Ectomycorrhizal fungal communities and enzymatic activities vary across an ecotone between a forest and field

Journal of Fungi

Volumn 1, Issue 2, 2015, Pages 185-210

  Rúa, Megan A ^a   Moore, Becky ^a   Hergott, Nicole ^a,b   Van, Lily ^a   Jackson, Colin R ^a   Hoeksema, Jason D ^a  

^a UNIVERSITY OF MISSISSIPPI   (United States)

^b UNIVERSITY OF TENNESSEE   (United States)

Author keywords

Carbon; Nitrogen; Peroxidase; Phenol oxidase; Phosphatase; Pinus taeda; Soil texture; glucosidase

Indexed keywords

EID: 84964351220     PISSN: None     EISSN: 2309608X     Source Type: Journal    
DOI: 10.3390/jof1020185     Document Type: Article

References (67)

1. Beckage, B.; Osborne, B.; Gavin, D.G.; Pucko, C.; Siccama, T.; Perkins, T. A rapid upward shift of a forest ecotone during 40 years of warming in the green mountains of vermont. Proc. Natl. Acad. Sci. USA 2008, 105, 4197–4202.
2. Fisichelli, N.A.; Frelich, L.E.; Reich, P.B. Temperate tree expansion into adjacent boreal forest patches facilitated by warmer temperatures. Ecography 2014, 37, 152–161.
3. Holland, M.M.; Risser, P.G.; Naiman, R.J. Ecotones: The Role of Landscape Boundaries in the Management and Restoration of Changing Environments; Chapman & Hall: New York, NY, USA, 1991.
4. Gosz, J.R. Gradient analysis of ecological change in time and space: Implications for forest management. Ecol. Appl. 1992, 2, 248–261.
5. Treseder, K.; Cross, A. Global distributions of arbuscular mycorrhizal fungi. Ecosystems 2006, 9, 305–316.
6. Twieg, B.D.; Durall, D.M.; Simard, S.W. Ectomycorrhizal fungal succession in mixed temperate forests. New Phytol. 2007, 176, 437–447.
7. Smith, S.E.; Read, D. Mycorrhizal Symbiosis, 3rd ed.; Elsevier: London, UK, 2008.
8. Ryberg, M.; Matheny, P.B. Asynchronous origins of ectomycorrhizal clades of agaricales. Proc. Biol. Sci. 2012, 279, 2003–2011.
9. Taylor, D.L.; Bruns, T.D. Community structure of ectomycorrhizal fungi in a Pinus muricata forest: Minimal overlap between the mature forest and resistant propagule communities. Mol. Ecol. 1999, 8, 1837–1850.
10. Leake, J.R.; Read, D.J. Chitin as a nitrogen source for mycorrhizal fungi. Mycol. Res. 1990, 94, 993–995.
11. Hodge, A.; Alexander, I.J.; Gooday, G.W.; Killham, K. Carbon allocation patterns in fungi in the presence of chitin in the external medium. Mycol. Res. 1996, 100, 1428–1430.
12. Tibbett, M.; Sanders, F.E.; Cairney, J.W.G.; Leake, J.R. Temperature regulation of extracellular proteases in ectomycorrhizal fungi (Hebeloma spp.) grown in axenic culture. Mycol. Res. 1999, 103, 707–714.
13. Leake, J.R.; Donnelly, D.P.; Boddy, L. Interaction between ectomycorrhizal and saprotrophic fungi. In Ecological Studies: Mycorrhizal Ecology; van der Heijden, M.G.A., Sanders, I., Eds.; Springer: Berlin, Germany, 2003; Volume 157, pp. 345–372.
14. Gramss, G.; Günther, T.; Fritsche, W. Spot tests for oxidative enzymes in ectomycorrhizal, wood-, and litter decaying fungi. Mycol. Res. 1998, 102, 67–72.
15. 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.
16. Courty, P.E.; Breda, N.; Garbaye, J. Relation between oak tree phenology and the secretion of organic matter degrading enzymes by Lactarius quietus ectomycorrhizas before and during bud break. Soil Biol. Biochem. 2007, 39, 1655–1663.
17. Courty, P.-E.; Pouysegur, R.; Buée, M.; Garbaye, J. Laccase and phosphatase activities of the dominant ectomycorrhizal types in a lowland oak forest. Soil Biol. Biochem. 2006, 38, 1219–1222.
18. Buée, M.; Courty, P.E.; Mignot, D.; Garbaye, J. Soil niche effect on species diversity and catabolic activities in an ectomycorrhizal fungal community. Soil Biol. Biochem. 2007, 39, 1947–1955.
19. 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.
20. Bruns, T. Thoughts on the processes that maintain local species diversity of ectomycorrhizal fungi. Plant Soil 1995, 170, 63–73.
21. Dickie, I.A.; Xu, B.; Koide, R.T. Vertical niche differentiation of ectomycorrhizal hyphae in soil as shown by T-RFLP analysis. New Phytol. 2002, 156, 527–535.
22. Tedersoo, L.; Kõljalg, U.; Hallenberg, N.; Larsson, K.-H. Fine scale distribution of ectomycorrhizal fungi and roots across substrate layers including coarse woody debris in a mixed forest. New Phytol. 2003, 159, 153–165.
23. Pritsch, K.; Garbaye, J. Enzyme secretion by ecm fungi and exploitation of mineral nutrients from soil organic matter. Ann. For. Sci. 2011, 68, 25–32.
24. Chalot, M.; Brun, A. Physiology of organic nitrogen acquisition by ectomycorrhizal fungi and ectomycorrhizas. FEMS Microbiol. Rev. 1998, 22, 21–44.
25. Lilleskov, E.A.; Hobbie, E.A.; Fahey, T.J. Ectomycorrhizal fungal taxa differing in response to nitrogen deposition also differ in pure culture organic nitrogen use and natural abundance of nitrogen isotopes. New Phytol. 2002, 154, 219–231.
26. Echt, C.; Saha, S.; Krutovsky, K.; Wimalanathan, K.; Erpelding, J.; Liang, C.; Nelson, C. An annotated genetic map of loblolly pine based on microsatellite and cDNA markers. BMC Genet. 2011, 12, 1–16.
27. Frederick, W.J.; Lien, S.J.; Courchene, C.E.; DeMartini, N.A.; Ragauskas, A.J.; Iisa, K. Co-production of ethanol and cellulose fiber from southern pine: A technical and economic assessment. Biomass Bioenergy 2008, 32, 1293–1302.
28. Ashkannejhad, S.; Horton, T.R. Ectomycorrhizal ecology under primary succession on coastal sand dunes: Interactions involving Pinus contorta, suilloid fungi and deer. New Phytol. 2006, 169, 345–354.
29. Ludley, K.E.; Robinson, C.H. “Decomposer” Basidiomycota in Arctic and Antarctic ecosystems. Soil Biol. Biochem. 2008, 40, 11–29.
30. Sinsabaugh, R.L. Phenol oxidase, peroxidase and organic matter dynamics of soil. Soil Biol. Biochem. 2010, 42, 391–404.
31. 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.; et al. Stoichiometry of soil enzyme activity at global scale. Ecol. Lett. 2008, 11, 1252–1264.
32. Jackson, C.R.; Tyler, H.L.; Millar, J.J. Determination of microbial extracellular enzyme activity in waters, soils, and sediments using high throughput microplate assays. J. Vis. Exp. 2013, 80, e50399.
33. Quiquampoix, H.; Servagent-Noinville, S.; Baron, M. Enzyme adsorption on soil mineral surfaces and consequences for the catalytic activity. In Enzymes in the Environment; Burns, R.G., Dick, R.P., Eds.; Marcel Dekker: New York, NY, USA, 2002.
34. Jackson, C.R.; Vallaire, S.C. Microbial activity and decomposition of fine particulate organic matter in a Louisiana cypress swamp. J. North Am. Benthol. Soc. 2007, 26, 743–753.
35. Martin, K.J.; Rygiewicz, P.T. Fungal specific primers developed for analysis of the ITS region of environmental DNA extracts. BMC Microbiol. 2005, 5, 28.
36. Gardes, M.; Bruns, T.D. Its primers with enhanced specificity for basidiomycetes—Application to the identification of mycorrhizae and rusts. Mol. Ecol. 1993, 2, 113–118.
37. Huang, X.; Madan, A. CAP3: A DNA sequence assembly program. Genome Res. 1999, 9, 868–877.
38. Taylor, D.L.; Herriott, I.C.; Long, J.; O’Neill, K. TOPO Ta is A-OK: A test of phylogenetic bias in fungal environmental clone library construction. Environ. Microbiol. 2007, 9, 1329–1334.
39. O’brien, H.E.; Parrent, J.L.; Jackson, J.A.; Moncalvo, J.M.; Vilgalys, R. Fungal community analysis by large-scale sequencing of environmental samples. Appl. Environ. Microbiol. 2005, 71, 5544–5550.
40. Izzo, A.; Agbowo, J.; Bruns, T.D. Detection of plot-level changes in ectomycorrhizal communities across years in an old-growth mixed-conifer forest. New Phytol. 2005, 166, 619–630.
41. Smith, M.D.; Douhan, G.; Rizzo, D. Ectomycorrhizal community structure in a xeric Quercus woodland based on rDNA sequence analyzsis of sporocarps and pooled roots. New Phytol. 2007, 174, 847–863.
42. Horton, T.R. Molecular approaches to ectomycorrhizal diversity studies: Variation in ITS at a local scale. Plant Soil 2002, 244, 29–39.
43. McCune, B.; Grace, J.B. Analysis of Ecological Communities; MjM Software Design: Gleneden Beach, OR, USA, 2002; Volume 28.
44. R Core Team. R: A language and environment for statistical computing. R Foundation for Statistical Computing, Vienna, Austria. Available online: http://www.R-project.org/.
45. Venables, W.N.; Ripley, B.D. Modern Applied Statistics with S, 4th ed.; Springer: New York, NY, USA, 2002.
46. Oksanen, J.; Blanchet, F.G.; Kindt, R.; Legendre, P.; Minchin, P.R.; O’Hara, R.B.; Simpson, G.L.; Solymos, P.; Stevens, M.H.H.; Wagner, H. Vegan: Community Ecology Package. R package Version 2.2-1. Available online: http://CRAN.R-project.org/package=vegan.
47. Wickham, H. GGplot2: Elegant Graphics for Data Analysis; Springer: New York, NY, USA, 2009.
48. Lefcheck, J.S.; Duffy, J.E. Multitrophic functional diversity predicts ecosystem functioning in experimental assemblages of estuarine consumers. Available online: http://dx.doi.org/10.7287/peerj.preprints.540v1.
49. Shipley, B. Confirmatory path analysis in a generalized multilevel context. Ecology 2009, 90, 363–368.
50. Shipley, B. The AIC model selection method applied to path analytic models compared using a d-separation test. Ecology 2013, 94, 560–564.
51. Agerer, R.; Schloter, M.; Hahn, C. Fungal enzymatic activity in fruitbodies. Nova Hedwig. 2000, 71, 315–336.
52. Chen, D.M.; Taylor, A.F.S.; Burke, R.M.; Cairney, J.W.G. Identification of genes for lignin peroxidases and manganese peroxidases in ectomycorrhizal fungi. New Phytol. 2001, 152, 151–158.
53. 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. ISME J. 2009, 3, 1387–1395.
54. Frey, S.D.; Knorr, M.; Parrent, J.L.; Simpson, R.T. Chronic nitrogen enrichment affects the structure and function of the soil microbial community in temperate hardwood and pine forests. For. Ecol. Manag. 2004, 196, 159–171.
55. Colpaert, J.V.; 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.
56. Conn, C.; Dighton, J. Litter quality influences on decomposition, ectomycorrhizal community structure and mycorrhizal root surface acid phosphatase activity. Soil Biol. Biochem. 2000, 32, 489–496.
57. Tedersoo, L.; Naadel, T.; Bahram, M.; Pritsch, K.; Buegger, F.; Leal, M.; Kõljalg, U.; Põldmaa, K. Enzymatic activities and stable isotope patterns of ectomycorrhizal fungi in relation to phylogeny and exploration types in an afrotropical rain forest. New Phytol. 2012, 195, 832–843.
58. Allison, S.D. Cheaters, diffusion, and nutrients constrain decomposition by microbial enzymes in spatially structured environments. Ecol. Lett. 2005, 8, 626–635.
59. Geisseler, D.; Horwath, W.R. Relationship between carbon and nitrogen availability and extracellular enzyme activities in soil. Pedobiologia 2009, 53, 87–98.
60. Six, J.; Frey, S.D.; Thiet, R.K.; Batten, K.M. Bacterial and fungal contributions to carbon sequestration in agroecosystems. Soil Sci. Soc. Am. J. 2006, 70, 555–569.
61. Zeglin, L.H.; Stursova, M.; Sinsabaugh, R.L.; Collins, S.L. Microbial responses to nitrogen addition in three contrasting grassland ecosystems. Oecologia 2007, 154, 349–359.
62. Sinsabaugh, R.L. Fungal enzymes at the community scale. In The Fungal Community; Dighton, J., Oudermans, P., White, J., Eds.; CRC Press: Boca Raton, FL, USA, 2005.
63. McClaugherty, C.A.; Linkins, A.E. Temperature responses of enzymes in 2 forest soils. Soil Biol. Biochem. 1990, 22, 29–33.
64. Nannipieri, P.; Muccini, L.; Ciardi, C. Microbial biomass and enzyme activities—Production and persistence. Soil Biol. Biochem. 1983, 15, 679–685.
65. Stursova, M.; Sinsabaugh, R.L. Stabilization of oxidative enzymes in desert soil may limit organic matter accumulation. Soil Biol. Biochem. 2008, 40, 550–553.
66. Rineau, F.; Courty, P.-E. Secreted enzymatic activities of ectomycorrhizal fungi as a case study of functional diversity and functional redundancy. Ann. For. Sci. 2011, 68, 69–80.
67. Courty, P.-E.; Buée, M.; Diedhiou, A.G.; Frey-Klett, P.; Le Tacon, F.; Rineau, F.; Turpault, M.-P.; Uroz, S.; Garbaye, J. The role of ectomycorrhizal communities in forest ecosystem processes: New perspectives and emerging concepts. Soil Biol. Biochem. 2010, 42, 679–698.