Skip to main content

Temperate Forests Dominated by Arbuscular or Ectomycorrhizal Fungi Are Characterized by Strong Shifts from Saprotrophic to Mycorrhizal Fungi with Increasing Soil Depth

Microbial Ecology volume 82, pages 377–390 (2021)Cite this article

Abstract

In temperate and boreal forests, competition for soil resources between free-living saprotrophs and ectomycorrhizal (EcM) fungi has been suggested to restrict saprotrophic fungal dominance to the most superficial organic soil horizons in forests dominated by EcM trees. By contrast, lower niche overlap with arbuscular mycorrhizal (AM) fungi could allow fungal saprotrophs to maintain this dominance into deeper soil horizons in AM-dominated forests. Here we used a natural gradient of adjacent forest patches that were dominated by either AM or EcM trees, or a mixture of both to determine how fungal communities characterized with high-throughput amplicon sequencing change across organic and mineral soil horizons. We found a general shift from saprotrophic to mycorrhizal fungal dominance with increasing soil depth in all forest mycorrhizal types, especially in organic horizons. Vertical changes in soil chemistry, including pH, organic matter, exchangeable cations, and extractable phosphorus, coincided with shifts in fungal community composition. Although fungal communities and soil chemistry differed among adjacent forest mycorrhizal types, variations were stronger within a given soil profile, pointing to the importance of considering horizons when characterizing soil fungal communities. Our results also suggest that in temperate forests, vertical shifts from saprotrophic to mycorrhizal fungi within organic and mineral horizons occur similarly in both ectomycorrhizal and arbuscular mycorrhizal forests.

This is a preview of subscription content, access via your institution.

Access options

Buy single article

Instant access to the full article PDF.

43,34 €

Price includes VAT (Finland)
Tax calculation will be finalised during checkout.

Fig. 1
Fig. 2
Fig. 3
Fig. 4
Fig. 5
Fig. 6

Data Availability

Sequence and chemistry data can be accessed at https://doi.org/10.5281/zenodo.3631861.

References

  1. Frey SD (2019) Mycorrhizal fungi as mediators of soil organic matter dynamics. Annu Rev Ecol Evol Syst 50:237–259. https://doi.org/10.1146/annurev-ecolsys-110617-062331

    Article  Google Scholar 

  2. Kubartová A, Ranger J, Berthelin J, Beguiristain T (2008) Diversity and decomposing ability of saprophytic fungi from temperate forest litter. Microb Ecol 58:98–107. https://doi.org/10.1007/s00248-008-9458-8

    Article  PubMed  Google Scholar 

  3. Crowther TW, Hoogen J van den, Wan J, et al (2019) The global soil community and its influence on biogeochemistry. Science 365:eaav0550. https://doi.org/10.1126/science.aav0550

  4. Brundrett MC (2017) Global diversity and importance of mycorrhizal and nonmycorrhizal plants. Biogeography of Mycorrhizal Symbiosis. Springer, Cham, pp 533–556

    Chapter  Google Scholar 

  5. Steidinger BS, Crowther TW, Liang J et al (2019) Climatic controls of decomposition drive the global biogeography of forest-tree symbioses. Nature 569:404–408. https://doi.org/10.1038/s41586-019-1128-0

    CAS  Article  PubMed  Google Scholar 

  6. Dickie IA, Koele N, Blum JD, Gleason JD, McGlone MS (2014) Mycorrhizas in changing ecosystems. Botany 92:149–160. https://doi.org/10.1139/cjb-2013-0091

    CAS  Article  Google Scholar 

  7. Fernandez CW, Kennedy PG (2016) Revisiting the ‘Gadgil effect’: do interguild fungal interactions control carbon cycling in forest soils? New Phytol 209:1382–1394. https://doi.org/10.1111/nph.13648

    CAS  Article  PubMed  Google Scholar 

  8. Verbruggen E, Pena R, Fernandez CW, Soong JL (2017) Chapter 24 - mycorrhizal interactions with saprotrophs and impact on soil carbon storage. In: Mycorrhizal Mediation of Soil. Elsevier, pp 441–460

  9. Smith SE, Smith FA (2011) Roles of arbuscular mycorrhizas in plant nutrition and growth: new paradigms from cellular to ecosystem scales. Annu Rev Plant Biol 62:227–250. https://doi.org/10.1146/annurev-arplant-042110-103846

    CAS  Article  PubMed  Google Scholar 

  10. Phillips RP, Brzostek E, Midgley MG (2013) The mycorrhizal-associated nutrient economy: a new framework for predicting carbon–nutrient couplings in temperate forests. New Phytol 199:41–51. https://doi.org/10.1111/nph.12221

    CAS  Article  PubMed  Google Scholar 

  11. Hodge A (2017) Chapter 8 - accessibility of inorganic and organic nutrients for mycorrhizas. Mycorrhizal Mediation of Soil. Elsevier, In, pp 129–148

    Google Scholar 

  12. Dixon RK, Solomon AM, Brown S, Houghton RA, Trexier MC, Wisniewski J (1994) Carbon pools and flux of global forest ecosystems. Science 263:185–190. https://doi.org/10.1126/science.263.5144.185

    CAS  Article  PubMed  Google Scholar 

  13. Scharlemann JP, Tanner EV, Hiederer R, Kapos V (2014) Global soil carbon: understanding and managing the largest terrestrial carbon pool. Carbon Management 5:81–91. https://doi.org/10.4155/cmt.13.77

    CAS  Article  Google Scholar 

  14. Averill C, Turner BL, Finzi AC (2014) Mycorrhiza-mediated competition between plants and decomposers drives soil carbon storage. Nature 505:543–545. https://doi.org/10.1038/nature12901

    CAS  Article  PubMed  Google Scholar 

  15. Craig ME, Turner BL, Liang C, Clay K, Johnson DJ, Phillips RP (2018) Tree mycorrhizal type predicts within-site variability in the storage and distribution of soil organic matter. Glob Chang Biol 24:3317–3330. https://doi.org/10.1111/gcb.14132

    Article  PubMed  Google Scholar 

  16. Peršoh D, Stolle N, Brachmann A, Begerow D, Rambold G (2018) Fungal guilds are evenly distributed along a vertical spruce forest soil profile while individual fungi show pronounced niche partitioning. Mycol Prog 17:925–939. https://doi.org/10.1007/s11557-018-1405-6

    Article  Google Scholar 

  17. Bödeker ITM, Lindahl BD, Olson Å, Clemmensen KE (2016) Mycorrhizal and saprotrophic fungal guilds compete for the same organic substrates but affect decomposition differently. Funct Ecol 30:1967–1978. https://doi.org/10.1111/1365-2435.12677

    Article  Google Scholar 

  18. Mujic AB, Durall DM, Spatafora JW, Kennedy PG (2016) Competitive avoidance not edaphic specialization drives vertical niche partitioning among sister species of ectomycorrhizal fungi. New Phytol 209:1174–1183. https://doi.org/10.1111/nph.13677

    Article  PubMed  Google Scholar 

  19. Dickie IA, Xu B, Koide RT (2002) Vertical niche differentiation of ectomycorrhizal hyphae in soil as shown by T-RFLP analysis. New Phytol 156:527–535. https://doi.org/10.1046/j.1469-8137.2002.00535.x

    CAS  Article  PubMed  Google Scholar 

  20. Rosling A, Landeweert R, Lindahl BD, Larsson KH, Kuyper TW, Taylor AFS, Finlay RD (2003) Vertical distribution of ectomycorrhizal fungal taxa in a podzol soil profile. New Phytol 159:775–783. https://doi.org/10.1046/j.1469-8137.2003.00829.x

    CAS  Article  PubMed  Google Scholar 

  21. Lindahl BD, Ihrmark K, Boberg J, Trumbore SE, Högberg P, Stenlid J, Finlay RD (2007) Spatial separation of litter decomposition and mycorrhizal nitrogen uptake in a boreal forest. New Phytol 173:611–620. https://doi.org/10.1111/j.1469-8137.2006.01936.x

    CAS  Article  PubMed  Google Scholar 

  22. McGuire KL, Allison SD, Fierer N, Treseder KK (2013) Ectomycorrhizal-dominated boreal and tropical forests have distinct fungal communities, but analogous spatial patterns across soil horizons. PLoS One 8:e68278. https://doi.org/10.1371/journal.pone.0068278

    CAS  Article  PubMed  PubMed Central  Google Scholar 

  23. Santalahti M, Sun H, Jumpponen A, Pennanen T, Heinonsalo J (2016) Vertical and seasonal dynamics of fungal communities in boreal Scots pine forest soil. FEMS Microbiol Ecol 92. https://doi.org/10.1093/femsec/fiw170

  24. Clemmensen KE, Bahr A, Ovaskainen O, Dahlberg A, Ekblad A, Wallander H, Stenlid J, Finlay RD, Wardle DA, Lindahl BD (2013) Roots and associated fungi drive long-term carbon sequestration in boreal forest. Science 339:1615–1618. https://doi.org/10.1126/science.1231923

    CAS  Article  PubMed  Google Scholar 

  25. Baskaran P, Hyvönen R, Berglund SL, Clemmensen KE, Ågren GI, Lindahl BD, Manzoni S (2017) Modelling the influence of ectomycorrhizal decomposition on plant nutrition and soil carbon sequestration in boreal forest ecosystems. New Phytol 213:1452–1465. https://doi.org/10.1111/nph.14213

    CAS  Article  PubMed  Google Scholar 

  26. Kyaschenko J, Clemmensen KE, Karltun E, Lindahl BD (2017) Below-ground organic matter accumulation along a boreal forest fertility gradient relates to guild interaction within fungal communities. Ecol Lett 20:1546–1555. https://doi.org/10.1111/ele.12862

    Article  PubMed  Google Scholar 

  27. Higo M, Isobe K, Yamaguchi M, Drijber RA, Jeske ES, Ishii R (2013) Diversity and vertical distribution of indigenous arbuscular mycorrhizal fungi under two soybean rotational systems. Biol Fertil Soils 49:1085–1096. https://doi.org/10.1007/s00374-013-0807-5

    Article  Google Scholar 

  28. Montero Sommerfeld H, Díaz LM, Alvarez M, Añazco Villanueva C, Matus F, Boon N, Boeckx P, Huygens D (2013) High winter diversity of arbuscular mycorrhizal fungal communities in shallow and deep grassland soils. Soil Biol Biochem 65:236–244. https://doi.org/10.1016/j.soilbio.2013.06.002

    CAS  Article  Google Scholar 

  29. Oehl F, Sieverding E, Ineichen K, Ris EA, Boller T, Wiemken A (2005) Community structure of arbuscular mycorrhizal fungi at different soil depths in extensively and intensively managed agroecosystems. New Phytol 165:273–283. https://doi.org/10.1111/j.1469-8137.2004.01235.x

    Article  PubMed  Google Scholar 

  30. Tedersoo L, Bahram M, Zobel M (2020) How mycorrhizal associations drive plant population and community biology. Science 367:eaba1223. https://doi.org/10.1126/science.aba1223

    CAS  Article  PubMed  Google Scholar 

  31. Read DJ (1991) Mycorrhizas in ecosystems. Experientia 47:376–391. https://doi.org/10.1007/BF01972080

    Article  Google Scholar 

  32. Smith SE, Read DJ (2008) Mycorrhizal Symbiosis. Academic Press

  33. Moyersoen B, Fitter AH, Alexander IJ (1998) Spatial distribution of ectomycorrhizas and arbuscular mycorrhizas in Korup National Park rain forest, Cameroon, in relation to edaphic parameters. New Phytol 139:311–320. https://doi.org/10.1046/j.1469-8137.1998.00190.x

    Article  Google Scholar 

  34. Schulze E-D, Chapin FS, Gebauer G (1994) Nitrogen nutrition and isotope differences among life forms at the northern treeline of Alaska. Oecologia 100:406–412. https://doi.org/10.1007/BF00317862

    Article  PubMed  Google Scholar 

  35. Neville J, Tessier JL, Morrison I, Scarratt J, Canning B, Klironomos JN (2002) Soil depth distribution of ecto- and arbuscular mycorrhizal fungi associated with Populus tremuloides within a 3-year-old boreal forest clear-cut. Appl Soil Ecol 19:209–216. https://doi.org/10.1016/S0929-1393 (01)00193-7

    Article  Google Scholar 

  36. Reddell P, Malajczuk N (1984) Formation of Mycorrhizae by Jarrah (Eucalyptus marginata Donn ex Smith) in litter and soil. Aust J Bot 32:511–520. https://doi.org/10.1071/bt9840511

    Article  Google Scholar 

  37. Teste FP, Jones MD, Dickie IA (2020) Dual-mycorrhizal plants: their ecology and relevance. New Phytol 225:1835–1851. https://doi.org/10.1111/nph.16190

    Article  PubMed  Google Scholar 

  38. Allen EB, Allen MF, Helm DJ, Trappe JM, Molina R, Rincon E (1995) Patterns and regulation of mycorrhizal plant and fungal diversity. Plant Soil 170:47–62. https://doi.org/10.1007/BF02183054

    CAS  Article  Google Scholar 

  39. Bunn RA, Simpson DT, Bullington LS, Lekberg Y, Janos DP (2019) Revisiting the ‘direct mineral cycling’ hypothesis: arbuscular mycorrhizal fungi colonize leaf litter, but why? The ISME Journal 13:1891–1898. https://doi.org/10.1038/s41396-019-0403-2

    Article  PubMed  PubMed Central  Google Scholar 

  40. Teste FP, Laliberté E, Lambers H, Auer Y, Kramer S, Kandeler E (2016) Mycorrhizal fungal biomass and scavenging declines in phosphorus-impoverished soils during ecosystem retrogression. Soil Biol Biochem 92:119–132. https://doi.org/10.1016/j.soilbio.2015.09.021

    CAS  Article  Google Scholar 

  41. Tedersoo L, May TW, Smith ME (2010) Ectomycorrhizal lifestyle in fungi: global diversity, distribution, and evolution of phylogenetic lineages. Mycorrhiza 20:217–263. https://doi.org/10.1007/s00572-009-0274-x

    Article  PubMed  Google Scholar 

  42. Weete JD, Gandhi SR (1999) Sterols and fatty acids of the Mortierellaceae: taxonomic implications. Mycologia 91:642–649. https://doi.org/10.1080/00275514.1999.12061063

    CAS  Article  Google Scholar 

  43. Lindahl BD, Nilsson RH, Tedersoo L, Abarenkov K, Carlsen T, Kjøller 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 199:288–299. https://doi.org/10.1111/nph.12243

    CAS  Article  PubMed  PubMed Central  Google Scholar 

  44. 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 20:241–248. https://doi.org/10.1016/j.funeco.2015.06.006

    Article  Google Scholar 

  45. Dickie IA, John MGS (2016) Second-generation molecular understanding of mycorrhizas in soil ecosystems. Molecular Mycorrhizal Symbiosis. John Wiley & Sons, Ltd, pp 473–491

    Chapter  Google Scholar 

  46. Nilsson RH, Anslan S, Bahram M, Wurzbacher C, Baldrian P, Tedersoo L (2019) Mycobiome diversity: high-throughput sequencing and identification of fungi. Nat Rev Microbiol 17:95–109. https://doi.org/10.1038/s41579-018-0116-y

    CAS  Article  PubMed  Google Scholar 

  47. Lindahl BD, Tunlid A (2015) Ectomycorrhizal fungi – potential organic matter decomposers, yet not saprotrophs. New Phytol 205:1443–1447. https://doi.org/10.1111/nph.13201

    CAS  Article  PubMed  Google Scholar 

  48. Sterkenburg E, Clemmensen KE, Ekblad A, Finlay RD, Lindahl BD (2018) Contrasting effects of ectomycorrhizal fungi on early and late stage decomposition in a boreal forest. The ISME Journal 1:2187–2197. https://doi.org/10.1038/s41396-018-0181-2

    CAS  Article  Google Scholar 

  49. Talbot JM, Bruns TD, Taylor JW, Smith DP, Branco S, Glassman SI, Erlandson S, Vilgalys R, Liao HL, Smith ME, Peay KG (2014) Endemism and functional convergence across the north American soil mycobiome. PNAS 111:6341–6346. https://doi.org/10.1073/pnas.1402584111

    CAS  Article  PubMed  PubMed Central  Google Scholar 

  50. 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 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. https://doi.org/10.1126/science.1256688

    CAS  Article  PubMed  Google Scholar 

  51. Bahram M, Peay KG, Tedersoo L (2015) Local-scale biogeography and spatiotemporal variability in communities of mycorrhizal fungi. New Phytol 205:1454–1463. https://doi.org/10.1111/nph.13206

    CAS  Article  PubMed  Google Scholar 

  52. Zak DR, Pellitier PT, Argiroff W, Castillo B, James TY, Nave LE, Averill C, Beidler KV, Bhatnagar J, Blesh J, Classen AT, Craig M, Fernandez CW, Gundersen P, Johansen R, Koide RT, Lilleskov EA, Lindahl BD, Nadelhoffer KJ, Phillips RP, Tunlid A (2019) Exploring the role of ectomycorrhizal fungi in soil carbon dynamics. New Phytol 223:33–39. https://doi.org/10.1111/nph.15679

    Article  PubMed  Google Scholar 

  53. Brundrett M, Murase G, Kendrick B (1990) Comparative anatomy of roots and mycorrhizae of common Ontario trees. Can J Bot 68:551–578. https://doi.org/10.1139/b90-076

    Article  Google Scholar 

  54. Poulson TL, Platt WJ (1996) Replacement patterns of beech and sugar maple in warren woods, Michigan. Ecology 77:1234–1253. https://doi.org/10.2307/2265592

    Article  Google Scholar 

  55. Duchesne L, Ouimet R, Moore J-D, Paquin R (2005) Changes in structure and composition of maple–beech stands following sugar maple decline in Québec, Canada. For Ecol Manag 208:223–236. https://doi.org/10.1016/j.foreco.2004.12.003

    Article  Google Scholar 

  56. Bélanger N, Côté B, Fyles JW et al (2004) Forest regrowth as the controlling factor of soil nutrient availability 75 years after fire in a deciduous forest of Southern Quebec. Plant Soil 262:363–272. https://doi.org/10.1023/B:PLSO.0000037054.21561.85

    Article  Google Scholar 

  57. Courchesne F, Côté B, Fyles JW, Hendershot WH, Biron PM, Roy AG, Turmel MC (2005) Recent changes in soil chemistry in a forested ecosystem of southern Québec, Canada. Soil Sci Soc Am J 69:1298–1313. https://doi.org/10.2136/sssaj2003.0129

    CAS  Article  Google Scholar 

  58. Côté B, Hendershot WH, Fyles JW, Roy AG, Bradley R, Biron PM, Courchesne F (1998) The phenology of fine root growth in a maple-dominated ecosystem: relationships with some soil properties. Plant Soil 201:59–69. https://doi.org/10.1023/A:1004351705516

    Article  Google Scholar 

  59. Courchesne F, Hendershot WH (1988) Cycle annuel des éléments nutritifs dans un bassin-versant forestier: contribution de la litière fraîche. Can J For Res 18:930–936. https://doi.org/10.1139/x88-141

    Article  Google Scholar 

  60. Saucier J-P, Robitaille A, Grondin P, et al (2011) Les régions écologiques du Québec méridional (4 version). Carte à l’échelle de 1 / 1 250 000

  61. Savage C (2001) Recolonisation forestière dans les Basses Laurentides au sud du domaine climacique de l’érablière à bouleau jaune. Université de Montréal

  62. Soil Classification Working Group (1998) The Canadian system of soil classification3rd edn. NRC Research Press, Ottawa, Canada

    Google Scholar 

  63. Brundrett M, Bougher N, Dell B, et al (1996) Working with Mycorrhizas in forestry and agriculture

  64. Vierheilig H, Coughlan AP, Wyss U, Piché Y (1998) Ink and vinegar, a simple staining technique for arbuscular-mycorrhizal fungi. Appl Environ Microbiol 64:5004–5007

    CAS  Article  Google Scholar 

  65. Vierheilig H, Schweiger P, Brundrett M (2005) An overview of methods for the detection and observation of arbuscular mycorrhizal fungi in roots†. Physiol Plant 125:393–404. https://doi.org/10.1111/j.1399-3054.2005.00564.x

    CAS  Article  Google Scholar 

  66. Tennant D (1975) A test of a modified line intersect method of estimating root length. J Ecol 63:995–1001. https://doi.org/10.2307/2258617

    Article  Google Scholar 

  67. Toju H, Tanabe AS, Yamamoto S, Sato H (2012) High-coverage ITS primers for the DNA-based identification of Ascomycetes and Basidiomycetes in environmental samples. PLoS One 7:e40863. https://doi.org/10.1371/journal.pone.0040863

    CAS  Article  PubMed  PubMed Central  Google Scholar 

  68. Toju H, Sato H, Tanabe AS (2014) Diversity and spatial structure of belowground plant–fungal symbiosis in a mixed subtropical forest of ectomycorrhizal and arbuscular mycorrhizal plants. PLoS One 9:e86566. https://doi.org/10.1371/journal.pone.0086566

    CAS  Article  PubMed  PubMed Central  Google Scholar 

  69. Callahan BJ, McMurdie PJ, Rosen MJ et al (2016) DADA2: high-resolution sample inference from Illumina amplicon data. Nat Methods 13:581–583. https://doi.org/10.1038/nmeth.3869

    CAS  Article  PubMed  PubMed Central  Google Scholar 

  70. Callahan BJ, McMurdie PJ, Holmes SP (2017) Exact sequence variants should replace operational taxonomic units in marker-gene data analysis. ISME J 11:2639–2643. https://doi.org/10.1038/ismej.2017.119

    Article  PubMed  PubMed Central  Google Scholar 

  71. Thompson LR, Sanders JG, McDonald D et al (2017) A communal catalogue reveals Earth’s multiscale microbial diversity. Nature advance online publication 551:457–463. https://doi.org/10.1038/nature24621

    CAS  Article  Google Scholar 

  72. Nilsson RH, Kristiansson E, Ryberg M, Hallenberg N, Larsson KH (2008) Intraspecific ITS variability in the kingdom fungi as expressed in the international sequence databases and ITS implications for molecular species identification. Evol Bioinformatics Online 4:193–201

    Google Scholar 

  73. Rosen MJ, Callahan BJ, Fisher DS, Holmes SP (2012) Denoising PCR-amplified metagenome data. BMC Bioinformatics 13:283. https://doi.org/10.1186/1471-2105-13-283

    Article  PubMed  PubMed Central  Google Scholar 

  74. 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 186:281–285. https://doi.org/10.1111/j.1469-8137.2009.03160.x

    Article  PubMed  Google Scholar 

  75. Nguyen NH, Smith D, Peay K, Kennedy P (2015) Parsing ecological signal from noise in next generation amplicon sequencing. New Phytol 205:1389–1393. https://doi.org/10.1111/nph.12923

    CAS  Article  PubMed  Google Scholar 

  76. Pauvert C, Buée M, Laval V, Edel-Hermann V, Fauchery L, Gautier A, Lesur I, Vallance J, Vacher C (2019) Bioinformatics matters: the accuracy of plant and soil fungal community data is highly dependent on the metabarcoding pipeline. Fungal Ecol 41:23–33. https://doi.org/10.1016/j.funeco.2019.03.005

    Article  Google Scholar 

  77. Legendre P, Legendre L (2012) Numerical Ecology. Elsevier

  78. Benjamini Y, Hochberg Y (1995) Controlling the false discovery rate: a practical and powerful approach to multiple testing. J R Stat Soc Ser B Methodol 57:289–300

    Google Scholar 

  79. Anderson MJ (2006) Distance-based tests for homogeneity of multivariate dispersions. Biometrics 62:245–253. https://doi.org/10.1111/j.1541-0420.2005.00440.x

    Article  PubMed  Google Scholar 

  80. Borcard D, Gillet F, Legendre P (2018) Numerical ecology with R2nd edn. Springer International Publishing

  81. Borcard D, Legendre P, Drapeau P (1992) Partialling out the spatial component of ecological variation. Ecology 73:1045–1055. https://doi.org/10.2307/1940179

    Article  Google Scholar 

  82. Legendre P, Oksanen J, ter Braak CJF (2011) Testing the significance of canonical axes in redundancy analysis. Methods Ecol Evol 2:269–277. https://doi.org/10.1111/j.2041-210X.2010.00078.x

    Article  Google Scholar 

  83. Peres-Neto PR, Legendre P, Dray S, Borcard D (2006) Variation partitioning of species data matrices: estimation and comparison of fractions. Ecology 87:2614–2625. https://doi.org/10.1890/0012-9658(2006)87[2614:VPOSDM]2.0.CO;2

    Article  PubMed  Google Scholar 

  84. Core Team R (2018) R: a language and environment for statistical computing. R Foundation for Statistical Computing, Vienna, Austria

    Google Scholar 

  85. Wickham H, Francois R, Henry L, Müller K (2017) dplyr: a grammar of data manipulation

  86. Lenth R (2019) emmeans: estimated marginal means, aka least-squares means

  87. Wickham H (2016) ggplot2: elegant graphics for data analysis. Springer-Verlag New York

    Book  Google Scholar 

  88. Kassambara A (2018) ggpubr: “ggplot2” based publication ready plots

  89. Pinheiro J, Bates D, DebRoy S, et al (2012) nlme: linear and nonlinear mixed effects models. R package version 3:

  90. McMurdie PJ, Holmes S (2013) phyloseq: an R package for reproducible interactive analysis and graphics of microbiome census data. PLOS ONE 8:e61217. https://doi.org/10.1371/journal.pone.0061217

  91. Oksanen J, Blanchet FG, Friendly M, et al (2017) vegan: community ecology package

  92. O’Brien HE, Parrent JL, Jackson JA et al (2005) Fungal community analysis by large-scale sequencing of environmental samples. Appl Environ Microbiol 71:5544–5550. https://doi.org/10.1128/AEM.71.9.5544-5550.2005

    CAS  Article  PubMed  PubMed Central  Google Scholar 

  93. Voříšková J, Brabcová V, Cajthaml T, Baldrian P (2014) Seasonal dynamics of fungal communities in a temperate oak forest soil. New Phytol 201:269–278. https://doi.org/10.1111/nph.12481

    CAS  Article  PubMed  Google Scholar 

  94. Schlatter DC, Kahl K, Carlson B, Huggins DR, Paulitz T (2018) Fungal community composition and diversity vary with soil depth and landscape position in a no-till wheat-based cropping system. FEMS Microbiol Ecol 94:. https://doi.org/10.1093/femsec/fiy098

  95. Nagati M, Roy M, Manzi S et al (2018) Impact of local forest composition on soil fungal communities in a mixed boreal forest. Plant Soil:1–13. https://doi.org/10.1007/s11104-018-3806-3

  96. Jumpponen A, Jones KL, Blair J (2010) Vertical distribution of fungal communities in tallgrass prairie soil. Mycologia 102:1027–1041. https://doi.org/10.3852/09-316

    Article  PubMed  Google Scholar 

  97. Cheeke TE, Phillips RP, Brzostek ER, Rosling A, Bever JD, Fransson P (2016) Dominant mycorrhizal association of trees alters carbon and nutrient cycling by selecting for microbial groups with distinct enzyme function. New Phytol 214:432–442. https://doi.org/10.1111/nph.14343

    CAS  Article  PubMed  Google Scholar 

  98. Bahnmann B, Mašínová T, Halvorsen R, Davey ML, Sedlák P, Tomšovský M, Baldrian P (2018) Effects of oak, beech and spruce on the distribution and community structure of fungi in litter and soils across a temperate forest. Soil Biol Biochem 119:162–173. https://doi.org/10.1016/j.soilbio.2018.01.021

    CAS  Article  Google Scholar 

  99. Awad A, Majcherczyk A, Schall P, Schröter K, Schöning I, Schrumpf M, Ehbrecht M, Boch S, Kahl T, Bauhus J, Seidel D, Ammer C, Fischer M, Kües U, Pena R (2019) Ectomycorrhizal and saprotrophic soil fungal biomass are driven by different factors and vary among broadleaf and coniferous temperate forests. Soil Biol Biochem 131:9–18. https://doi.org/10.1016/j.soilbio.2018.12.014

    CAS  Article  Google Scholar 

  100. Dickie IA, Boyer S, Buckley HL, Duncan RP, Gardner PP, Hogg ID, Holdaway RJ, Lear G, Makiola A, Morales SE, Powell JR, Weaver L (2018) Towards robust and repeatable sampling methods in eDNA-based studies. Mol Ecol Resour 18:940–952. https://doi.org/10.1111/1755-0998.12907

    Article  Google Scholar 

  101. McGuire KL, Zak DR, Edwards IP et al (2010) Slowed decomposition is biotically mediated in an ectomycorrhizal, tropical rain forest. Oecologia 164:785–795. https://doi.org/10.1007/s00442-010-1686-1

    Article  PubMed  Google Scholar 

  102. van der Linde S, Suz LM, Orme CDL, Cox F, Andreae H, Asi E, Atkinson B, Benham S, Carroll C, Cools N, de Vos B, Dietrich HP, Eichhorn J, Gehrmann J, Grebenc T, Gweon HS, Hansen K, Jacob F, Kristöfel F, Lech P, Manninger M, Martin J, Meesenburg H, Merilä P, Nicolas M, Pavlenda P, Rautio P, Schaub M, Schröck HW, Seidling W, Šrámek V, Thimonier A, Thomsen IM, Titeux H, Vanguelova E, Verstraeten A, Vesterdal L, Waldner P, Wijk S, Zhang Y, Žlindra D, Bidartondo MI (2018) Environment and host as large-scale controls of ectomycorrhizal fungi. Nature 558:243–248. https://doi.org/10.1038/s41586-018-0189-9

    CAS  Article  PubMed  Google Scholar 

  103. Hart MM, Aleklett K, Chagnon P-L, Egan C, Ghignone S, Helgason T, Lekberg Y, Öpik M, Pickles BJ, Waller L (2015) Navigating the labyrinth: a guide to sequence-based, community ecology of arbuscular mycorrhizal fungi. New Phytol 207:235–247. https://doi.org/10.1111/nph.13340

    Article  PubMed  Google Scholar 

  104. McMurdie PJ, Holmes S (2014) Waste not, want not: why rarefying microbiome data is inadmissible. PLoS Comput Biol 10:e1003531. https://doi.org/10.1371/journal.pcbi.1003531

    CAS  Article  PubMed  PubMed Central  Google Scholar 

  105. Weiss S, Xu ZZ, Peddada S, Amir A, Bittinger K, Gonzalez A, Lozupone C, Zaneveld JR, Vázquez-Baeza Y, Birmingham A, Hyde ER, Knight R (2017) Normalization and microbial differential abundance strategies depend upon data characteristics. Microbiome 5:27. https://doi.org/10.1186/s40168-017-0237-y

    Article  PubMed  PubMed Central  Google Scholar 

  106. Gao C, Montoya L, Xu L, Madera M, Hollingsworth J, Purdom E, Hutmacher RB, Dahlberg JA, Coleman-Derr D, Lemaux PG, Taylor JW (2019) Strong succession in arbuscular mycorrhizal fungal communities. ISME J 13:214–226. https://doi.org/10.1038/s41396-018-0264-0

    Article  PubMed  Google Scholar 

  107. Krüger M, Stockinger H, Krüger C, Schüßler A (2009) DNA-based species level detection of Glomeromycota: one PCR primer set for all arbuscular mycorrhizal fungi. New Phytol 183:212–223. https://doi.org/10.1111/j.1469-8137.2009.02835.x

    CAS  Article  PubMed  Google Scholar 

  108. Öpik M, Davison J, Moora M, Zobel M (2013) DNA-based detection and identification of Glomeromycota: the virtual taxonomy of environmental sequences. Botany 92:135–147. https://doi.org/10.1139/cjb-2013-0110

    CAS  Article  Google Scholar 

  109. Kress WJ, Erickson DL (2007) A two-locus global DNA barcode for land plants: the coding rbcL gene complements the non-coding trnH-psbA spacer region. PLoS One 2:e508. https://doi.org/10.1371/journal.pone.0000508

    CAS  Article  PubMed  PubMed Central  Google Scholar 

Download references

Acknowledgments

We are grateful to two anonymous reviewers for the suggestions that improved the manuscript. We would like to thank Dayana Agudo, William Barrette, Aleksandra Bielnicka, Sarah Dupont, Paola Escobar, Caroline Fink-Mercier, Audren Jiquel, and David Poissant for the field and laboratory assistance. We also thank the staff from the Station de biologie des Laurentides (SBL) of Université de Montréal for facilitating the field work. Funding, including scholarships to AC, was provided by Discovery Grants to EL (RGPIN-2014-06106, RGPIN-2019-04537) by the Natural Sciences and Engineering Research Council of Canada (NSERC) as well as a “Nouveau Chercheur” grant (2016-NC-188823) by the Fonds de recherche du Québec sur la Nature et technologies (FRQNT). AC would like to sincerely thank the Institut de recherche en biologie végétale, Centre d’étude de la forêt, Centre de la science de la biodiversité du Québec, Université de Montréal, and the FRQNT for providing generous financial support.

Code Availability

Custom code for bioinformatical and statistical analyses are available at https://doi.org/10.5281/zenodo.3631982.

Funding

This study received financial support from the Discovery Grants (RGPIN-2014-06106, RGPIN-2019-04537) by the Natural Sciences and Engineering Research Council of Canada (NSERC) and “Nouveau Chercheur” grant (2016-NC-188823) by the Fonds de recherche du Québec sur la Nature et technologies (FRQNT).

Author information

Affiliations

  1. Institut de recherche en biologie végétale, Département de sciences biologiques, Université de Montréal, 4101 Sherbrooke Est, Montréal, H1X 2B2, Canada

    Alexis Carteron, Marie Beigas, Simon Joly & Etienne Laliberté

  2. Montreal Botanical Garden, 4101 Sherbrooke Est, Montréal, H1X 2B2, Canada

    Simon Joly

  3. Smithsonian Tropical Research Institute, Apartado 0843-03092, Balboa, Ancon, Republic of Panama

    Benjamin L. Turner

Authors
  1. Alexis Carteron
    View author publications

    You can also search for this author in PubMed Google Scholar

  2. Marie Beigas
    View author publications

    You can also search for this author in PubMed Google Scholar

  3. Simon Joly
    View author publications

    You can also search for this author in PubMed Google Scholar

  4. Benjamin L. Turner
    View author publications

    You can also search for this author in PubMed Google Scholar

  5. Etienne Laliberté
    View author publications

    You can also search for this author in PubMed Google Scholar

Contributions

EL and AC conceived the ideas and designed methodology; AC, BT, SJ, and MB collected the data; AC analyzed the data; AC and EL interpreted the results; AC led the writing of the manuscript. All authors contributed critically to the drafts and gave final approval for publication.

Corresponding author

Correspondence to Alexis Carteron.

Ethics declarations

Conflict of Interest

The authors declare that they have no conflicts of interest.

Electronic supplementary material

ESM 1

(DOCX 4517 kb)

Rights and permissions

Reprints and Permissions

About this article

Verify currency and authenticity via CrossMark

Cite this article

Carteron, A., Beigas, M., Joly, S. et al. Temperate Forests Dominated by Arbuscular or Ectomycorrhizal Fungi Are Characterized by Strong Shifts from Saprotrophic to Mycorrhizal Fungi with Increasing Soil Depth. Microb Ecol 82, 377–390 (2021). https://doi.org/10.1007/s00248-020-01540-7

Download citation

  • Received:

  • Accepted:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1007/s00248-020-01540-7

Keywords

  • Fungal guilds
  • Soil physico-chemistry
  • Podzolic soil
  • Vertical segregation
  • Acer saccharum
  • Fagus grandifolia