Advertisement

Microbial Ecology

, Volume 76, Issue 1, pp 156–168 | Cite as

Fungal Communities and Functional Guilds Shift Along an Elevational Gradient in the Southern Appalachian Mountains

  • Allison M. Veach
  • C. Elizabeth Stokes
  • Jennifer Knoepp
  • Ari Jumpponen
  • Richard Baird
Fungal Microbiology

Abstract

Nitrogen deposition alters forest ecosystems particularly in high elevation, montane habitats where nitrogen deposition is greatest and continues to increase. We collected soils across an elevational (788–1940 m) gradient, encompassing both abiotic (soil chemistry) and biotic (vegetation community) gradients, at eight locations in the southern Appalachian Mountains of southwestern North Carolina and eastern Tennessee. We measured soil chemistry (total N, C, extractable PO4, soil pH, cation exchange capacity [ECEC], percent base saturation [% BS]) and dissected soil fungal communities using ITS2 metabarcode Illumina MiSeq sequencing. Total soil N, C, PO4, % BS, and pH increased with elevation and plateaued at approximately 1400 m, whereas ECEC linearly increased and C/N decreased with elevation. Fungal communities differed among locations and were correlated with all chemical variables, except PO4, whereas OTU richness increased with total N. Several ecological guilds (i.e., ectomycorrhizae, saprotrophs, plant pathogens) differed in abundance among locations; specifically, saprotroph abundance, primarily attributable to genus Mortierella, was positively correlated with elevation. Ectomycorrhizae declined with total N and soil pH and increased with total C and PO4 where plant pathogens increased with total N and decreased with total C. Our results demonstrate significant turnover in taxonomic and functional fungal groups across elevational gradients which facilitate future predictions on forest ecosystem change in the southern Appalachians as nitrogen deposition rates increase and regional temperature and precipitation regimes shift.

Keywords

ITS2 gene sequencing Fungal ecology Coweeta hydrologic laboratory Great Smoky Mountains Soil chemistry 

Notes

Acknowledgements

Appreciation is extended to Highlands Biological Station, Highlands, NC for the Grant-In-Aids financial support awarded to R. Baird. We thank Jason Love, Coweeta LTER Site Manager, for field assistance, Shawn Brown for laboratory and bioinformatics assistance, and Alina Akhunova at the Kansas State University Integrated Genomics Facility for assistance and preparation of ITS library sequencing. Additional laboratory facilities were provided by Mississippi State University. Soil sample collection and chemical analyses were supported by NSF grants DEB0218001 and DEB0823293 to the Coweeta LTER program at the University of Georgia and by USDA Forest Service, Southern Research Station, Coweeta Hydrologic Laboratory project funds.

Supplementary material

248_2017_1116_MOESM1_ESM.xlsx (21 kb)
ESM 1 (XLSX 21 kb)

References

  1. 1.
    Cannon PF, Sutton BC (2004) Microfungi on wood and plant debris. In: Foster MS, Bills GF, Mueller GM (eds) Biodiversity of fungi: inventory and monitoring methods. Elsevier, Amsterdam, pp 217–239CrossRefGoogle Scholar
  2. 2.
    Baird RE, Watson CE, Woolfolk S (2007) Microfungi from bark of healthy and damaged American beech, Frasier fir, and eastern hemlock trees during an all taxa biodiversity inventory in forests of the great Smoky Mountains National Park. Southeast. Nat. 6:67–82CrossRefGoogle Scholar
  3. 3.
    Baird RE, Woolfolk S, Watson CE (2009) Microfungi of forest litter from healthy American beech, Fraser fir, and eastern hemlock stands in great Smoky Mountains National Park. Southeast. Nat. 8:609–630CrossRefGoogle Scholar
  4. 4.
    Baird RE, Wallace L, Baker G, Scruggs M (2013) Stipitate hydnums of the temperate southeastern united state. Fungal Divers 62:41–114CrossRefGoogle Scholar
  5. 5.
    Schoch CL, Seifert KA, Huhndorf S, Robert V, Spouge JL, Levesque CA, Chen W, Fungal Barcoding Consortium (2012) Nuclear ribosomal internal transcribed spacer (ITS) region as a universal DNA barcode marker for fungi. Proc Natl Acad Sci U S A 109:6241–6246CrossRefPubMedPubMedCentralGoogle Scholar
  6. 6.
    Lindahl BD, Nilsson RH, Tedersoo L, Abarenkov K, Carlsen T, Kjoller R, Kõljalg U, Pennanen T, Rosendahl S, Stenlid J, Kauserud H (2013) Fungal community analysis by high-throughput sequencing of amplified markers – a user’s guide. New Phytol. 199:288–299CrossRefPubMedPubMedCentralGoogle Scholar
  7. 7.
    Toljander JF, Eberhardt U, Toljander YK, Paul LR, Yalor AF (2006) Species composition of an ectomycorrhizal fungal community along a local nutrient gradient in a boreal forest. New Phytol. 170:873–883CrossRefPubMedGoogle Scholar
  8. 8.
    Lauber CL, Strickland MS, Bradford MA, Fierer N (2008) The influence of soil properties on the structure of bacterial and fungal communities across land-use types. Soil Biol. Biochem. 40:2407–2415CrossRefGoogle Scholar
  9. 9.
    Allison SD, Hanson CA, Treseder KK (2007) Nitrogen fertilization reduces diversity and alters community structure of active fungi in boreal ecosystems. Soil Biol. Biochem. 39:1878–1887CrossRefGoogle Scholar
  10. 10.
    Avis PG (2003) The effects of long-term nitrogen fertilization on the ectomycorrhizal communities of a temperate deciduous ecosystem. Dissertation, University of MinnesotaGoogle Scholar
  11. 11.
    Trudell SA, Edmonds RL (2004) Macrofungus communities correlate with moisture and nitrogen abundance in two old-growth conifer forests, Olympic National Park, Washington, USA. Can. J. Bot. 82:781–883CrossRefGoogle Scholar
  12. 12.
    Arnold EEF (1991) Decline of ectomycorrhizal fungi in Europe. Agric. Ecosyst. Environ. 35:209–244CrossRefGoogle Scholar
  13. 13.
    Arnold AE, Lamit LJ, Gehring CA, Bidartondo MI, Callahan H (2010) Interwoven branches of the plant and fungal trees of life. New Phytol. 185:874–878CrossRefPubMedGoogle Scholar
  14. 14.
    Driscoll CT, Whitall D, Aber J, Boyer E, Castro M, Cronan C, Goodale CL, Groffman P, Hopkinson C, Lambert K, Lawrence G, Ollinger S (2003) Nitrogen pollution in the northeastern United States: sources, effects, and management options. Bioscience 53:357–374CrossRefGoogle Scholar
  15. 15.
    Baumgardner R, Lavery TF, Rogers CM, Isil SS (2002) Estimates of the atmospheric deposition of sulfur and nitrogen species: clean air status and trends network, 1990-2000. Environ Sci Technol 36:2614–2629CrossRefPubMedGoogle Scholar
  16. 16.
    Knoepp JD, Vose JM, Swank WT (2008) Nitrogen deposition and cycling across an elevation and vegetation gradients in southern Appalachian forests. Int. J. Environ. Stud. 65:391–410CrossRefGoogle Scholar
  17. 17.
    IPCC (2014) Climate change 2014: synthesis report. Contribution of Working Groups I, II and III to the Fifth Assessment Report of the Intergovernmental Panel on Climate Change. In: Core Writing Team, Pachauri RK, Meyer LA (eds). IPCC, Geneva. IPCC ARS Synthesis Report website: http://ar5-syr.ipcc.ch
  18. 18.
    Vitousek PM, Aber JD, Howarth RW, Likens GE, Matson PA, Schindler DW, Schlesinger WH, Tilman DG (1997) Human alteration of the global nitrogen cycle: sources and consequences. Ecol. Appl. 7:737–750Google Scholar
  19. 19.
    Aber J, McDowell W, Nadelhoffer K, Magill A, Berntson G, Kamakea M, McNulty S, Currie W, Rustad L, Fernandez I (1998) Nitrogen saturation in temperate forest ecosystems. Bioscience 48:921–934CrossRefGoogle Scholar
  20. 20.
    Coker WC, Beers AH (1951) The stipitate hydnums of the eastern United States. Chapel HillGoogle Scholar
  21. 21.
    Newton AC, Holden E, Davy LM, Ward SD, Fleming LV, Watling R (2002) Status and distribution of stipitate hydnoid fungi in Scottish coniferous forests. Biol. Conserv. 107:181–192CrossRefGoogle Scholar
  22. 22.
    Knoepp JD, Swank WT (1998) Rates of nitrogen mineralization across an elevation and vegetation gradients in the southern Appalachians. Plant Soil 204:235–241CrossRefGoogle Scholar
  23. 23.
    Knoepp JD, Coleman DD, Crossley DA, Clark JS (2000) Biological indices of soil quality: an ecosystem case study of their use. For Ecol Manag 138:357–368CrossRefGoogle Scholar
  24. 24.
    Elliott KJ, Vose JM (2011) The contribution of Coweeta hydrologic laboratory to developing an understanding of long-term (1934-2008) changes in managed and unmanaged forests. For Ecol Manag 261:900–910CrossRefGoogle Scholar
  25. 25.
    USEPA (1983) Methods for chemical analysis of water and waste. Determination of nitrogen as ammonia. Method 350.1, environmental monitoring and support laboratory, Office of Research and Development, USEPA, CincinnatiGoogle Scholar
  26. 26.
    Kuo S (1996) Phosphorus. In: Sparks DL (ed) Methods of soil analysis, part 3 – chemical methods, Madison, pp 869–920Google Scholar
  27. 27.
    Miniat CF, Brown CL, Harper C, Gregory S, Welch B (2014) Procedures for chemical analysis at the Coweeta hydrologic laboratory. Coweeta files. Coweeta Hydrologic Laboratory, Otto, p 206Google Scholar
  28. 28.
    Berry D, Mahfoudh KB, Wagner M, Loy A (2011) Barcoded primers used in multiplex amplicon pyrosequencing bias amplification. Appl Environ Microbiol 77:7846–7849CrossRefPubMedPubMedCentralGoogle Scholar
  29. 29.
    Gardes M, Bruns TD (1993) ITS primers with enhanced specificity for basidiomycetes-application to the identification of mycorrhizae and rusts. Mol Ecol 2:113–138CrossRefPubMedGoogle Scholar
  30. 30.
    Schloss PD, Westcott SL, Ryabin T, Hall JR, Hartmann M, Hollister EB, Lesniewski RA, Oakley BB, Parks DH, Robinson CJ, Sahl JW, Stres B, Thallinger GG, Van Horn DJ, Weber CF (2009) Introducing mothur: open-source, platform-independent, community-supported software for describing and comparing microbial communities. Appl Environ Microbiol 75:7537–7541CrossRefPubMedPubMedCentralGoogle Scholar
  31. 31.
    Huse SM, Dethlefsen L, Huber JA, Welch DM, Relman DA, Sogin ML (2008) Exploring microbial diversity and taxonomy using SSU rRNA hypervariable tag sequencing. PLoS Genet 4:1–10CrossRefGoogle Scholar
  32. 32.
    Edgar RC, Haas BJ, Clemente JC, Quince C, Knight R (2011) UCHIME improves sensitivity and speed of chimera detection. Bioinformatics 27:2194–2200CrossRefPubMedPubMedCentralGoogle Scholar
  33. 33.
    Wang Q, Garrity GM, Cole JR (2007) Naïve Bayesian classifier for rapid assignment of rRNA sequences into the new bacterial taxonomy. Appl Environ Microbiol 73:5261–5267CrossRefPubMedPubMedCentralGoogle Scholar
  34. 34.
    Tedersoo L, Nilsson RH, Abarenkov K, Jairus T, Sadam A, Saar I, Bahram M, Bechem E, Chuyong G, Kõljalg U (2010) 454 pyrosequencing and sanger sequencing of tropical mycorrhizal fungi provide similar results but reveal substantial methodological biases. New Phytol 188:291–301CrossRefPubMedGoogle Scholar
  35. 35.
    Brown SP, Veach AM, Rigdon-Huss AR, Grond K, Licktieg SK, Lothamer K, Oliver AK, Jumpponen A (2015) Scraping the bottom of the barrel: are rare high throughput sequences artifacts? Fungal Ecol 13:221–225CrossRefGoogle Scholar
  36. 36.
    Harrell F, Dupont C (2017) Hmisc: Harrell Miscellaneous. R package. http://biostat.mc.vanderbilt.edu/Hmisc
  37. 37.
    Pohlert T (2016) PMCMR: calculate pairwise multiple comparisons of mean rank sums. R package. https://CRAN.R-project.org/package=PMCMR
  38. 38.
    Chambers JM (1992) Linear models. In: Chambers JM, Hastie TJ (eds) Statistical models in S. Chapman & Hall/CRC, Boca Raton, pp 95–138Google Scholar
  39. 39.
    Symonds MRE, Moussalli A (2011) A brief guide to model selection, multimodal interference and model averaging in behavioural ecology using Akaike’s information criterion. Behav Ecol Sociobiol 65:13–21CrossRefGoogle Scholar
  40. 40.
    Venables WN, Ripley BD (2002) Modern applied statistics. Springer, New YorkCrossRefGoogle Scholar
  41. 41.
    Oksanen J, Blanchet FG, Friendly M, Kindt R, Legendre P, McGlinn D, Minchin PR, O’Hara RB, Simpson GL, Solymos P, Stevens MHH, Szoecs E, Wagner H (2017) Package vegan. R package. https://CRAN.R-project.org/package=vegan
  42. 42.
    Anderson MJ (2001) A new method for non-parametric multivariate analysis of variance. Austral Ecol 26:32–46Google Scholar
  43. 43.
    Hervé M (2017) RVAideMemoire: diverse basic statistical and graphical functions. R package. https://CRAN.R-project.org/package=RVAideMemoire
  44. 44.
    Nguyen NH, Song Z, Bates ST, Branco S, Tedersoo L, Menke L, Schilling JS, Kennedy PG (2015) FUNGuild: an open annotation tool for parsing fungal community datasets by ecological guild. Fungal Ecol 20:241–248CrossRefGoogle Scholar
  45. 45.
    R Core Team (2016) R: a language and environment for statistical computing. R Foundation for Statistical Computing, ViennaGoogle Scholar
  46. 46.
    Tedersoo L, Bahram M, Põlme S, Kõljalg 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, Põldmaa K, Piepenbring M, Phosri C, Peterson M, Parts K, Pärtel 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 L, Greslebin A, Grelet G, Geml J, Gates G, Dunstan W, Dunk C, Drenkhan R, Dearnaley J, Kesel AD, Dan T, Chen X, Buegger F, Brearley FQ, Bonito G, Anslan S, Abell S, Abarenkov K (2014) Global diversity and geography of soil fungi. Science 346:1078CrossRefGoogle Scholar
  47. 47.
    Kivlin SN, Hawkes CV, Treseder KK (2011) Global diversity and distribution of arbuscular mycorrhizal fungi. Soil Biol Biochem 43:2294–2303CrossRefGoogle Scholar
  48. 48.
    Weber CF, Vilgalys R, Kuske CR (2013) Changes in fungal community composition in response to elevated atmospheric CO2 and nitrogen fertilization varies with soil horizon. Front Microbiol 4:1–14CrossRefGoogle Scholar
  49. 49.
    Lilleskov EA, Fahey TJ, Horton TR, Lovett GM (2002) Belowground ectomycorrhizal fungal community change over a nitrogen deposition gradient in Alaska. Ecology 83:104–115CrossRefGoogle Scholar
  50. 50.
    Teseder KK (2004) A meta-analysis of mycorrhizal responses to nitrogen, phosphorus, and atmospheric CO2 in field studies. New Phytol 164:347–355CrossRefGoogle Scholar
  51. 51.
    Paungfoo-Lonhienne C, Yeoh YK, Kasinadhuni NRP, Lonhienne TGA, Robinson N, Hugenholtz P, Ragan MA, Schmidt S (2015) Nitrogen fertilizer dose alters fungal communities in sugarcane soil and rhizosphere. Sci Rep 5:8678.  https://doi.org/10.1038/srep08678 CrossRefPubMedPubMedCentralGoogle Scholar
  52. 52.
    Li Y, Schichtel BA, Walker JT, Schwede DB, Chen X, Lehmann CN, Puchalski MA, Gay DA, Collett JL (2016) Increasing importance of deposition of reduced nitrogen in the United States. Proc Natl Acad Sci U S A 113:5474–5879Google Scholar
  53. 53.
    Kircher M, Kelso J (2010) High-throughput DNA sequencing—concepts and limitations. BioEssays 32:524–536CrossRefPubMedGoogle Scholar
  54. 54.
    Walker JF, Miller Jr OK, Horton JL (2005) Hyperdiversity of ectomycorrhizal fungus assemblages on oak seedlings in mixed forests in the southern Appalachian Mountains. Mol Ecol 14:829–838CrossRefPubMedGoogle Scholar
  55. 55.
    Toju H, Sato H, Yamamoto S, Kadowaki K, Tanabe AS, Yazawa S, Nishimura O, Agata K (2013) How are plant and fungal communities linked to each other in belowground ecosystems? A massively parallel pyrosequencing analysis of the association specificity of root-associated fungi and their host plants. Ecol Evol 3:3112–3124CrossRefPubMedPubMedCentralGoogle Scholar
  56. 56.
    Hui N, Jumpponen A, Francini G, Kotze DJ, Liu X, Romantschuk ML, Strömmer RH, Setälä HM (2017) Soil microbial communities are shaped by vegetation type and park age in cities under cold climate. Environ Microbiol 19:1281–1295CrossRefPubMedGoogle Scholar
  57. 57.
    Bezemer TM, Lawson CS, Hedlund K, Edwards AR, Brook AJ, Igual JM, Mortimer SR, Van der Putten WH (2006) Plant species and functional group effects on abiotic and microbial soil properties and plant-soil feedback responses in two grasslands. J Ecol 94:893–904CrossRefGoogle Scholar
  58. 58.
    Uroz S, Oger P, Tisserand E, Cébron A, Turpault MP, Buée M, De Boer W, Leveau JHJ, Frey- Klett P (2016) Specific impacts of beech and Norway spruce on the structure and diversity of the rhizosphere and soil microbial communities. Sci Rep 6:27756.  https://doi.org/10.1038/srep27756 CrossRefPubMedPubMedCentralGoogle Scholar
  59. 59.
    Sundqvist MK, Sander NJ, Wardle DA (2013) Community and ecosystem responses to elevational gradients: processes, mechanisms, and insights for global change. Annu Rev Ecol 44:261–280CrossRefGoogle Scholar
  60. 60.
    Baird R, Stokes CE, Wood-Jones A, Alexander M, Watson C, Taylor G, Johnson K, Diehl S (2014) Fleshy ectomycorrhizal fungal community associated with healthy and declining eastern hemlock stands in great Smoky Mountains National Park. Southeast Nat 13:192–218CrossRefGoogle Scholar
  61. 61.
    Verbeken A, Nuytinck J (2013) Not every milkcap is a Lactarius. Scripta Botan Belg 51:162–168Google Scholar
  62. 62.
    Baird R, Stokes CE, Wood-Jones A, Alexander M, Watson C, Taylor G, Johnson K, Threadgill P, Diehl S (2014) A molecular clone and culture inventory of the root fungal community associated with eastern hemlock in great Smoky Mountains national park. Southeast Nat 13:219–237CrossRefGoogle Scholar
  63. 63.
    Baird R, Stokes CE, Frampton J, Smith B, Watson C, Pilgram C, Scruggs M (2014) Density and diversity of ectomycorrhizal fungal community present in high elevation Fraser fir of great Smoky Mountains National Park. North Am Fungi 9:1–21CrossRefGoogle Scholar
  64. 64.
    Baird R, Wood-Jones CA, Varco J, Watson C, Starrett W, Taylor G, Johnson K (2014) Rhododendron decline in great Smoky Mountains and surrounding areas: intensive site study of biotic and abiotic parameters associated with the decline. Southeast Nat 13:1–25CrossRefGoogle Scholar
  65. 65.
    Bills GF, Holtzman GI, Miller OK (1986) Comparison of ectomycorrhizal-basidiomycete communities in red spruce versus northern hardwood forests of West Virginia. Can J Bot 64:760–768CrossRefGoogle Scholar
  66. 66.
    Bird C, McCleneghan C (2005) Morphological and functional diversity of EM fungi on Roan Mountain (NC/TN). Southeast Nat 4:121–132CrossRefGoogle Scholar
  67. 67.
    Suvi T, Tedersoo L, Abarenkov K, Beaver K, Gerlach J, Kõljalg U (2010) Mycorrhizal symbionts of Pisonia grandis and P. sechellarum in Seychelles: identification of mycorrhizal fungi and description of new Tomentella species. Mycologia 102:522–533CrossRefPubMedGoogle Scholar
  68. 68.
    Lilleskov EA, Bruns TD (2005) Spore dispersal of a resupinate ectomycorrhizal fungus, Tomentella sublilacina, via soil food webs. Mycologia 97:762–769CrossRefPubMedGoogle Scholar
  69. 69.
    Watanabe T (1994) Pictorial atlas of soil and seed fungi: morphologies of cultured fungi and key to species. CRC Press LLC, Boca RatonGoogle Scholar
  70. 70.
    Kirk PM, Cannon PF, Minter DW, Stalpers JA (2008) Dictionary of the fungi10th edn. Cromwell Press, TrowbridgeGoogle Scholar
  71. 71.
    Leite DP, Amadio JVRS, Martins ER, Simões SAA, Yamamoto ACA, Leal-Santos FA, Takahara DT, Hahn RC (2012) Cryptococcus spp isolated from dust microhabitat in Brazilian libraries. J Ocul Med Toxicol 7:11CrossRefGoogle Scholar
  72. 72.
    Reverchon F, Ortega-Larrocea MP, Pérez-Moreno J (2010) Saprophytic fungal communities change in diversity and species composition across a volcanic soil chronosequence at sierra del Chichinautzin, Mexico. Ann Microbiol 60:217–226CrossRefGoogle Scholar

Copyright information

© Springer Science+Business Media, LLC, part of Springer Nature 2017

Authors and Affiliations

  1. 1.Division of BiologyKansas State UniversityManhattanUSA
  2. 2.Oak Ridge National Laboratory, Biosciences DivisionOak RidgeUSA
  3. 3.Department of Forest ProductsMississippi State UniversityStarkvilleUSA
  4. 4.Department of Biochemistry, Molecular Biology, Entomology, and Plant PathologyMississippi State UniversityStarkvilleUSA
  5. 5.USDA, Forest Service, Southern Research Station, Center for Forest Watershed Research, Coweeta Hydrologic LaboratoryOttoUSA

Personalised recommendations