article  Google Scholar 

  66. Stahl PD, Parkin TB (1996) Relationship of soil ergosterol concentration and fungal biomass. Soil Biol Biochem 28:847–855

    Article  CAS  Google Scholar 

  67. Thomas A, Nicholas P, Parkinson D (1965) Modification of the agar film technique for assaying lengths of mycelium in soil. Nature 205:105

    Article  Google Scholar 

  68. Tibbett M, Cairney JWG (2007) The cooler side of mycorrhizas: their occurrence and functioning at low temperatures. Can J Bot 85:51–62

    Article  Google Scholar 

  69. Tilston EL, Sparrman T, Öquist MG (2010) Unfrozen water content moderates temperature dependence of sub-zero microbial respiration. Soil Biol Biochem 42:1396–1407

    Article  CAS  Google Scholar 

  70. Tscherko D, Rustemeier J, Richter A, Wanek W, Kandeler E (2003) Functional diversity of the soil microflora in primary succession across two glacier forelands in the Central Alps. Eur J Soil Sci 54:685–696

    Article  Google Scholar 

  71. Tscherko D, Hammesfahr U, Marx MC, Kandeler E (2004) Shifts in rhizosphere microbial communities and enzyme activity of Poa alpina across an alpine chronosequence. Soil Biol Biochem 36:1685–1698

    Article  CAS  Google Scholar 

  72. Tscherko D, Hammesfahr U, Zeltner G, Kandeler E, Bocker R (2005) Plant succession and rhizosphere microbial communities in a recently deglaciated alpine terrain. Basic and Applied Ecology 6:367–383

    Article  CAS  Google Scholar 

  73. Tscherko D, Hammesfahr U, Zeltner G, Kandeler E, Böcker R (2007) Soil microflora function and composition in recently deglaciated alpine terrain: impact of early and late coloniser plants. Basic Appl Ecol 6:367–383

    Article  Google Scholar 

  74. Turchetti B, Buzzini P, Goretti M, Branda E, Diolaiuti G, D’Agata C, Smiraglia C, Vaughan-Martini A (2008) Psychrophilic yeasts in glacial environments of Alpine glaciers. FEMS Microbiol Ecol 63:73–83

    Article  PubMed  CAS  Google Scholar 

  75. Uchida M, Mo W, Nakatsubo T, Tsuchiya Y, Horikoshi T, Koizumi H (2005) Microbial activity and litter decomposition under snow cover in a cool-temperate broad-leaved deciduous forest. Agricult Forest Meterol 134:102–109

    Article  Google Scholar 

  76. Wallander H, Nilsson LO, Hagerberg D, Baath E (2001) Estimation of the biomass and seasonal growth of external mycelium of ectomycorrhizal fungi in the field. New Phytol 151:753–760

    Article  CAS  Google Scholar 

  77. Wardle DA, Bardgett RD, Klironomos JN, Setälä H, van der Putten WH, Wall DH (2004) Ecological linkages between aboveground and belowground biota. Science 304:1629–1633

    Article  PubMed  CAS  Google Scholar 

  78. Weete JD, Abril M, Blackwell M (2010) Phylogenetic distribution of fungal sterols. PLoS One 5:e10899

    Article  PubMed  Google Scholar 

  79. White TJ, Bruns T, Lee S, Taylor J (1990) Amplification and direct sequencing of fungal ribosomal RNA genes for phylogenetics. In: Michael AI et al (eds) PCR protocols: a guide to methods and applications. Academic, New York

    Google Scholar 

  80. Zeller V, Bahn M, Aichner M, Tappeiner U (2000) Impact of land-use change on nitrogen mineralization in subalpine grasslands in the Southern Alps. Biol Fert Soils 31:441–448

    Article  CAS  Google Scholar 

  81. Zeller V, Bardgett RD, Tappeiner U (2001) Site and management effects on soil microbial properties of subalpine meadows: a study of land abandonment along a north-south gradient in the European Alps. Soil Biol Biochem 33:639–649

    Article  CAS  Google Scholar 

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Acknowledgments

This study was funded by the FWF Project P17910-B03 “Seasonal dynamics of underground fungal communities in an alpine environment.” Thanks to Margit Bacher, Margreth Fleisch, and Oliver Mühlmann for their assistance with sampling and to Rüdiger Kaufmann for soil temperature and moisture.

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  1. Institute of Microbiology, University of Innsbruck, Technikerstr. 25, 6020, Innsbruck, Austria

    Regina Kuhnert, Irmgard Oberkofler & Ursula Peintner

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  1. Regina Kuhnert
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  2. Irmgard Oberkofler
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  3. Ursula Peintner
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Correspondence to Ursula Peintner.

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Supplementary Table 1

Fungal taxa (OTUs) recovered in ingrowth mesh bags buried during winter in snow-covered soil with Kobresia, Polygonum, or Salix vegetation or in unvegetated soil. OTUs were identified based on 97% rDNA ITS sequence similarities. OTUs with lower sequence homology were identified on genus level or on a lower taxonomic rank. The GenBank accession number, similarity, and BLAST score are provided for the best BLAST match. OTUs are sorted based on abundances (number of clones). (DOC 270 kb)

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Kuhnert, R., Oberkofler, I. & Peintner, U. Fungal Growth and Biomass Development is Boosted by Plants in Snow-Covered Soil. Microb Ecol 64, 79–90 (2012). https://doi.org/10.1007/s00248-011-0001-y

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