1932

Abstract

Inhabiting the interface between plant roots and soil, mycorrhizal fungi play a unique but underappreciated role in soil organic matter (SOM) dynamics. Their hyphae provide an efficient mechanism for distributing plant carbon throughout the soil, facilitating its deposition into soil pores and onto mineral surfaces, where it can be protected from microbial attack. Mycorrhizal exudates and dead tissues contribute to the microbial necromass pool now known to play a dominant role in SOM formation and stabilization. While mycorrhizal fungi lack the genetic capacity to act as saprotrophs, they use several strategies to access nutrients locked in SOM and thereby promote its decay, including direct enzymatic breakdown, oxidation via Fenton chemistry, and stimulation of heterotrophic microorganisms through carbon provision to the rhizosphere. An additional mechanism, competition with free-living saprotrophs, potentially suppresses SOM decomposition, leading to its accumulation. How these various nutrient acquisition strategies differentially influence SOM formation, stabilization, and loss is an area of critical research need.

Loading

Article metrics loading...

/content/journals/10.1146/annurev-ecolsys-110617-062331
2019-11-02
2024-03-28
Loading full text...

Full text loading...

/deliver/fulltext/ecolsys/50/1/annurev-ecolsys-110617-062331.html?itemId=/content/journals/10.1146/annurev-ecolsys-110617-062331&mimeType=html&fmt=ahah

Literature Cited

  1. Alberton O, Kuyper TW, Gorissen A 2005. Taking mycocentrism seriously: mycorrhizal fungal and plant responses to elevated CO2. New Phytol 167:859–68
    [Google Scholar]
  2. Allen MF, Kitajima K. 2014. Net primary production of ectomycorrhizas in a California forest. Fungal Ecol 10:81–90
    [Google Scholar]
  3. Arantes V, Goodell B. 2014. Current understanding of brown-rot fungal biodegradation mechanisms: a review. Deterioration and Protection of Sustainable Biomaterials TP Schultz, B Goodell, DD Nicholas 3–21 Washington, DC: Am. Chem. Soc.
    [Google Scholar]
  4. Averill C. 2016. Slowed decomposition in ectomycorrhizal ecosystems is independent of plant chemistry. Soil Biol. Biochem. 102:52–54
    [Google Scholar]
  5. Averill C, Hawkes CV. 2016. Ectomycorrhizal fungi slow soil carbon cycling. Ecol. Lett. 19:937–47
    [Google Scholar]
  6. Averill C, Turner BL, Finzi AC 2014. Mycorrhiza-mediated competition between plants and decomposers drives soil carbon storage. Nature 505:543–45
    [Google Scholar]
  7. Bååth E, Nilsson LO, Göransson H, Wallander H 2004. Can the extent of degradation of soil fungal mycelium during soil incubation be used to estimate ectomycorrhizal biomass in soil. Soil Biol. Biochem. 36:2105–9
    [Google Scholar]
  8. Baskaran P, Hyvönen R, Berglund SL, Clemmensen KE, Ågren GI et al. 2017. Modelling the influence of ectomycorrhizal decomposition on plant nutrition and soil carbon sequestration in boreal forest ecosystems. New Phytol 213:1452–65
    [Google Scholar]
  9. Beeck M, Troein C, Peterson C, Persson P, Tunlid A 2018. Fenton reaction facilitates organic nitrogen acquisition by an ectomycorrhizal fungus. New Phytol 218:335–43
    [Google Scholar]
  10. Bending GD, Read DJ. 1996. Nitrogen mobilization from protein-polyphenol complex by ericoid and ectomycorrhizal fungi. Soil Biol. Biochem. 28:1603–12
    [Google Scholar]
  11. Bödeker ITM, Clemmensen KE, Boer W, Martin F, Olson Å et al. 2014. Ectomycorrhizal Cortinarius species participate in enzymatic oxidation of humus in northern forest ecosystems. New Phytol 203:245–56
    [Google Scholar]
  12. Bödeker ITM, Nygren CM, Taylor AF, Olson Å, Lindahl BD 2009. Class II peroxidase–encoding genes are present in a phylogenetically wide range of ectomycorrhizal fungi. ISME J 3:1387–95
    [Google Scholar]
  13. Brzostek ER, Dragoni D, Brown ZA, Phillips RP 2015. Mycorrhizal type determines the magnitude and direction of root-induced changes in decomposition in a temperate forest. New Phytol 206:1274–82
    [Google Scholar]
  14. Bukovská P, Bonkowski M, Konvalinková T, Beskid O, Jujslová M et al. 2018. Utilization of organic nitrogen by arbuscular mycorrhizal fungi—is there a specific role for protists and ammonia oxidizers. Mycorrhiza 28:269–83
    [Google Scholar]
  15. Cairney JWG. 2012. Extramatrical mycelia of ectomycorrhizal fungi as moderators of carbon dynamics in forest soil. Soil Biol. Biochem. 47:198–208
    [Google Scholar]
  16. Cheeke TE, Phillips RP, Brzostek ER, Rosling A, Bever JD, Fransson P 2017. Dominant mycorrhizal association of trees alters carbon and nutrient cycling by selecting for microbial groups with distinct enzyme function. New Phytol 214:432–42
    [Google Scholar]
  17. Clemmensen KE, Bahr A, Ovaskainen O, Dahlberg A, Ekblad A et al. 2013. Roots and associated fungi drive long-term carbon sequestration in boreal forest. Science 339:1615–18
    [Google Scholar]
  18. Clemmensen KE, Finlay RD, Dahlberg A, Stenlid J, Wardle DA, Lindahl BD 2015. Carbon sequestration is related to mycorrhizal fungal community shifts during longterm succession in boreal forests. New Phytol 205:1525–36
    [Google Scholar]
  19. Cornelissen J, Aerts R, Cerabolini B, Werger M, van der Heijden MGA 2001. Carbon cycling traits of plant species are linked with mycorrhizal strategy. Oecologia 129:611–19
    [Google Scholar]
  20. Corrales A, Mangan SA, Turner BL, Dalling JW 2016. An ectomycorrhizal nitrogen economy facilitates monodominance in a neotropical forest. Ecol. Lett. 19:38–92
    [Google Scholar]
  21. Cotrufo MF, Wallenstein MD, Boot CM, Denef K, Paul E 2013. The microbial efficiency-matrix stabilization (MEMS) framework integrates plant litter decomposition with soil organic matter stabilization: Do labile plant inputs form stable soil organic matter. Glob. Change Biol. 19:988–95
    [Google Scholar]
  22. 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. Change Biol. 24:3317–30
    [Google Scholar]
  23. Dakora FD, Phillips DA. 2002. Root exudates as mediators of mineral acquisition in low-nutrient environments. Plant Soil 245:35–47
    [Google Scholar]
  24. Dashtban M, Schraft H, Syed TA, Qin W 2010. Fungal biodegradation and enzymatic modification of lignin. Int. J. Biochem. Mol. Biol. 1:36–50
    [Google Scholar]
  25. Deslippe JR, Hartmann M, Grayston SJ, Smard SW, Mohn WW 2016. Stable isotope probing implicates a species of Cortinarius in carbon transfer through ectomycorrhizal fungal mycelial networks in Arctic tundra. New Phytol 210:383–90
    [Google Scholar]
  26. Dickie IA, Alexander I, Lennon S, Öpik M, Selosse MA et al. 2015. Evolving insights to understanding mycorrhizas. New Phytol 205:1369–74
    [Google Scholar]
  27. Dijkstra FA, Carrillo Y, Pendall E, Morgan JA 2013. Rhizosphere priming: a nutrient perspective. Front. Microbiol. 4:1–8
    [Google Scholar]
  28. Dix NJ, Webster J. 1995. Fungal Ecology London, UK: Chapman & Hall
  29. Drigo B, Pijl AS, Duyts H, Kielak AM, Gamper HA et al. 2010. Shifting carbon flow from roots into associated microbial communities in response to elevated atmospheric CO2. PNAS 107:10938–42
    [Google Scholar]
  30. Ekblad A, Wallander H, Godbold DL, Cruz C, Johnson D et al. 2013. The production and turnover of extrametrical mycelium of ectomycorrhizal fungi in forest soils: role in carbon cycling. Plant Soil 366:1–27
    [Google Scholar]
  31. Fernandez CW, Heckman K, Kolka R, Kennedy PG 2019. Melanin mitigates the accelerated decay of mycorrhizal necromass with peatland warming. Ecol. Lett. 22:498–505
    [Google Scholar]
  32. Fernandez CW, Kennedy PG. 2016. Revisiting the ‘Gadgil effect’: Do interguild fungal interactions control carbon cycling in forest soils. New Phytol 209:1382–94
    [Google Scholar]
  33. Fernandez CW, Kennedy PG. 2018. Melanization of mycorrhizal fungal necromass structures microbial decomposer communities. J. Ecol. 106:468–79
    [Google Scholar]
  34. Fernandez CW, Koide RT. 2012. The role of chitin in the decomposition of ectomycorrhizal fungal litter. Ecology 93:24–28
    [Google Scholar]
  35. Fernandez CW, Koide RT. 2014. Initial melanin and nitrogen concentrations control the decomposition of ectomycorrhizal fungal litter. Soil Biol. Biochem. 77:150–57
    [Google Scholar]
  36. Fernandez CW, Langley JA, Chapman S, McCormack ML, Koide RT 2016. The decomposition of ectomycorrhizal fungal necromass. Soil Biol. Biochem. 93:38–49
    [Google Scholar]
  37. Fomina M, Gadd GM. 2003. Metal sorption by biomass of melanin-producing fungi grown in clay-containing medium. J. Chem. Technol. Biotechnol. 78:23–34
    [Google Scholar]
  38. Gadgil PD, Gadgil RL. 1975. Suppression of litter decomposition by mycorrhizal roots of Pinus radiata. N. Z. J. For. Sci. 5:33–41
    [Google Scholar]
  39. Gadgil RL, Gadgil PD. 1971. Mycorrhiza and litter decomposition. Nature 233:133
    [Google Scholar]
  40. Gale WJ, Cambardella CA. 2000. Carbon dynamics of surface residue- and root-derived organic matter under simulated no-till. Soil Sci. Soc. Am. J. 64:190–95
    [Google Scholar]
  41. Gill AL, Finzi AC. 2016. Belowground carbon flux links biogeochemical cycles and resource-use efficiency at the global scale. Ecol. Lett. 19:1419–28
    [Google Scholar]
  42. Godbold DL, Hoosbeek MR, Lukac M, Cotrufo MF, Janssens IA et al. 2006. Mycorrhizal hyphal turnover as a dominant process for carbon input into soil organic matter. Plant Soil 281:15–24
    [Google Scholar]
  43. Grandy AS, Neff JC. 2008. Molecular C dynamics downstream: the biochemical decomposition sequence and its impact on soil organic matter structure and function. Sci. Tot. Environ. 404:297–307
    [Google Scholar]
  44. Hagenbo A, Clemmensen KE, Finlay RD, Kyaschenko J, Lindahl BD et al. 2017. Changes in turnover rather than production regulate biomass of ectomycorrhizal fungal mycelium across a Pinus sylvestris chronosequence. New Phytol 214:424–31
    [Google Scholar]
  45. Hibbett DS, Gilbert L-B, Donoghue MJ 2000. Evolutionary instability of ectomycorrhizal symbioses in basidiomycetes. Nature 407:506–8
    [Google Scholar]
  46. Hobbie EA. 2006. Carbon allocation to ectomycorrhizal fungi correlates with belowground allocation in culture studies. Ecology 87:563–69
    [Google Scholar]
  47. Hobbie EA, Hobbie JE. 2008. Natural abundance of 15N in nitrogen-limited forests and tundra can estimate nitrogen cycling through mycorrhizal fungi: a review. Ecosystems 11:815–30
    [Google Scholar]
  48. Hobbie EA, Ouimette AP, Schuur EAG, Kierstead D, Trappe JM et al. 2013. Radiocarbon evidence for the mining of organic nitrogen from soil by mycorrhizal fungi. Biogeochemistry 114:381–89
    [Google Scholar]
  49. Hobbie JE, Hobbie EA. 2006. 15N in symbiotic fungi and plants estimates nitrogen and carbon flux rates in arctic tundra. Ecology 87:816–22
    [Google Scholar]
  50. Hobbie SE, Reich PB, Oleksyn J, Ogdahl M, Zytkowiak R et al. 2006. Effects on decomposition and forest floor dynamics in a common garden. Ecology 87:2288–97
    [Google Scholar]
  51. Hodge A, Campbell CD, Fitter AH 2001. An arbuscular mycorrhizal fungus accelerates decomposition and acquires nitrogen directly from organic material. Nature 413:297–99
    [Google Scholar]
  52. Högberg MN, Högberg P. 2002. Extramatrical ectomycorrhizal mycelium contributes one-third of microbial biomass and produces, together with associated roots, half the dissolved organic carbon in a forest soil. New Phytol 154:791–95
    [Google Scholar]
  53. Jacobs LM, Sulman BN, Brzostek ER, Feighery JJ, Phillips RP 2018. Interactions among decaying leaf litter, root litter and soil organic matter vary with mycorrhizal type. J. Ecol. 106:502–13
    [Google Scholar]
  54. Jilling A, Contosta AR, Frey SD, Schimel J, Schnecker J et al. 2018. Minerals in the rhizosphere: overlooked mediators of soil nitrogen availability to plants and microbes. Biogeochemistry 139:103–22
    [Google Scholar]
  55. Jo I, Songlin F, Oswalt CM, Domke GM, Phillips RP 2019. Shifts in dominant tree mycorrhizal associations in response to anthropogenic impacts. Sci. Adv. 5:eaav6358
    [Google Scholar]
  56. Kaiser C, Kilburn MR, Clode PL, Fuchslueger L, Koranda M et al. 2015. Exploring the transfer of recent plant photosynthates to soil microbes: mycorrhizal pathway versus direct root exudation. New Phytol 205:1537–51
    [Google Scholar]
  57. Kaiser C, Koranda M, Kitzler B, Fuchslueger L, Schnecker J et al. 2010. Belowground carbon allocation by trees drives seasonal patterns of extracellular enzyme activities by altering microbial community composition in a beech forest soil. New Phytol 187:843–58
    [Google Scholar]
  58. Kallenbach CM, Grandy AS, Frey SD 2016. Direct evidence for microbial-derived soil organic matter formation and its ecophysiological controls. Nat. Commun. 7:13630
    [Google Scholar]
  59. Kamel L, Keller-Pearson M, Roux C, Ané J 2017. Biology and evolution of arbuscular mycorrhizal symbiosis in the light of genomics. New Phytol 213:531–36
    [Google Scholar]
  60. Keiluweit M, Bougoure JJ, Nico PS, Pett-Ridge J, Weber PK, Kleber M 2015. Mineral protection of soil carbon counteracted by root exudates. Nat. Clim. Change 5:588–95
    [Google Scholar]
  61. Keller AB, Phillips RP. 2018. Leaf litter decay rates differ between mycorrhizal groups in temperate, but not tropical, forests. New Phytol 222:556–64
    [Google Scholar]
  62. Kleber M, Eusterhues K, Keiluweit M, Mikutta C, Mikutta R, Nico PS 2015. Mineral–organic associations: formation, properties, and relevance in soil environments. Adv. Agron. 130:1–140
    [Google Scholar]
  63. Kögel-Knabner I. 2002. The macromolecular organic composition of plant and microbial residues as inputs to soil organic matter. Soil Biol. Biochem. 34:139–62
    [Google Scholar]
  64. Kohler A, Kuo A, Nagy LG, Morin E, Barry KW et al. 2015. Convergent losses of decay mechanisms and rapid turnover of symbiosis genes in mycorrhizal mutualists. Nat. Genet. 47:410–15
    [Google Scholar]
  65. Koide RT, Malcolm GM. 2009. N concentration controls decomposition rates of different strains of ectomycorrhizal fungi. Fungal Ecol 2:197–202
    [Google Scholar]
  66. Koide RT, Wu T. 2003. Ectomycorrhizas and retarded decomposition in a Pinus resinosa plantation. New Phytol 158:401–7
    [Google Scholar]
  67. Konvalinková T, Püschel D, Řezáčová V, Gryndlerová H, Jansa J et al. 2017. Carbon flow from plant to arbuscular mycorrhizal fungi is reduced under phosphorus fertilization. Plant Soil 419:319–33
    [Google Scholar]
  68. Kuzyakov Y. 2002. Review: factors affecting rhizosphere priming effects. J. Plant Nutr. Soil Sci. 165:382–96
    [Google Scholar]
  69. Kuzyakov Y. 2010. Priming effects: interactions between living and dead organic matter. Soil Biol. Biochem. 42:1363–71
    [Google Scholar]
  70. 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. 20:1546–55
    [Google Scholar]
  71. Lambers H, Raven JA, Shaver GR, Smith SE 2008. Plant nutrient-acquisition strategies change with soil age. Trends Ecol. Evol. 23:95–103
    [Google Scholar]
  72. Lehmann A, Leifheit EF, Rillig MC 2017. Mycorrhizas and soil aggregation. Mycorrhizal Mediation of Soil: Fertility, Structure, and Carbon Storage NC Johnson, C Gehring, J Jansa 241–62 Amsterdam: Elsevier
    [Google Scholar]
  73. Lehmann J, Kleber M. 2015. The contentious nature of soil organic matter. Nature 528:60–68
    [Google Scholar]
  74. Leifheit EF, Verbruggen E, Rillig MC 2015. Arbuscular mycorrhizal fungi reduce decomposition of woody plant litter while increasing soil aggregation. Soil Biol. Biochem. 81:323–28
    [Google Scholar]
  75. Lekberg Y, Rosendahl S, Michelsen A, Olsson PA 2013. Seasonal carbon allocation to arbuscular mycorrhizal fungi assessed by microscopic examination, stable isotope probing and fatty acid analysis. Plant Soil 368:547–55
    [Google Scholar]
  76. Liang C, Cheng G, Wixon DL, Balser TC 2011. An absorbing Markov chain approach to understanding the microbial role in soil carbon stabilization. Biogeochemistry 106:303–9
    [Google Scholar]
  77. Lilleskov EA, Kuyper TW, Bidartondo MI, Hobbie EA 2019. Atmospheric nitrogen deposition impacts on the structure and function of forest mycorrhizal communities: a review. Environ. Pollut. 246:148–62
    [Google Scholar]
  78. Lin GH, McCormack ML, Ma C, Guo DL 2017. Similar below-ground carbon cycling dynamics but contrasting modes of nitrogen cycling between arbuscular mycorrhizal and ectomycorrhizal forests. New Phytol 213:1440–51
    [Google Scholar]
  79. Lindahl BD, Ihrmark K, Boberg J, Trumbore SE, Högberg P et al. 2007. Spatial separation of litter decomposition and mycorrhizal nitrogen uptake in a boreal forest. New Phytol 173:611–20
    [Google Scholar]
  80. Lindahl BD, Tunlid A. 2015. Ectomycorrhizal fungi—potential organic matter decomposers, yet not saprotrophs. New Phytol 205:1443–47
    [Google Scholar]
  81. Martin F, Aerts A, Ahrén D, Brun A, Danchin E et al. 2008. The genome of Laccaria bicolor provides insights into mycorrhizal symbiosis. Nature 452:88–92
    [Google Scholar]
  82. Martin F, Kohler A, Murat C, Veneault-Fourrey C, Hibbett DS 2016. Unearthing the roots of ectomycorrhizal symbiosis. Nat. Rev. Microbiol. 14:760–73
    [Google Scholar]
  83. Midgley MG, Brzostek E, Phillips RP 2015. Decay rates of leaf litters from arbuscular mycorrhizal trees are more sensitive to soil effects than litters from ectomycorrhizal trees. J. Ecol. 103:1454–63
    [Google Scholar]
  84. Moeller HV, Peay KG. 2016. Competition–function tradeoffs in ectomycorrhizal fungi. PeerJ 4:e2270
    [Google Scholar]
  85. Moore JA, Jiang J, Patterson CM, Mayes MA, Wang G, Classen AT 2015. Interactions among roots, mycorrhizas and free-living microbial communities differentially impact soil carbon processes. J. Ecol. 103:1442–53
    [Google Scholar]
  86. Nasholm T, Hogberg P, Franklin O, Metcalfe D, Keel SG et al. 2013. Are ectomycorrhizal fungi alleviating or aggravating nitrogen limitation of tree growth in boreal forests. New Phytol 198:214–21
    [Google Scholar]
  87. Nguyen C. 2003. Rhizodeposition of organic C by plants: mechanisms and controls. Agronomie 23:375–96
    [Google Scholar]
  88. Nicolás C, Martin-Bertelsen T, Floudas D, Bentzer J, Smits M et al. 2018. The soil organic matter decomposition mechanisms in ectromycorrhizal fungi are tuned for liberating soil organic nitrogen. ISME J 13:977–88
    [Google Scholar]
  89. Orwin KH, Kirschbaum MU, St John MG, Dickie IA 2011. Organic nutrient uptake by mycorrhizal fungi enhances ecosystem carbon storage: a model-based assessment. Ecol. Lett. 14:493–502
    [Google Scholar]
  90. Ouimette AP, Ollinger SV, Lepine LC, Stephens RB, Rowe RJ et al. 2019. Accounting for allocation to mycorrhizal fungi may resolve discrepancies in forest carbon budgets. Ecosystems In press
    [Google Scholar]
  91. Pausch J, Kuzyakov Y. 2017. Carbon input by roots into the soil: quantification of rhizodeposition from root to ecosystem scale. Glob. Change Biol. 24:1–12
    [Google Scholar]
  92. Paustian K, Lehmann J, Ogle S, Reay D, Robertson GP, Smith P 2016. Climate-smart soils. Nature 532:49–57
    [Google Scholar]
  93. Peay KG. 2016. The mutualistic niche: mycorrhizal symbiosis and community dynamics. Annu. Rev. Ecol. Evol. Syst. 47:143–64
    [Google Scholar]
  94. Pellitier PT, Zak DR. 2018. Ectomycorrhizal fungi and the enzymatic liberation of nitrogen from soil organic matter: why evolutionary history matters. New Phytol 217:68–73
    [Google Scholar]
  95. Phillips RP, Beier IC, Bernhardt ES, Grandy AS, Wickings K, Finzi AC 2012. Roots and fungi accelerate carbon and nitrogen cycling in forests exposed to elevated CO2. Ecol. Lett. 15:1042–49
    [Google Scholar]
  96. 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
    [Google Scholar]
  97. Read DJ. 1991. Mycorrhizas in ecosystems. Experientia 47:376–91
    [Google Scholar]
  98. Rineau F, Roth D, Shah F, Smits M, Johansson T et al. 2012. The ectomycorrhizal fungus Paxillus involutus converts organic matter in plant litter using a trimmed brown-rot mechanism involving Fenton chemistry. Environ. Microbiol. 14:1477–87
    [Google Scholar]
  99. Rineau F, Shah F, Smits MM, Persson P, Johansson T et al. 2013. Carbon availability triggers the decomposition of plant litter and assimilation of nitrogen by an ectomycorrhizal fungus. ISME J 7:2010–22
    [Google Scholar]
  100. Rosling A, Midgley MG, Cheeke TE, Urbina H, Fransson P, Phillips RP 2016. Phosphorus cycling in deciduous forest soil differs between stands dominated by ecto- and arbuscular mycorrhizal trees. New Phytol 209:1184–95
    [Google Scholar]
  101. Schlesinger WH, Andrews JA. 2000. Soil respiration and the global carbon cycle. Biogeochemistry 48:7–20
    [Google Scholar]
  102. Schmidt MW, Torn MS, Abiven S, Dittmar T, Guggenberger G et al. 2011. Persistence of soil organic matter as an ecosystem property. Nature 478:49–56
    [Google Scholar]
  103. Schneider T, Keiblinger KM, Schmid E, Sterflinger-Gleixner K, Ellersdorfer G et al. 2012. Who is who in litter decomposition? Metaproteomics reveals major microbial players and their biogeochemical functions. ISME J 6:1749–62
    [Google Scholar]
  104. Schweigert M, Herrmann S, Miltner A, Fester T, Kästner M 2015. Fate of ectomycorrhizal fungal biomass in a soil bioreactor system and its contribution to soil organic matter formation. Soil Biol. Biochem. 88:120–27
    [Google Scholar]
  105. Shah F, Nicolás C, Bentzer J, Ellstrom M, Smits M et al. 2016. Ectomycorrhizal fungi decompose soil organic matter using oxidative mechanisms adapted from saprotrophic ancestors. New Phytol 209:1705–19
    [Google Scholar]
  106. Siletti CE, Zeiner CA, Bhatnagar JM 2017. Distributions of fungal melanin across species and soil. Soil Biol. Biochem. 113:285–93
    [Google Scholar]
  107. Simpson AJ, Simpson MJ, Smith E, Kelleher BP 2007. Microbially derived inputs to soil organic matter: Are current estimates too low. Environ. Sci. Technol. 41:8070–76
    [Google Scholar]
  108. Six J, Elliott ET, Paustian K, Doran JW 1998. Aggregation and soil organic matter accumulation in cultivated and native grassland soils. Soil Sci. Soc. Am. J. 62:1367–77
    [Google Scholar]
  109. Soudzilovskaia NA, van der Heijden MGA, Cornelissen JHC, Makarov MI, Onipchenko VG et al. 2015. Quantitative assessment of the differential impacts of arbuscular and ectomycorrhiza on soil carbon cycling. New Phytol 208:280–93
    [Google Scholar]
  110. 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. ISME J 12:2187–97
    [Google Scholar]
  111. Strullu-Derrien C, Selosse MA, Kenrick P, Martin FM 2018. The origin and evolution of mycorrhizal symbioses: from paleomycology to phylogenomics. New Phytol 220:1012–30
    [Google Scholar]
  112. Sulman BN, Brostek ER, Medici C, Shevliakova E, Menge DNL, Phillips RP 2017. Feedbacks between plant N demand and rhizosphere priming depend on type of mycorrhizal association. Ecol. Lett. 20:1043–53
    [Google Scholar]
  113. Talbot JM, Allison S, Treseder K 2008. Decomposers in disguise: mycorrhizal fungi as regulators of soil C dynamics in ecosystems under global change. Funct. Ecol. 22:955–63
    [Google Scholar]
  114. Talbot JM, Martin F, Kohler A, Henrissat B, Peay KG 2015. Functional guild classification predicts the enzymatic role of fungi in litter and soil biogeochemistry. Soil Biol. Biochem. 88:441–56
    [Google Scholar]
  115. Tang N, San Clemente H, Roy S, Bécard G, Zhao B, Roux C 2016. A survey of the gene repertoire of Gigaspora rosea unravels conserved features among Glomeromycota for obligate biotrophy. Front. Microbiol. 7:233
    [Google Scholar]
  116. Taylor MK, Lankau R, Wurzburger N 2016. Mycorrhizal associations of trees have different indirect effects on organic matter decomposition. J. Ecol. 104:1575–84
    [Google Scholar]
  117. Tisserant E, Malbreil M, Kuo A, Kohler A, Symeonidi A et al. 2013. Genome of an arbuscular mycorrhizal fungus provides insight into the oldest plant symbiosis. PNAS 110:20117–22
    [Google Scholar]
  118. Toljander JF, Lindahl BD, Paul LR, Elfstrand M, Finlay RD 2007. Influence of arbuscular mycorrhizal mycelial exudates on soil bacterial growth and community structure. FEMS Microbiol. Ecol. 61:295–304
    [Google Scholar]
  119. Treseder KK, Lennon JT. 2015. Fungal traits that drive ecosystem dynamics on land. Microbiol. Mol. Biol. Rev. 79:243–62
    [Google Scholar]
  120. Treseder KK, Torn MS, Masiello CA 2006. An ecosystem-scale radiocarbon tracer to test use of litter carbon by ectomycorrhizal fungi. Soil Biol. Biochem. 38:1077–82
    [Google Scholar]
  121. Vázquez MM, César S, Azcón R, Barea JM 2000. Interactions between arbuscular mycorrhizal fungi and other microbial inoculants (Azospirillum, Pseudomonas, Trichoderma) and their effects on microbial population and enzyme activities in the rhizosphere of maize plants. Appl. Soil Ecol. 15:261–72
    [Google Scholar]
  122. Vicca S, Luyssaert S, Peñuelas J, Campioli M, Chapin FS et al. 2012. Fertile forests produce biomass more efficiently. Ecol. Lett. 15:520–26
    [Google Scholar]
  123. Wallander H, Göransson H, Rosengren U 2004. Production, standing biomass and natural abundance of 15N and 13C in ectomycorrhizal mycelia collected at different soil depths in two forest types. Oecologia 139:89–97
    [Google Scholar]
  124. Wallander H, Johansson U, Sterkenburg E, Durling MB, Lindahl B 2010. Production of ectomycoorhizal mycelium peaks during canopy closure in Norway spruce forests. New Phytol 187:1124–34
    [Google Scholar]
  125. Wallander H, Nilsson LO, Hagerberg D, Bååth E 2001. Estimation of the biomass and seasonal growth of external mycelium of ectomycorrhizal fungi in the field. New Phytol 151:753–60
    [Google Scholar]
  126. Wang T, Tian Z, Bengtson P, Tunlid A, Persson P 2017. Mineral surface-reactive metabolites secreted during fungal decomposition contribute to the formation of soil organic matter. Environ. Microbiol. 19:5117–29
    [Google Scholar]
  127. Waring BG, Adams R, Branco S, Powers JS 2016. Scale-dependent variation in nitrogen cycling and soil fungal communities along gradients of forest composition and age in regenerating tropical dry forests. New Phytol 209:845–54
    [Google Scholar]
  128. Weigt RB, Raidl S, Verma R, Agerer R 2012. Exploration type–specific standard values of extramatrical mycelium—a step towards quantifying ectomycorrhizal space occupation and biomass in natural soil. Mycol. Prog. 11:287–97
    [Google Scholar]
  129. Wolfe BE, Tulloss RE, Pringle A 2012. The irreversible loss of a decomposition pathway marks the single origin of an ectomycorrhizal symbiosis. PLOS ONE 7:e39597
    [Google Scholar]
  130. Wurzburger N, Brookshire ENJ. 2017. Experimental evidence that mycorrhizal nitrogen strategies affect soil carbon. Ecology 98:1491–97
    [Google Scholar]
  131. Yin H, Wheeler E, Phillips RP 2014. Root-induced changes in nutrient cycling in forests depend on exudation rates. Soil Biol. Biochem. 78:213–21
    [Google Scholar]
  132. Zak DR, Pellitier PT, Argiroff WA, Castillo B, James TY et al. 2019. Exploring the role of ectomycorrhizal fungi in soil carbon dynamics. New Phytol 223:33–39
    [Google Scholar]
  133. Zeglin LH, Myrold DD. 2013. Fate of decomposed fungal cell wall material in organic horizons of old-growth Douglas-fir forest soils. Soil Sci. Soc. Am. J. 77:489–500
    [Google Scholar]
  134. Zhang L, Shi N, Fan J, Wang F, George TS, Feng G 2018. Arbuscular mycorrhizal stimulate organic phosphate mobilization associated with changing bacterial community structure under field conditions. Environ. Microbiol. 20:2639–51
    [Google Scholar]
  135. Zhang L, Xu M, Liu Y, Zhang F, Hodge A, Feng G 2016. Carbon and phosphorus exchange may enable cooperation between an arbuscular mycorrhizal fungus and a phosphate-solubilizing bacterium. New Phytol 210:1022–32
    [Google Scholar]
  136. Zhang Z, Phillips RP, Zhao W, Yuan Y, Liu Q, Yin H 2019. Mycelia-derived C contributes more to nitrogen cycling than root-derived C in ectomycorrhizal alpine forests. Fungal Ecol 33:346–59
    [Google Scholar]
  137. Zhu K, McCormack ML, Lankau RA, Egan JF, Wurzburger N 2018. Association of ectomycorrhizal trees with high carbon-to-nitrogen ratio soils across temperate forests is driven by smaller nitrogen not larger carbon stocks. J. Ecol. 106:534–35
    [Google Scholar]
/content/journals/10.1146/annurev-ecolsys-110617-062331
Loading
/content/journals/10.1146/annurev-ecolsys-110617-062331
Loading

Data & Media loading...

  • Article Type: Review Article
This is a required field
Please enter a valid email address
Approval was a Success
Invalid data
An Error Occurred
Approval was partially successful, following selected items could not be processed due to error