Ectomycorrhizal fungi mediate belowground carbon transfer between pines and oaks
Jazyk angličtina Země Anglie, Velká Británie Médium print-electronic
Typ dokumentu časopisecké články, práce podpořená grantem
Grantová podpora
849740
EC | EU Framework Programme for Research and Innovation H2020 | H2020 Priority Excellent Science | H2020 European Research Council (H2020 Excellent Science - European Research Council)
PubMed
35042973
PubMed Central
PMC9039061
DOI
10.1038/s41396-022-01193-z
PII: 10.1038/s41396-022-01193-z
Knihovny.cz E-zdroje
- MeSH
- dub (rod) * mikrobiologie MeSH
- kořeny rostlin mikrobiologie MeSH
- mykorhiza * genetika metabolismus MeSH
- oxid uhličitý MeSH
- půda MeSH
- stromy mikrobiologie MeSH
- uhlík metabolismus MeSH
- Publikační typ
- časopisecké články MeSH
- práce podpořená grantem MeSH
- Názvy látek
- oxid uhličitý MeSH
- půda MeSH
- uhlík MeSH
Inter-kingdom belowground carbon (C) transfer is a significant, yet hidden, biological phenomenon, due to the complexity and highly dynamic nature of soil ecology. Among key biotic agents influencing C allocation belowground are ectomycorrhizal fungi (EMF). EMF symbiosis can extend beyond the single tree-fungus partnership to form common mycorrhizal networks (CMNs). Despite the high prevalence of CMNs in forests, little is known about the identity of the EMF transferring the C and how these in turn affect the dynamics of C transfer. Here, Pinus halepensis and Quercus calliprinos saplings growing in forest soil were labeled using a 13CO2 labeling system. Repeated samplings were applied during 36 days to trace how 13C was distributed along the tree-fungus-tree pathway. To identify the fungal species active in the transfer, mycorrhizal fine root tips were used for DNA-stable isotope probing (SIP) with 13CO2 followed by sequencing of labeled DNA. Assimilated 13CO2 reached tree roots within four days and was then transferred to various EMF species. C was transferred across all four tree species combinations. While Tomentella ellisii was the primary fungal mediator between pines and oaks, Terfezia pini, Pustularia spp., and Tuber oligospermum controlled C transfer among pines. We demonstrate at a high temporal, quantitative, and taxonomic resolution, that C from EMF host trees moved into EMF and that C was transferred further to neighboring trees of similar and distinct phylogenies.
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Steidinger BS, Crowther TW, Liang J, Van Nuland ME, Werner GD, Reich PB, et al. Climatic controls of decomposition drive the global biogeography of forest-tree symbioses. Nature. 2019;569:404–8. doi: 10.1038/s41586-019-1128-0. PubMed DOI
Finlay RD. Ecological aspects of mycorrhizal symbiosis: with special emphasis on the functional diversity of interactions involving the extraradical mycelium. J Exp Bot. 2008;59:1115–26. doi: 10.1093/jxb/ern059. PubMed DOI
Smith SE, Read D. Nitrogen mobilization and nutrition in ectomycorrhizal plants. Mycorrhizal Symbiosis. 2008;321–48. 10.1016/b978-012370526-6.50011-8.
Osonubi O, Mulongoy K, Awotoye OO, Atayese MO, Okali DUU. Effects of ectomycorrhizal and vesicular-arbuscular mycorrhizal fungi on drought tolerance of four leguminous woody seedlings. Plant Soil. 1991;136:131–43. doi: 10.1007/BF02465228. DOI
Mayerhofer W, Schintlmeister A, Dietrich M, Gorka S, Wiesenbauer J, Martin V, et al. Ectomycorrhizal fungi induce systemic resistance against insects on a nonmycorrhizal plant in a CERK1-dependent manner. N Phytol. 2020;228:728–40. doi: 10.1111/nph.16715. PubMed DOI
Mayerhofer W, Schintlmeister A, Dietrich M, Gorka S, Wiesenbauer J, Martin V, et al. Mycorrhizal networks: mechanisms, ecology and modelling. Fungal Biol Rev. 2012;26:39–60. doi: 10.1016/j.fbr.2012.01.001. DOI
Molina R, Horton TR. Mycorrhiza specificity: its role in the development and function of common mycelial networks. Mycorrhizal Netw. 2015. 10.1007/978-94-017-7395-9_1.
Van der Heijden MGA, Martin FM, Selosse MA, Sanders IR. Mycorrhizal ecology and evolution: the past, the present, and the future. N Phytol. 2015;205:1406–23. doi: 10.1111/nph.13288. PubMed DOI
Brundrett MC. Coevolution of roots and mycorrhizas of land plants. N Phytol. 2002;154:275–304. doi: 10.1046/j.1469-8137.2002.00397.x. PubMed DOI
Linkies A, Graeber K, Knight C, Leubner-Metzger G. The evolution of seeds. N Phytol. 2010;186:817–31. doi: 10.1111/j.1469-8137.2010.03249.x. PubMed DOI
Nara K. Ectomycorrhizal networks and seedling establishment during early primary succession. N Phytol. 2006;169:169–78. doi: 10.1111/j.1469-8137.2005.01545.x. PubMed DOI
Horton TR, Molina R, Hood K. Douglas-fir ectomycorrhizae in 40- and 400-year-old stands: mycobiont availability to late successional western hemlock. Mycorrhiza. 2005;15:393–403. doi: 10.1007/s00572-004-0339-9. PubMed DOI
Teste FP, Simard SW, Durall DM, Guy RD, Jones MD, Schoonmaker AL. Access to mycorrhizal networks and roots of trees: importance for seedling survival and resource transfer. Ecology. 2009;90:2808–22. doi: 10.1890/08-1884.1. PubMed DOI
Teste FP, Simard SW. Mycorrhizal networks and distance from mature trees alter patterns of competition and facilitation in dry Douglas-fir forests. Oecologia. 2008;158:193–203. doi: 10.1007/s00442-008-1136-5. PubMed DOI
Egerton-Warburton LM, Querejeta JI, Allen MF. Common mycorrhizal networks provide a potential pathway for the transfer of hydraulically lifted water between plants. J Exp Bot. 2007;58:1473–83. doi: 10.1093/jxb/erm009. PubMed DOI
Wallander H, Ekblad A. The Importance of ectomycorrhizal networks for nutrient retention and carbon sequestration in forest ecosystems. Mycorrhizal Netw. 2015;69–90. 10.1007/978-94-017-7395-9_3.
Song YY, Simard SW, Carroll A, Mohn WW, Zeng RS. Defoliation of interior Douglas-fir elicits carbon transfer and stress signalling to ponderosa pine neighbors through ectomycorrhizal networks. Sci Rep. 2015;5:1–9. PubMed PMC
Selosse MA, Richard F, He X, Simard SW. Mycorrhizal networks: des liaisons dangereuses? Trends Ecol Evol. 2006;21:621–8. doi: 10.1016/j.tree.2006.07.003. PubMed DOI
Robinson D, Fitter A. The magnitude and control of carbon transfer between plants linked by a common mycorrhizal network. J Exp Bot. 1999;50:9–13. doi: 10.1093/jxb/50.330.9. DOI
Hoeksema JD. Experimentally testing effects of mycorrhizal networks on plant-plant interactions and distinguishing among mechanisms. Mycorrhizal Netw. 2015;255–77. 10.1007/978-94-017-7395-9_9.
Teste FP, Karst J, Jones MD, Simard SW, Durall DM. Methods to control ectomycorrhizal colonization: effectiveness of chemical and physical barriers. Mycorrhiza. 2006;17:51–65. doi: 10.1007/s00572-006-0083-4. PubMed DOI
Graves JD, Watkins NK, Fitter AH, Robinson D, Scrimgeour C. Intraspecific transfer of carbon between plants linked by a common mycorrhizal network. Plant Soil. 1997;192:153–9. doi: 10.1023/A:1004257812555. DOI
Wu B, Nara K, Hogetsu T. Can 14C-labeled photosynthetic products move between Pinus densiflora seedlings linked by ectomycorrhizal mycelia? N Phytol. 2001;149:137–46. doi: 10.1046/j.1469-8137.2001.00010.x. PubMed DOI
Bever JD, Dickie IA, Facelli E, Facelli JM, Klironomos J, Moora M, et al. Rooting theories of plant community ecology in microbial interactions. Trends Ecol Evol. 2010;25:468–78. doi: 10.1016/j.tree.2010.05.004. PubMed DOI PMC
Scheublin TR, Van Logtestijn RSP, Van Der Heijden MGA. Presence and identity of arbuscular mycorrhizal fungi influence competitive interactions between plant species. J Ecol. 2007;95:631–8. doi: 10.1111/j.1365-2745.2007.01244.x. DOI
Epron D, Bahn M, Derrien D, Lattanzi FA, Pumpanen J, Gessler A, et al. Pulse-labelling trees to study carbon allocation dynamics: a review of methods, current knowledge and future prospects. Tree Physiol. 2012;32:776–98. doi: 10.1093/treephys/tps057. PubMed DOI
Whiteside MD, Werner GD, Caldas VE, Padje A, Dupin SE, Elbers B, et al. Mycorrhizal fungi respond to resource inequality by moving phosphorus from rich to poor patches across networks. Curr Biol. 2019;29:2043–50.e8. doi: 10.1016/j.cub.2019.04.061. PubMed DOI PMC
Gorka S, Dietrich M, Mayerhofer W, Gabriel R, Wiesenbauer J, Martin V, et al. Rapid transfer of plant photosynthates to soil bacteria via ectomycorrhizal hyphae and its interaction with nitrogen availability. Front Microbiol. 2019;10:1–20. doi: 10.3389/fmicb.2019.00168. PubMed DOI PMC
Leake JR, Donnelly DP, Saunders EM, Boddy L, Read DJ. Rates and quantities of carbon flux to ectomycorrhizal mycelium following 14C pulse labeling of Pinus sylvestris seedlings: effects of litter patches and interaction a wood-decomposer fungus. Tree Physiol. 2001;21:71–82. doi: 10.1093/treephys/21.2-3.71. PubMed DOI
Kiers ET, Duhamel M, Beesetty Y, Mensah JA, Franken O, Verbruggen E, et al. Reciprocal rewards stabilize cooperation in the mycorrhizal symbiosis. Science. 2011;333:880–2. doi: 10.1126/science.1208473. PubMed DOI
Simard SW, Perry DA, Jones MD, Myrold DD, Durall DM, Molina R. Net transfer of carbon between ectomycorrhizal tree species in the field. Nature. 1997;388:579–82. doi: 10.1038/41557. PubMed DOI
Klein T, Siegwolf RTW, Körner C. Belowground carbon trade among tall trees in a temperate forest. Science. 2016;1500:15–8. PubMed
Rog I, Rosenstock NP, Körner C, Klein T. Share the wealth: trees with greater ectomycorrhizal species overlap share more carbon. Mol Ecol. 2020;29:2321–33. doi: 10.1111/mec.15351. PubMed DOI PMC
Pickles BJ, Wilhelm R, Asay AK, Hahn AS, Simard SW, Mohn WW. Transfer of 13C between paired Douglas-fir seedlings reveals plant kinship effects and uptake of exudates by ectomycorrhizas. N Phytol. 2017;214:400–11. doi: 10.1111/nph.14325. PubMed DOI
Lu Y, Conrad R. In situ stable isotope probing of methanogenic Archaea in the rice rhizosphere. Science. 2005;309:1088–90. doi: 10.1126/science.1113435. PubMed DOI
Haichar Z, Heulin T, Guyonnet JP, Achouak W. Science direct stable isotope probing of carbon flow in the plant holobiont. Curr Opin Biotechnol. 2016;41:9–13. doi: 10.1016/j.copbio.2016.02.023. PubMed DOI
Sietiö OM, Tuomivirta T, Santalahti M, Kiheri H, Timonen S, Sun H, et al. Ericoid plant species and Pinus sylvestris shape fungal communities in their roots and surrounding soil. N Phytol. 2018;218:738–51. doi: 10.1111/nph.15040. PubMed DOI
Sapes G, Demaree P, Lekberg Y, Sala A. Plant carbohydrate depletion impairs water relations and spreads via ectomycorrhizal networks. N Phytol. 2021;229:3172–83. doi: 10.1111/nph.17134. PubMed DOI
Sheffer E. A review of the development of Mediterranean pine-oak ecosystems after land abandonment and afforestation: are they novel ecosystems? Ann Sci. 2012;69:429–43. doi: 10.1007/s13595-011-0181-0. DOI
Ajbilou R, Marañón T, Arroyo J. Ecological and biogeographical analyses of Mediterranean forests of northern Morocco. Acta Oecologica. 2006;29:104–13. doi: 10.1016/j.actao.2005.08.006. DOI
Loudermilk E, Hiers J, Pokswinski S, O’Brien JJ, Barnett A, Mitchell RJ. The path back: Oaks (Quercus spp.) facilitate longleaf pine (Pinus palustris) seedling establishment in xeric sites. Ecosphere. 2016;7:1–14.
Hynes MM, Smith ME, Zasoski RJ, Bledsoe CS. A molecular survey of ectomycorrhizal hyphae in a California Quercus-Pinus woodland. Mycorrhiza. 2010;20:265–74. doi: 10.1007/s00572-009-0281-y. PubMed DOI
Rog I, Jakoby G, Klein T. Forest ecology and management carbon allocation dynamics in conifers and broadleaved tree species revealed by pulse labeling and mass balance. Ecol Manag. 2021;493:119258. doi: 10.1016/j.foreco.2021.119258. DOI
Jia Z, Cao W, Herna M. DNA-Based stable isotope probing. Springer. 2019;2046:17–29. PubMed
Neufeld JD, Vohra J, Dumont MG, Lueders T, Manefield M, Friedrich MW, et al. DNA stable-isotope probing. Nat Protoc. 2007;2:860–6. doi: 10.1038/nprot.2007.109. PubMed DOI
Taylor DL, Walters WA, Lennon NJ, Bochicchio J, Krohn A, Caporaso JG, et al. Accurate estimation of fungal diversity and abundance through improved lineage-specific primers optimized for Illumina amplicon sequencing. Appl Environ Microbiol. 2016;82:7217–26. doi: 10.1128/AEM.02576-16. PubMed DOI PMC
Blecher-Gonen R, Barnett-Itzhaki Z, Jaitin D, Amann-Zalcenstein D, Lara-Astiaso D, Amit I. High-throughput chromatin immunoprecipitation for genome-wide mapping of in vivo protein-DNA interactions and epigenomic states. Nat Protoc. 2013;8:539–54. doi: 10.1038/nprot.2013.023. PubMed DOI
Callahan BJ, McMurdie PJ, Rosen MJ, Han AW, Johnson AJA, Holmes SP. DADA2: high-resolution sample inference from Illumina amplicon data. Nat Methods. 2016;13:581–3. doi: 10.1038/nmeth.3869. PubMed DOI PMC
Buckley DH, Barnett SE, Youngblut ND. Data analysis for DNA stable isotope probing experiments using multiple window high-resolution SIP Chapter 9. Springer. 2019;2046:44–5. PubMed
Martin BD, Witten D, Willis AD. Modeling microbial abundances and dysbiosis with beta-binomial regression. Ann Appl Stat. 2020;14:94–115. doi: 10.1214/19-AOAS1283. PubMed DOI PMC
Kuzyakov Y, Gavrichkova O. time lag between photosynthesis and carbon dioxide efflux from soil: a review of mechanisms and controls. Glob Chang Biol. 2010;16:3386–406. doi: 10.1111/j.1365-2486.2010.02179.x. DOI
Hagedorn F, Joseph J, Peter M, Luster J, Pritsch K, Geppert U, et al. Recovery of trees from drought depends on belowground sink control. Nat Plants. 2016;2:1–5. doi: 10.1038/nplants.2016.111. PubMed DOI
Moreno-Arroyo B, Infante F, Pulido E, Gómez J. The biogeography and taxonomy of Tuber oligospermum (Tul. and C. Tul.) Trappe (Ascomycota) Cryptogam Mycol. 2000;21:147–52. doi: 10.1016/S0181-1584(00)00115-9. DOI
Buscardo E, Rodríguez-Echeverría S, Martín MP, De Angelis P, Pereira JS, Freitas H. Impact of wildfire return interval on the ectomycorrhizal resistant propagules communities of a Mediterranean open forest. Fungal Biol. 2010;114:628–36. doi: 10.1016/j.funbio.2010.05.004. PubMed DOI
Louro R, Santos-Silva C, Nobre T. What is in a name? Terfezia classification revisited. Fungal Biol. 2019;123:267–73. doi: 10.1016/j.funbio.2019.01.003. PubMed DOI
Tedersoo L, Arnold AE, Hansen K. Novel aspects in the life cycle and biotrophic interactions in Pezizomycetes (Ascomycota, Fungi) Mol Ecol. 2013;22:1488–93. doi: 10.1111/mec.12224. PubMed DOI
Tedersoo L, Smith ME. Lineages of ectomycorrhizal fungi revisited: Foraging strategies and novel lineages revealed by sequences from belowground. Fungal Biol Rev. 2013;27:83–99. doi: 10.1016/j.fbr.2013.09.001. DOI
Agerer R. Fungal relationships and structural identity of their ectomycorrhizae. Mycol Prog. 2006;5:67–107. doi: 10.1007/s11557-006-0505-x. DOI
Tedersoo L, May TW, Smith ME. Ectomycorrhizal lifestyle in fungi: global diversity, distribution, and evolution of phylogenetic lineages. Mycorrhiza. 2010;20:217–63. doi: 10.1007/s00572-009-0274-x. PubMed DOI
Miyauchi S, Kiss E, Kuo A, Drula E, Kohler A, Sánchez-García M, et al. Large-scale genome sequencing of mycorrhizal fungi provides insights into the early evolution of symbiotic traits. Nat Commun. 2020;11:1–17. doi: 10.1038/s41467-020-18795-w. PubMed DOI PMC
Bruns TD, Bidartondo MI, Taylor DL. Host specificity in ectomycorrhizal communities: what do the exceptions tell us? Integr Comp Biol. 2002;42:352–9. doi: 10.1093/icb/42.2.352. PubMed DOI
Pumpanen JS, Heinonsalo J, Rasilo T, Hurme KR, Ilvesniemi H. Carbon balance and allocation of assimilated CO2 in Scots pine, Norway spruce, and Silver birch seedlings determined with gas exchange measurements and 14C pulse labelling. Trees Struct Funct. 2009;23:611–21. doi: 10.1007/s00468-008-0306-8. DOI
Heinonsalo J, Pumpanen J, Rasilo T, Hurme KR, Ilvesniemi H. Carbon partitioning in ectomycorrhizal Scots pine seedlings. Soil Biol Biochem. 2010;42:1614–23. doi: 10.1016/j.soilbio.2010.06.003. DOI
Wallander H, Göransson H, Rosengren U. Production, standing biomass and natural abundance of 15N and 13C in ectomycorrhizal mycelia collected at different soil depths in two forest types. Oecologia. 2004;139:89–97. doi: 10.1007/s00442-003-1477-z. PubMed DOI
Wilhelm R, Szeitz A, Klassen TL, Mohn WW. Sensitive, efficient quantitation of 13C-enriched nucleic acids via ultrahigh-performance liquid chromatography-tandem mass spectrometry for applications in stable isotope probing. Appl Environ Microbiol. 2014;80:7206–11. doi: 10.1128/AEM.02223-14. PubMed DOI PMC
Schildkraut CL, Marmur J, Doty P. Determination of the base composition of deoxyribonucleic acid from its buoyant density in CsCl. J Mol Biol. 1962;4:430–43. doi: 10.1016/S0022-2836(62)80100-4. PubMed DOI
Jakoby G, Rog I, Megidish S, Klein T. Enhanced root exudation of mature broadleaf and conifer trees in a Mediterranean forest during the dry season. Tree Physiol. 2020;40:1595–605. doi: 10.1093/treephys/tpaa092. PubMed DOI
Meier IC, Pritchard SG, Brzostek ER, Mccormack ML, Phillips RP. The rhizosphere and hyphosphere differ in their impacts on carbon and nitrogen cycling in forests exposed to elevated CO2. N Phytol. 2015;205:1164–74. doi: 10.1111/nph.13122. PubMed DOI
Ranjard L, Dequiedt S, Prévost-Bouré NC, Thioulouse J, Saby NPA, Lelievre M, et al. Turnover of soil bacterial diversity driven by wide-scale environmental heterogeneity. Nat. Commun. 2013;4:1–10. doi: 10.1038/ncomms2431. PubMed DOI
Carmi I, Yakir D, Yechieli Y, Kronfield J, Stiller M. Variations in the isotopic composition of dissolved inorganic carbon in the unsaturated zone of a semi-arid region. Radiocarbon. 2015;57:397–406. doi: 10.2458/azu_rc.57.18356. DOI
Klein T, Hoch G. Tree carbon allocation dynamics determined using a carbon mass balance approach. N Phytol. 2015;205:147–59. doi: 10.1111/nph.12993. PubMed DOI
Mayerhofer W, Schintlmeister A, Dietrich M, Gorka S, Wiesenbauer J, Martin V, et al. Recently photoassimilated carbon and fungus-delivered nitrogen are spatially correlated in the ectomycorrhizal tissue of Fagus sylvatica. N Phytol. 2021;232:2457–74. doi: 10.1111/nph.17591. PubMed DOI PMC
Fraser EC, Lieffers VJ, Landhäusser SM. Carbohydrate transfer through root grafts to support shaded trees. Tree Physiol. 2006;26:1019–23. doi: 10.1093/treephys/26.8.1019. PubMed DOI
Van Der Heijden MGA, Horton TR. Socialism in soil? the importance of mycorrhizal fungal networks for facilitation in natural ecosystems. J Ecol. 2009;97:1139–50. doi: 10.1111/j.1365-2745.2009.01570.x. DOI