The ectomycorrhizal fungus Paxillus involutus converts organic matter in plant litter using a trimmed brown‐rot mechanism involving Fenton chemistry

Abstract

Summary Soils in boreal forests contain large stocks of carbon. Plants are the main source of this carbon through tissue residues and root exudates. A major part of the exudates are allocated to symbiotic ectomycorrhizal fungi. In return, the plant receives nutrients, in particular nitrogen from the mycorrhizal fungi. To capture the nitrogen, the fungi must at least partly disrupt the recalcitrant organic matter–protein complexes within which the nitrogen is embedded. This disruption process is poorly characterized. We used spectroscopic analyses and transcriptome profiling to examine the mechanism by which the ectomycorrhizal fungus Paxillus involutus degrades organic matter when acquiring nitrogen from plant litter. The fungus partially degraded polysaccharides and modified the structure of polyphenols. The observed chemical changes were consistent with a hydroxyl radical attack, involving Fenton chemistry similar to that of brown‐rot fungi. The set of enzymes expressed by Pa. involutus during the degradation of the organic matter was similar to the set of enzymes involved in the oxidative degradation of wood by brown‐rot fungi. However, Pa. involutus lacked transcripts encoding extracellular enzymes needed for metabolizing the released carbon. The saprotrophic activity has been reduced to a radical‐based biodegradation system that can efficiently disrupt the organic matter–protein complexes and thereby mobilize the entrapped nutrients. We suggest that the released carbon then becomes available for further degradation and assimilation by commensal microbes, and that these activities have been lost in ectomycorrhizal fungi as an adaptation to symbiotic growth on host photosynthate. The interdependence of ectomycorrhizal symbionts and saprophytic microbes would provide a key link in the turnover of nutrients and carbon in forest ecosystems.

Shown for reading. Its publisher allows quoting it, not republishing it.

References 59

1. 1.

   Allison SD. Soil minerals and humic acids alter enzyme stability: implications for ecosystem processes. Biogeochemistry. 2006;81:361-373.

   Not in our library

2. 2.

   Baldrian P. Ectomycorrhizal fungi and their enzymes in soils: is there enough evidence for their role as facultative soil saprotrophs? Oecologia. 2009;161:657-660.

   Not in our library10.1007/s00442-009-1433-7

3. 3.

   Baldrian P, Valaskova V. Degradation of cellulose by basidiomycetous fungi. FEMS Microbiol Rev. 2008;32:501-521.

   Not in our library10.1111/j.1574-6976.2008.00106.x

4. 4.

   Bending GD, Read DJ. The structure and function of the vegetative mycelium of ectomycorrhizal plants V. Foraging behaviour and translocation of nutrients from exploited litter. New Phytol. 1995a;130:401-409.

   Not in our library

5. 5.

   Bending GD, Read DJ. The structure and the function of the vegetative mycelium of ectomycorrhizal plants. VI. Activities of nutrient mobilizing enzymes in birch litter colonized by Paxillus involutus (Fr.) Fr. New Phytol. 1995b;130:411-417.

   Not in our library

6. 6.

   Bending GD, Read DJ. Nitrogen mobilization from protein-polyphenol complex by ericoid and ectomycorrhizal fungi. Soil Biol Biochem. 1996;28:1603-1612.

   Not in our library

7. 7.

   Biely P, Mislovicova D, Toman R. Soluble chromogenic substrates for the assay of endo-1,4-beta-xylanases and endo-1,4-beta-glucanases. Anal Biochem. 1985;144:142-146.

   Not in our library10.1016/0003-2697(85)90095-8

8. 8.

   Binder M, Hibbett DS. Molecular systematics and biological diversification of Boletales. Mycologia. 2006;98:971-981.

   Not in our library10.3852/mycologia.98.6.971

9. 9.

   Boer W, Folman LB, Summerbell RC, Boddy L. Living in a fungal world: impact of fungi on soil bacterial niche development. FEMS Microbiol Rev. 2005;29:795-811.

   Not in our library10.1016/j.femsre.2004.11.005

10. 10.

    Bolan NS, Adrianao DC, Kunhikrishnan A, James T, McDowell R, Senesi N. Dissolved organic matter: biogeochemistry, dynamics, and environemntal significance in soils. Adv Agron. 2011;100:1-75.

    Not in our library

11. 11.

    Chengrong RC, Zhihong HX. Analysis and behaviour of soluble organic nitrogen in forest soils. J Soils Sediments. 2008;8:363-378.

    Not in our library

12. 12.

    Colpaert JV, Van Laere A. A comparison of the extracellular enzyme activities of two ectomycorrhizal and a leaf-saprotrophic basidiomycete colonizing beech leaf litter. New Phytol. 1996;134:133-141.

    Not in our library

13. 13.

    Courty P-E, Pritsch K, Schloter M, Hartmann A, Garbaye J. Activity profiling of ectomycorrhiza communities in two forest soils using multiple enzymatic tests. New Phytol. 2005;167:309-319.

    Not in our library10.1111/j.1469-8137.2005.01401.x

14. 14.

    Courty P-E, Hoegger PJ, Kilaru S, Kohler A, Buée M, Garbaye J, et al. Phylogenetic analysis, genomic organization, and expression analysis of multi-copper oxidases in the ectomycorrhizal basidiomycete Laccaria bicolor. New Phytol. 2009;182:736-750.

    Not in our library10.1111/j.1469-8137.2009.02774.x

15. 15.

    Davidson EA, Galloway LF, Strand MK. Assessing available carbon: comparison of techniques across selected forest soils. Commun Soil Sci Plant Analysis. 1987;18:45-65.

    Not in our library

16. 16.

    Edgar R, Domrachev M, Lash AE. Gene Expression Omnibus: NCBI gene expression and hybridization array data repository. Nucleic Acids Res. 2002;30:207-210.

    Not in our library10.1093/nar/30.1.207

17. 17.

    Falkowski P, Scholes RJ, Boyle E, Canadell J, Canfield D, Elser J, et al. The global carbon cycle: a test of our knowledge of earth as a system. Science. 2000;290:291-296.

    Not in our library10.1126/science.290.5490.291

18. 18.

    Feling R, Steglich W, Muhlbacher J, Bringmann G. The absolute configuration of the mushroom metabolite involutin and chamonixin. Tetrahedon. 2001;57:7857-7863.

    Not in our library

19. 19.

    Ferrari GM, Mingazzini M. Synchronous fluorescence spectra of dissolved organic matter (DOM) of algal origin in marine coastal waters. Mar Ecol Prog Ser. 1995;125:305-315.

    Not in our library

20. 20.

    Goodell B, Daniel G, Jellison J, Qian Y. Iron-reducing capacity of low-molecular weight compounds produced in wood by fungi. Holzforschung. 2006;60:630-636.

    Not in our library

21. 21.

    Green F, Highley TL. Mechanism of brown-rot decay: paradigm or paradox. Int Biodeterior Biodegradation. 1997;39:113-124.

    Not in our library

22. 22.

    Grell MN, Jensen AB, Olsen PB, Eilenberg J, Lange L. Secretome of fungus-infected aphids documents high pathogen activity and weak host response. Fungal Genet Biol. 2011;48:343-352.

    Not in our library10.1016/j.fgb.2010.12.003

23. 23.

    Haselwandter K, Bobleter O, Read DJ. Degradation of 14C-labelled lignin and dehydropolymer of coniferyl alcohol by ericoid and ectomycorrhizal fungi. Arch Microbiol. 1990;153:352-354.

    Not in our library

24. 24.

    Högberg MN, Högberg P. Extramatrical ectomycorrhizal mycelium contributes one-third of microbial biomass and produces, together with associated roots, half of the dissolved organic carbon in a forest soil. New Phytol. 2002;154:791-795.

    Not in our library10.1046/j.1469-8137.2002.00417.x

25. 25.

    Högberg P, Read DJ. Towards a more plant physiological perspective on soil ecology. Trends Ecol Evol. 2006;21:548-554.

    Not in our library10.1016/j.tree.2006.06.004

26. 26.

    Izumi H, Finlay RD. Ectomycorrhizal roots select distinctive bacterial and ascomycete communities in Swedish subarctic forests. Environ Microbiol. 2011;13:819-830.

    Not in our library10.1111/j.1462-2920.2010.02393.x

27. 27.

    Kostylev M, Moran-Mirabal JM, Walker LP, Wilson DB. Determination of the molecular states of the processive endocellulase Thermobifida fusca Cel9A during crystalline celulose depolymerization. Biotechnol Bioeng. 2012;109:295-299.

    Not in our library10.1002/bit.23299

28. 28.

    Langston JA, Shaghasi T, Abbate E, Xu F, Vlasenko E, Sweeney MD. Oxidoreductive cellulose depolymerization by the enzymes cellobiose dehydrogenase and glycoside hydrolase 61. Appl Environ Microbiol. 2011;77:7007-7015.

    Not in our library10.1128/aem.05815-11

29. 29.

    Leonowicz A, Grzywnowicz K. Quantitative estimation of laccase forms in some white-rot fungi using syringaldazine as a substrate. Enzyme Microb Technol. 1981;3:55-58.

    Not in our library

30. 30.

    Lindahl BD, Ihrmark K, Boberg J, Trumbore SE, Hogberg P, Stenlid J, Finlay RD. Spatial separation of litter decomposition and mycorrhizal nitrogen uptake in a boreal forest. New Phytol. 2007;173:611-620.

    Not in our library10.1111/j.1469-8137.2006.01936.x

31. 31.

    Lynd LR, Weimer PJ, van Zyl WH, Pretorius IS. Microbial cellulose utilization: fundamentals and biotechnology. Microbiol Mol Biol Rev. 2002;66:506-577.

    Not in our library10.1128/mmbr.66.3.506-577.2002

32. 32.

    Mäkelä MR, Hilden K, Lundell TK. Oxalate decarboxylase: biotechnological update and prevalence of the enzyme in filamentous fungi. Appl Microbiol Biotechnol. 2010;87:801-814.

    Not in our library10.1007/s00253-010-2650-z

33. 33.

    Martin F, Aerts A, Ahren D, Brun A, Danchin EG, Duchaussoy F, et al. The genome of Laccaria bicolor provides insights into mycorrhizal symbiosis. Nature. 2008;452:88-92.

    Not in our library10.1038/nature06556

34. 34.

    Martinez AT, Rencoret J, Nieto L, Jimenez-Barbero J, Gutierrez A, Rio JC. Selective lignin and polysaccharide removal in natural fungal decay of wood as evidenced by in situ structural analyses. Environ Microbiol. 2011;13:96-107.

    Not in our library10.1111/j.1462-2920.2010.02312.x

35. 35.

    Martinez D, Challacombe J, Morgenstern I, Hibbett D, Schmoll M, Kubicek CP, et al. Genome, transcriptome, and secretome analysis of wood decay fungus Postia placenta supports unique mechanisms of lignocellulose conversion. Proc Natl Acad Sci USA. 2009;106:1954-1959.

    Not in our library10.1073/pnas.0809575106

36. 36.

    Nagendran S, Hallen-Adams HE, Paper JM, Aslam N, Walton JD. Reduced genomic potential for secreted plant cell-wall-degrading enzymes in the ectomycorrhizal fungus Amanita bisporigera, based on the secretome of Trichoderma reesei. Fungal Genet Biol. 2009;46:427-435.

    Not in our library10.1016/j.fgb.2009.02.001

37. 37.

    Nannipieri P, Eldor P. The chemical and functional characterization of soil N and its biotic components. Soil Biol Biochem. 2009;41:2357-2369.

    Not in our library

38. 38.

    Newcombe D, Paszczynski A, Gajewska W, Kröger M, Feis G, Crawford R. Production of small molecular weight catalysts and the mechanism of trinitrotoluene degradation by several Gloeophyllum species. Enzyme Microb Technol. 2002;30:506-517.

    Not in our library

39. 39.

    Nierop KGJ, van Bergen PF, Buurman P, van Lagen B. NaOH and Na4P2O7 extractable organic matter in two allophanic volcanic ash soils of the Azores Islands-a pyrolysis GC/MS study. Geoderma. 2005;127:36-51.

    Not in our library

40. 40.

    Norkrans B. Studies in growth and cellulolytic enzymes of Tricholoma. Symbolae Botanicae Upsaliensis. 1950;11:1-126.

    Not in our library

41. 41.

    Olsson PA, Chalot M, Bååth E, Finlay RD, Söderström B. Ectomycorrhizal mycelia reduce bacterial activity in a sandy soil. FEMS Microbiol Ecol. 1996;21:77-86.

    Not in our library

42. 42.

    Palmieri G, Giardina P, Bianco C, Scaloni A, Capasso A, Sannia G. A novel white laccase from Pleurotus ostreatus. J Biol Chem. 1997;272:31301-31307.

    Not in our library10.1074/jbc.272.50.31301

43. 43.

    Piccolo A. The supramolecular structure of humic substances. Soil Sci. 2001;166:810-832.

    Not in our library

44. 44.

    Pierpoint WS. The extraction of enzymes from plant tissues rich in phenolic compounds. Methods Mol Biol. 1996;59:69-80.

    Not in our library10.1385/0-89603-336-8:69

45. 45.

    Quinlan RJ, Sweeney MD, Lo LL, Otten H, Poulsen JC, Johansen KS, et al. Insights into the oxidative degradation of cellulose by a copper metalloenzyme that exploits biomass components. Proc Natl Acad Sci USA. 2011;108:15079-15084.

    Not in our library10.1073/pnas.1105776108

46. 46.

    Read DJ, Leake JR, Perez-Moreno J. Mycorrhizal fungi as drivers of ecosystem processes in heathland and boreal forest biomes. Can J Bot. 2004;82:1243-1263.

    Not in our library

47. 47.

    Schmidt MW, Torn MS, Abiven S, Dittmar T, Guggenberger G, Janssens IA, et al. Persistence of soil organic matter as an ecosystem property. Nature. 2011;478:49-56.

    Not in our library10.1038/nature10386

48. 48.

    van Schöll L, Hoffland E, van Bremen N. Organic anion exudation by ectomycorrhizal fungi and Pinus sylvestris in response to nutrient deficiencies. New Phytol. 1996;170:153-163.

    Not in our library10.1111/j.1469-8137.2006.01649.x

49. 49.

    Senesi N, Miano TM, Provenzano MR, Brunetti G. Characterization, differentiation, and classification of humic substances by fluorescence spectroscopy. Soil Science. 1991;152:259-271.

    Not in our library

50. 50.

    Simard SW, Jones MD, Durall DM, van der Heijden MGA, Sanders IR. Carbon and nutrient fluxes in within and between mycorrhizal plants. Mycorrhizal Ecology. 2002;33-74.

    Not in our library

51. 51.

    Suzuki MR, Hunt CG, Houtman CJ, Dalebroux ZD, Hammel KE. Fungal hydroquinones contribute to brown rot of wood. Environ Microbiol. 2006;8:2214-2223.

    Not in our library10.1111/j.1462-2920.2006.01160.x

52. 52.

    Talbot JM, Allison SD, Treseder KK. Decomposer in disguise: mycorrhizal fungi as regulators of soil C dynamics in ecosystems under global change. Funct Ecol. 2008;22:955-963.

    Not in our library

53. 53.

    Tanaka H, Yoshida G, Baba Y, Matsumura K, Wasada H, Murata J, et al. Characterization of a hydroxyl-radical-producing glycoprotein and its presumptive genes from the white-rot basidiomycete Phanerochaete chrysosporium. J Biotechnol. 2007;128:500-511.

    Not in our library10.1016/j.jbiotec.2006.12.010

54. 54.

    Tien M, Kirk TK. Lignin peroxidase of Phanerochaete chrysosporium. Methods Enzymol. 1988;161:238-249.

    Not in our library

55. 55.

    Treseder KK, Torn MS, Masiello CA. An ecosystem-scale radiocarbon tracer to test use of litter carbon by ectomycorrhizal fungi. Soil Biol Biochem. 2006;38:1077-1082.

    Not in our library

56. 56.

    Trojanowski J, Haider K, Huttermann A. Decomposition of 14C labelled lignin, holocelllulose and lignocellulose by mycorrhizal fungi. Arch Microbiol. 1984;139:202-206.

    Not in our library

57. 57.

    Vanden Wymelenberg A, Gaskell J, Mozuch M, Sabat G, Ralph J, Skyba O, et al. Comparative transcriptome and secretome analysis of wood decay fungi Postia placenta and Phanerochaete chrysosporium. Appl Environ Microbiol. 2010;76:3599-3610.

    Not in our library10.1128/aem.00058-10

58. 58.

    Wallander H, Söderström B, Cairney JWG, Chambers SM. Paxillus. Ectomycorrhizal Fungi: Key Genera in Profile. 1999;231-252.

    Not in our library

59. 59.

    Yelle DJ, Wei D, Ralph J, Hammel KE. Multidimensional NMR analysis reveals truncated lignin structures in wood decayed by the brown rot basidiomycete Postia placenta. Environ Microbiol. 2011;13:1091-1100.

    Not in our library10.1111/j.1462-2920.2010.02417.x

Cited by papers we hold 2

• Ectomycorrhizal fungi decompose soil organic matter using oxidative mechanisms adapted from saprotrophic ancestors · 2015
  No notice
• The diversity of fungal genome · 2015
  No notice

Reads

A person counts once a day per paper. We keep no cookie and no address: a reader is a hash that changes every day. Any month under five reads shows no number.