Functional guild classification predicts the enzymatic role of fungi in litter and soil biogeochemistry

Soil Biology and Biochemistry

Volumn 88, Issue , 2015, Pages 441-456

  Talbot, Jennifer M ^a   Martin, Francis ^b   Kohler, Annegret ^b   Henrissat, Bernard ^c,d   Peay, Kabir G ^e  

^a USA   (United States)

^b UNIVERSITÉ DE LORRAINE   (France)

^c AIX MARSEILLE UNIVERSITY   (France)

^d KING ABDULAZIZ UNIVERSITY   (Saudi Arabia)

^e STANFORD UNIVERSITY   (United States)

Author keywords

Biogeochemistry; Carbon cycle; Decomposition; Ectomycorrhizal; Fungal communities; Soil

Indexed keywords

BIOGEOCHEMISTRY; CARBON; DECOMPOSITION; DIGITAL STORAGE; ECOLOGY; ECOSYSTEMS; ENZYMES; FORESTRY; GENES; PHOSPHATASES; SOILS;

CARBON CYCLES; COMMUNITY COMPOSITION; ECTOMYCORRHIZAL; ECTOMYCORRHIZAL FUNGI; FUNGAL COMMUNITY; MICROBIAL COMMUNITIES; PEROXIDASE ACTIVITIES; PHYLOGENETIC LINEAGES;

FUNGI;

BIOGEOCHEMISTRY; BIOMASS; CARBON CYCLE; COMMUNITY COMPOSITION; ECOSYSTEM FUNCTION; ECTOMYCORRHIZA; ENZYME ACTIVITY; FUNCTIONAL CHANGE; FUNGUS; LEAF LITTER; MICROBIAL COMMUNITY; SOIL CARBON;

FUNGI;

EID: 84937578545     PISSN: 00380717     EISSN: None     Source Type: Journal    
DOI: 10.1016/j.soilbio.2015.05.006     Document Type: Article

References (101)

1. Ander P., Eriksson K.-E. Selective degradation of wood components by white-rot fungi. Physiologia Plantarum 1977, 41:239-248.
2. Anderson I.C., Cairney J.W.G. Diversity and ecology of soil fungal communities: increased understanding through the application of molecular techniques. Environmental Microbiology 2004, 6:769-779.
3. Averill C., Turner B.L., Finzi A.C. Mycorrhiza-mediated competition between plants and decomposers drives soil carbon storage. Nature 2014, 505:543-545.
4. Bååth E. Estimation of fungal growth rates in soil using 14C-acetate incorporation into ergosterol. Soil Biology and Biochemistry 2001, 33:2011-2018.
5. 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.
6. Baldrian P., Kolařík M., Štursová M., Kopecký J., Valášková V., Větrovský T. Active and total microbial communities in forest soil are largely different and highly stratified during decomposition. The ISME Journal 2011, 6:248-258.
7. Bell A.A., Wheeler M.H. Biosynthesis and functions of fungal melanins. Annual Review of Phytopathology 1986, 24:411-451.
8. Bending G.D., Read D.J. The structure and function of the vegetative mycelium of ectomycorrhizal plants .5. Foraging behavior and translocation of nutrients from exploited litter. New Phytologist 1995, 130:401-409.
9. Bending G.D., Read D.J. The structure and function of the vegetative mycelium of ectomycorrhizal plants .6. Activities of nutrient mobilizing enzymes in birch litter colonized by Paxillus involutus (Fr) Fr. New Phytologist 1995, 130:411-417.
10. Binder M., Larsson K.-H., Matheny P.B., Hibbett D.S. Amylocorticiales ord. nov. and Jaapiales ord. nov.: early diverging clades of Agaricomycetidae dominated by corticoid forms. Mycologia 2010, 102:865-880.
11. Blomberg S.P., Garland T., Ives A.R. Testing for phylogenetic signal in comparative data: behavioral traits are more labile. Evolution 2003, 57:717-745.
12. Bödeker I.T.M., Clemmensen K.E., de Boer W., Martin F., Olson A., Lindahl B.D. Ectomycorrhizal Cortinarius species participate in enzymatic oxidation of humus in northern forest ecosystems. New Phytologist 2014, 203:245-256.
13. Bödeker I.T.M., Nygren C.M.R., Taylor A.F.S., Olson Å., Lindahl B.D. ClassII peroxidase-encoding genes are present in a phylogenetically wide range of ectomycorrhizal fungi. The ISME Journal 2009, 3:1387-1395.
14. Bridge P., Spooner B. Soil fungi: diversity and detection. Plant and Soil 2001, 232:147-154.
15. Burke D.J., Smemo K.A., Hewins C.R. Ectomycorrhizal fungi isolated from old-growth northern hardwood forest display variability in extracellular enzyme activity in the presence of plant litter. Soil Biology and Biochemistry 2014, 68:219-222.
16. Burke R.M., Cairney J.W.G. Carbohydrate oxidases in ericoid and ectomycorrhizal fungi: a possible source of Fenton radicals during the degradation of lignocellulose. New Phytologist 1998, 139:637-645.
17. Burke R.M., Cairney J.W.G. Laccases and other polyphenol oxidases in ecto- and ericoid mycorrhizal fungi. Mycorrhiza 2002, 12:105-116.
18. Burnham K.P., Anderson D.R. Model Selection and Multi-model Inference: a Practical Information-theoretic Approach 2002, Springer.
19. Burns R.G., DeForest J.L., Marxsen J., Sinsabaugh R.L., Stromberger M.E., Wallenstein M.D., Weintraub M.N., Zoppini A. Soil enzymes in a changing environment: current knowledge and future directions. Soil Biology and Biochemistry 2013, 58:216-234.
20. Butler M., Day A. Fungal melanins: a review. Canadian Journal of Microbiology 1998, 44:1115-1136.
21. Castro M.F.P.M.d., Bragagnolo N., Valentini S.R.d.T. The relationship between fungi growth and aflatoxin production with ergosterol content of corn grains. Brazilian Journal of Microbiology 2002, 33:22-26.
22. Conover W.J., Johnson M.E., Johnson M.M. A comparative study of tests for homogeneity of variances, with applications to the outer continental shelf bidding data. Technometrics 1981, 23:351-361.
23. Crowther T.W., Jones T.H., Boddy L., Baldrian P. Invertebrate grazing determines enzyme production by basidiomycete fungi. Soil Biology and Biochemistry 2011, 43:2060-2068.
24. Crowther T.W., Maynard D.S., Crowther T.R., Peccia J., Smith J.R., Bradford M.A. Untangling the fungal niche: the trait-based approach. Frontiers in Microbiology 2014, 5.
25. Deckmyn G., Meyer A., Smits M.M., Ekblad A., Grebenc T., Komarov A., Kraigher H. Simulating ectomycorrhizal fungi and their role in carbon and nitrogen cycling in forest ecosystems. Canadian Journal of Forest Research 2014, 44:535-553.
26. Fernandez C.W., Koide R.T. The function of melanin in the ectomycorrhizal fungus Cenococcum geophilum under water stress. Fungal Ecology 2013, 6:479-486.
27. Floudas D., Binder M., Riley R., Barry K., Blanchette R.A., Henrissat B., Martinez A.T., Otillar R., Spatafora J.W., Yadav J.S., Aerts A., Benoit I., Boyd A., Carlson A., Copeland A., Coutinho P.M., de Vries R.P., Ferreira P., Findley K., Foster B., Gaskell J., Glotzer D., Gorecki P., Heitman J., Hesse C., Hori C., Igarashi K., Jurgens J.A., Kallen N., Kersten P., Kohler A., Kues U., Kumar T.K.A., Kuo A., LaButti K., Larrondo L.F., Lindquist E., Ling A., Lombard V., Lucas S., Lundell T., Martin R., McLaughlin D.J., Morgenstern I., Morin E., Murat C., Nagy L.G., Nolan M., Ohm R.A., Patyshakuliyeva A., Rokas A., Ruiz-Duenas F.J., Sabat G., Salamov A., Samejima M., Schmutz J., Slot J.C., John F.S., Stenlid J., Sun H., Sun S., Syed K., Tsang A., Wiebenga A., Young D., Pisabarro A., Eastwood D.C., Martin F., Cullen D., Grigoriev I.V., Hibbett D.S. The Paleozoic origin of enzymatic lignin decomposition reconstructed from 31 fungal genomes. Science 2012, 336:1715-1719.
28. Fukami T. Community assembly dynamics in space. Community Ecology: Processes, Models, and Applications 2010, 45-54.
29. Fukami T., Dickie I.A., Paula Wilkie J., Paulus B.C., Park D., Roberts A., Buchanan P.K., Allen R.B. Assembly history dictates ecosystem functioning: evidence from wood decomposer communities. Ecology Letters 2010, 13:675-684.
30. Garamszegi L.Z. Modern Phylogenetic Comparative Methods and Their Application in Evolutionary Biology 2014, Springer.
31. Garcia-Sandoval R., Wang Z., Binder M., Hibbett D.S. Molecular phylogenetics of the gloeophyllales and relative ages of clades of Agaricomycotina producing a brown rot. Mycologia 2011, 103:510-524.
32. German D.P., Weintraub M.N., Grandy A.S., Lauber C.L., Rinkes Z.L., Allison S.D. Optimization of hydrolytic and oxidative enzyme methods for ecosystem studies. Soil Biology and Biochemistry 2011, 43:1387-1397.
33. Grafen A. The phylogenetic regression. Philosophical Transactions of the Royal Society of London. Series B, Biological Sciences 1989, 119-157.
34. Graham E.B., Wieder W.R., Leff J.W., Weintraub S.R., Townsend A.R., Cleveland C.C., Philippot L., Nemergut D.R. Do we need to understand microbial communities to predict ecosystem function? A comparison of statistical models of nitrogen cycling processes. Soil Biology and Biochemistry 2014, 68:279-282.
35. Gramss G., Kirsche B., Voigt K.-D., Günther T., Fritsche W. Conversion rates of five polycyclic aromatic hydrocarbons in liquid cultures of fifty-eight fungi and the concomitant production of oxidative enzymes. Mycological Research 1999, 103:1009-1018.
36. Heinonsalo J., Kabiersch G., Niemi R., Simpanen S., Ilvesniemi H., Hofrichter M., Hatakka A., Steffen K. Filter centrifugation as a sampling method for miniaturization of extracellular fungal enzyme activity measurements in solid media. Fungal Ecology 2012, 5:261-269.
37. Hibbett D.S., Donoghue M.J. Integrating phylogenetic analysis and classification in fungi. Mycologia 1998, 90:347-356.
38. Hibbett D.S., Donoghue M.J. Analysis of character correlations among wood decay mechanisms, mating systems, and substrate ranges in homobasidiomycetes. Systematic Biology 2001, 50:215-242.
39. Hiscox J., Baldrian P., Rogers H.J., Boddy L. Changes in oxidative enzyme activity during interspecific mycelial interactions involving the white-rot fungus Trametes versicolor. Fungal Genetics and Biology 2010, 47:562-571.
40. Hobbie S.E. Contrasting effects of substrate and fertilizer nitrogen on the early stages of litter decomposition. Ecosystems 2005, 8:644-656.
41. Hofmockel K.S., Zak D.R., Blackwood C.B. Does atmospheric NO 3- deposition alter the abundance and activity of ligninolytic fungi in forest soils?. Ecosystems 2007, 10:1278-1286.
42. Holm S. A simple sequentially rejective multiple test procedure. Scandinavian Journal of Statistics 1979, 65-70.
43. Huckfeldt T., Schmidt O. Identification key for European strand-forming house-rot fungi. Mycologist 2006, 20:42-56.
44. Huelsenbeck J.P., Crandall K.A. Phylogeny estimation and hypothesis testing using maximum likelihood. Annual Review of Ecology and Systematics 1997, 28:437-466.
45. James T.Y., Kauff F., Schoch C.L., Matheny P.B., Hofstetter V., Cox C.J., Celio G., Gueidan C., Fraker E., Miadlikowska J. Reconstructing the early evolution of Fungi using a six-gene phylogeny. Nature 2006, 443:818-822.
46. Kembel S.W., Cowan P.D., Helmus M.R., Cornwell W.K., Morlon H., Ackerly D.D., Blomberg S.P., Webb C.O. Picante: R tools for integrating phylogenies and ecology. Bioinformatics 2010, 26:1463-1464.
47. Kennedy P.G., Bruns T.D. Priority effects determine the outcome of ectomycorrhizal competition between two Rhizopogon species colonizing Pinus muricata seedlings. New Phytologist 2005, 166:631-638.
48. Kirby A.J., Hollfelder F. From Enzyme Models to Model Enzymes 2009, Royal Society of Chemistry.
49. Kirk T.K., Farrell R.L. Enzymatic Combustion - the microbial-degradation of lignin. Annual Review of Microbiology 1987, 41:465-505.
50. Kohler A., Kuo A., Nagy L.G., Morin E., Barry K.W., Buscot F., Canback B., Choi C., Cichocki N., Clum A., Colpaert J., Copeland A., Costa M.D., Dore J., Floudas D., Gay G., Girlanda M., Henrissat B., Herrmann S., Hess J., Hogberg N., Johansson T., Khouja H.-R., LaButti K., Lahrmann U., Levasseur A., Lindquist E.A., Lipzen A., Marmeisse R., Martino E., Murat C., Ngan C.Y., Nehls U., Plett J.M., Pringle A., Ohm R.A., Perotto S., Peter M., Riley R., Rineau F., Ruytinx J., Salamov A., Shah F., Sun H., Tarkka M., Tritt A., Veneault-Fourrey C., Zuccaro A., Mycorrhizal Genomics Initiative C., Tunlid A., Grigoriev I.V., Hibbett D.S., Martin F. Convergent losses of decay mechanisms and rapid turnover of symbiosis genes in mycorrhizal mutualists. Nature Genetics 2015, 47:410-415.
51. Larsson E., Larsson K.-H. Phylogenetic relationships of russuloid basidiomycetes with emphasis on aphyllophoralean taxa. Mycologia 2003, 95:1037-1065.
52. LeBauer D.S. Litter degradation rate and β-glucosidase activity increase with fungal diversity. Canadian Journal of Forest Research 2010, 40:1076-1085.
53. Levasseur A., Drula E., Lombard V., Coutinho P.M., Henrissat B. Expansion of the enzymatic repertoire of the CAZy database to integrate auxiliary redox enzymes. Biotechnol Biofuels 2013, 6:41.
54. Lindahl B.D., Tunlid A. Ectomycorrhizal fungi - potential organic matter decomposers, yet not saprotrophs. New Phytologist 2015, 205:1443-1447.
55. Lindner D.L., Banik M.T. Molecular phylogeny of Laetiporus and other brown rot polypore genera in North America. Mycologia 2008, 100:417-430.
56. Little E.L., Viereck L.A. Atlas of United States Trees 1971, US Dept. of Agriculture, Forest Service.
57. Lombard N., Prestat E., van Elsas J.D., Simonet P. Soil-specific limitations for access and analysis of soil microbial communities by metagenomics. FEMS Microbiology Ecology 2011, 78:31-49.
58. Lombard V., Ramulu H.G., Drula E., Coutinho P.M., Henrissat B. The carbohydrate-active enzymes database (CAZy) in 2013. Nucleic Acids Research 2014, 42:D490-D495.
59. Martin F., Aerts A., Ahren D., Brun A., Danchin E.G.J., Duchaussoy F., Gibon J., Kohler A., Lindquist E., Pereda V., Salamov A., Shapiro H.J., Wuyts J., Blaudez D., Buee M., Brokstein P., Canback B., Cohen D., Courty P.E., Coutinho P.M., Delaruelle C., Detter J.C., Deveau A., DiFazio S., Duplessis S., Fraissinet-Tachet L., Lucic E., Frey-Klett P., Fourrey C., Feussner I., Gay G., Grimwood J., Hoegger P.J., Jain P., Kilaru S., Labbe J., Lin Y.C., Legue V., Le Tacon F., Marmeisse R., Melayah D., Montanini B., Muratet M., Nehls U., Niculita-Hirzel H., Secq M.P.O.-L., Peter M., Quesneville H., Rajashekar B., Reich M., Rouhier N., Schmutz J., Yin T., Chalot M., Henrissat B., Kues U., Lucas S., Van de Peer Y., Podila G.K., Polle A., Pukkila P.J., Richardson P.M., Rouze P., Sanders I.R., Stajich J.E., Tunlid A., Tuskan G., Grigoriev I.V. The genome of Laccaria bicolor provides insights into mycorrhizal symbiosis. Nature 2008, 452:88-92.
60. Martins E.P., Hansen T.F. Phylogenies and the comparative method: a general approach to incorporating phylogenetic information into the analysis of interspecific data. American Naturalist 1997, 646-667.
61. McGuire K.L., Bent E., Borneman J., Majumder A., Allison S.D., Treseder K.K. Functional diversity in resource use by fungi. Ecology 2010, 91:2324-2332.
62. Monod M., Capoccia S., Léchenne B., Zaugg C., Holdom M., Jousson O. Secreted proteases from pathogenic fungi. International Journal of Medical Microbiology 2002, 292:405-419.
63. Montgomery H.J., Monreal C.M., Young J.C., Seifert K.A. Determination of soil fungal biomass from soil ergosterol analyses. Soil Biology & Biochemistry 2000, 32:1207-1217.
64. Orwin K.H., Kirschbaum M.U., St John M.G., Dickie I.A. Organic nutrient uptake by mycorrhizal fungi enhances ecosystem carbon storage: a model-based assessment. Ecology Letters 2011, 14:493-502.
65. Osono T., Takeda H. Fungal decomposition of Abies needle and Betula leaf litter. Mycologia 2006, 98:172-179.
66. Paradis E. Analysis of Phylogenetics and Evolution with R 2011, Springer.
67. Peay K.G., Baraloto C., Fine P.V. Strong coupling of plant and fungal community structure across western Amazonian rainforests. The ISME Journal 2013, 7:1852-1861.
68. Peay K.G., Belisle M., Fukami T. Phylogenetic relatedness predicts priority effects in nectar yeast communities. Proceedings of the Royal Society B: Biological Sciences 2012, 279:749-758.
69. Phillips R.P., Finzi A.C., Bernhardt E.S. Enhanced root exudation induces microbial feedbacks to N cycling in a pine forest under long-term CO2 fumigation. Ecology Letters 2011, 14:187-194.
70. Pinheiro J., Bates D., DebRoy S., Sarkar D. Linear and nonlinear mixed effects models. R Package Version 2007, 3:57.
71. Pritsch K., Garbaye J. Enzyme secretion by ECM fungi and exploitation of mineral nutrients from soil organic matter. Annals of Forest Science 2011, 68:25-32.
72. Quast C., Pruesse E., Yilmaz P., Gerken J., Schweer T., Yarza P., Peplies J., Glöckner F.O. The SILVA ribosomal RNA gene database project: improved data processing and web-based tools. Nucleic Acids Research 2013, 41:D590-D596.
73. Rao M.B., Tanksale A.M., Ghatge M.S., Deshpande V.V. Molecular and biotechnological aspects of microbial proteases. Microbiology and Molecular Biology Reviews 1998, 62:597-635.
74. Revell L.J., Harmon L.J., Collar D.C. Phylogenetic signal, evolutionary Process, and rate. Systematic Biology 2008, 57:591-601.
75. Riley R., Salamov A.A., Brown D.W., Nagy L.G., Floudas D., Held B.W., Levasseur A., Lombard V., Morin E., Otillar R. Extensive sampling of basidiomycete genomes demonstrates inadequacy of the white-rot/brown-rot paradigm for wood decay fungi. Proceedings of the National Academy of Sciences 2014, 111:9923-9928.
76. Rineau F., Roth D., Shah F., Smits M., Johansson T., Canbäck B., Olsen P.B., Persson P., Grell M.N., Lindquist E., Grigoriev I.V., Lange L., Tunlid A. The ectomycorrhizal fungus Paxillus involutus converts organic matter in plant litter using a trimmed brown-rot mechanism involving Fenton chemistry. Environmental Microbiology 2012, 14:1477-1487.
77. Rineau F., Shah F., Smits M., Persson P., Johansson T., Carleer R., Troein C., Tunlid A. Carbon availability triggers the decomposition of plant litter and assimilation of nitrogen by an ectomycorrhizal fungus. The ISME Journal 2013, 7:2010-2022.
78. Schmidt O. Wood and Tree Fungi 2006, Springer.
79. Schomburg I., Chang A., Placzek S., Söhngen C., Rother M., Lang M., Munaretto C., Ulas S., Stelzer M., Grote A. BRENDA in 2013: integrated reactions, kinetic data, enzyme function data, improved disease classification: new options and contents in BRENDA. Nucleic Acids Research 2013, 41:D764-D772.
80. Scott B., Eaton C.J. Role of reactive oxygen species in fungal cellular differentiations. Current Opinion in Microbiology 2008, 11:488-493.
81. Setala H., McLean M.A. Decomposition rate of organic substrates in relation to the species diversity of soil saprophytic fungi. Oecologia 2004, 139:98-107.
82. Sinsabaugh R.L. Fungal enzymes at the community scale. Mycology Series 2005, 23:349.
83. Sinsabaugh R.L. Phenol oxidase, peroxidase and organic matter dynamics of soil. Soil Biology and Biochemistry 2010, 42:391-404.
84. Sinsabaugh R.L., Lauber C.L., Weintraub M.N., Ahmed B., Allison S.D., Crenshaw C., Contosta A.R., Cusack D., Frey S., Gallo M.E. Stoichiometry of soil enzyme activity at global scale. Ecology Letters 2008, 11:1252-1264.
85. Srivastava D.S., Cardinale B.J., Downing A.L., Duffy J.E., Jouseau C., Sankaran M., Wright J.P. Diversity has stronger top-down than bottom-up effects on decomposition. Ecology 2009, 90:1073-1083.
86. Sun Y., Cheng J. Hydrolysis of lignocellulosic materials for ethanol production: a review. Bioresource Technology 2002, 83:1-11.
87. Swenson N.G., Enquist B.J., Thompson J., Zimmerman J.K. The influence of spatial and size scale on phylogenetic relatedness in tropical forest communities. Ecology 2007, 88:1770-1780.
88. Talbot J., Treseder K. Controls over mycorrhizal uptake of organic nitrogen. Pedobiologia 2010, 53:169-179.
89. Talbot J.M., Bruns T.D., Smith D.P., Branco S., Glassman S.I., Erlandson S., Vilgalys R., Peay K.G. Independent roles of ectomycorrhizal and saprotrophic communities in soil organic matter decomposition. Soil Biology and Biochemistry 2013, 57:282-291.
90. Talbot J.M., Bruns T.D., Taylor J.W., Smith D.P., Branco S., Glassman S.I., Erlandson S., Vilgalys R., Liao H.-L., Smith M.E. Endemism and functional convergence across the North American soil mycobiome. Proceedings of the National Academy of Sciences 2014, 111:6341-6346.
91. Taylor D.L., Herriott I.C., Stone K.E., McFarland J.W., Booth M.G., Leigh M.B. Structure and resilience of fungal communities in Alaskan boreal forest soils. Canadian Journal of Forest Research 2010, 40:1288-1301.
92. Tedersoo L., Bahram M., Põlme S., Kõljalg U., Yorou N.S., Wijesundera R., Ruiz L.V., Vasco-Palacios A.M., Thu P.Q., Suija A. Global diversity and geography of soil fungi. Science 2014, 346:1256688.
93. Tedersoo L., May T.W., Smith M.E. Ectomycorrhizal lifestyle in fungi: global diversity, distribution, and evolution of phylogenetic lineages. Mycorrhiza 2010, 20:217-263.
94. Treseder K.K., Kivlin S.N., Hawkes C.V. Evolutionary trade-offs among decomposers determine responses to nitrogen enrichment. Ecology Letters 2011, 14:933-938.
95. Tunlid A., Rineau F., Smits M., Shah F., Nicolas C., Johansson T., Persson P., Martin F. Genomics and Spectroscopy Provide Novel Insights into the Mechanisms of Litter Decomposition and Nitrogen Assimilation by Ectomycorrhizal Fungi, Genomics of Soil-and Plant-associated Fungi 2013, 191-211. Springer.
96. van der Wal A., Geydan T.D., Kuyper T.W., de Boer W. A thready affair: linking fungal diversity and community dynamics to terrestrial decomposition processes. FEMS Microbiology Reviews 2013, 37:477-494.
97. White T.J., Bruns T.D., Lee S., Taylor J.W. Amplification and direct sequencing of fungal ribosomal RNA genes for phylogenetics. PCR Protocols: a Guide to Methods and Applications 1990, 315-322. Academic Press, New York. M.A. Innis, D.H. Gelfand, J.J. Sninsky, T.J. White (Eds.).
98. Wieder W.R., Bonan G.B., Allison S.D. Global soil carbon projections are improved by modelling microbial processes. Nature Climate Change 2013, 3:909-912.
99. Worrall J.J., Anagnost S.E., Zabel R.A. Comparison of wood decay among diverse lignicolous fungi. Mycologia 1997, 89:199-219.
100. Zanne A.E., Chapman C.A., Kitajima K. Evolutionary and ecological correlates of early seedling morphology in East African trees and shrubs. American Journal of Botany 2005, 92:972-978.
101. Zwickl D. Genetic Algorithm Approaches for the Phylogenetic Analysis of Large Biological Sequence Datasets under the Maximum Likelihood Criterion 2006, (Ph. D. dissertation), University of Texas, Austin, TX.