Advertisement

Trees

, Volume 30, Issue 2, pp 497–508 | Cite as

Ectomycorrhizal fungal exoenzyme activity differs on spruce seedlings planted in forests versus clearcuts

  • Jennifer K. M. Walker
  • Valerie Ward
  • Melanie D. Jones
Original Paper
Part of the following topical collections:
  1. Mycorrhiza

Abstract

Key message

Ectomycorrhizal (ECM) fungal community structure and potential exoenzymatic activity change after clearcut harvesting, but functional complementarity and redundancy among those ECM fungal species remaining support growth of regenerating seedlings.

Abstract

Ectomycorrhizal (ECM) fungal community composition is altered by forest harvesting, but it is not clear if this shift in structure influences ECM fungal physiological function at the community level. In this study, we characterized activities of extracellular enzymes in the ectomycorrhizospheres of Picea engelmannii seedlings grown in forest and clearcut plots. These exoenzymes are critical for the breakdown of large organic molecules, from which nutrients are subsequently absorbed and translocated by ECM fungi to host plants. We found that ectomycorrhizae on seedlings planted in forests had different exoenzyme activity profiles than those on seedlings planted in clearcuts. Specifically, the activities of glucuronidase, laccase, and acid phosphatase were higher on forest seedlings (P ≤ 0.006). These differences may have been partly driven by soil properties. Total carbon, total nitrogen (N), extractable phosphorus, extractable ammonium-N, and mineralizable N were higher, while pH was lower in forest plots (P ≤ 0.01). However, we also found that enzyme activity only shifted where community composition also changed. Functional complementarity can be inferred within ECM fungal communities in both forests and clearcuts because ectomycorrhizae formed by different species in the same environment had distinct enzyme profiles (P < 0.0001). However, ectomycorrhizae of Thelephora terrestris exhibited high levels of N- and P-mobilizing exoenzyme activities. Seedling biomass did not differ between forest and clearcut environments, so the high abundance of T. terrestris ectomycorrhizae in the clearcuts may have sustained nutrient acquisition by clearcut seedlings even in soils with lower N and P and with reduced ECM fungal species richness.

Keywords

Exoenzyme assay Ectomycorrhizal physiology Functional complementarity and redundancy Picea engelmannii Bioassay seedling Clearcut harvesting 

Notes

Acknowledgments

This research was supported by a Discovery Grant from the Natural Sciences and Engineering Research Council of Canada and by the Forest Investment Account of the Forest Science Program of the British Columbia (BC) Ministry of Forests, Lands and Natural Resource Operations (MFLNRO) awarded to MJ. JW acknowledges support from the University of British Columbia, Okanagan Campus and the Province of British Columbia for scholarships. We thank Alan Vyse for access to information about the Sicamous Creek field site, MaryAnn Olson, Fawn Ross, and Brendan Twieg for help in the field, and Natasha Lukey and Ayla Fortin for help in the field and lab. Finally, we are immensely grateful to the BC MFLNRO for establishment and long-term maintenance of the Sicamous Creek Silvicultural System Research Project (http://www.for.gov.bc.ca/rsi/research/sicamous/index.htm).

Conflict of interest

The authors declare that they have no conflict of interest.

Supplementary material

468_2015_1239_MOESM1_ESM.docx (45 kb)
Supplementary material 1 (DOCX 44 kb)

References

  1. Agerer R (1987–2002) Colour atlas of ectomycorrhizae. Einhorn-Verlag Eduard Dietenberger, Schwäbisch GmündGoogle Scholar
  2. Berg MP, Ellers J (2010) Trait plasticity in species interactions: a driving force of community dynamics. Evol Ecol 24:617–629CrossRefGoogle Scholar
  3. Bever JD, Dickie IA, Facelli E, Facelli JM, Klironomos J, Moora M, Rillig MC, Stock WD, Tibbett M, Zobel M (2010) Rooting theories of plant community ecology in microbial interactions. Trends Ecol Evol 25:468–478CrossRefPubMedPubMedCentralGoogle Scholar
  4. Botton S, van Heusden M, Parsons JR, Smidt H, van Straalen N (2006) Resilience of microbial systems towards disturbances. Crit Rev Microbiol 32:101–112CrossRefPubMedGoogle Scholar
  5. Buée M, Courty PE, Mignot D, Garbaye J (2007) Soil niche effect on species diversity and catabolic activities in an ectomycorrhizal fungal community. Soil Biol Biochem 39:1947–1955CrossRefGoogle Scholar
  6. Burke DJ, Weintraub MN, Hewins CR, Kalisz S (2011) Relationship between soil enzyme activities, nutrient cycling and soil fungal communities in a northern hardwood forest. Soil Biol Biochem 43:795–803CrossRefGoogle Scholar
  7. Courty PE, Pritsch K, Schloter M, Hartmann A, Garbaye J (2005) Activity profiling of ectomycorrhiza communities in two forest soil using multiple enzymatic tests. New Phytol 167:309–319CrossRefPubMedGoogle Scholar
  8. Courty PE, Pouysegur R, Buée M, Garbaye J (2006) Laccase and phosphatase activities of the dominant ectomycorrhizal types in a lowland oak forest. Soil Biol Biochem 38:1219–1222CrossRefGoogle Scholar
  9. Courty PE, Breda N, Garbaye J (2007) Relationship between oak tree phenology and the secretion of organic matter degrading enzymes by Lactarius quietus ectomycorrhizas before and during bud break. Soil Biol Biochem 39:1655–1663CrossRefGoogle Scholar
  10. Dickie IA, Reich PB (2005) Ectomycorrhizal fungal communities at forest edges. J Ecol 93:244–255CrossRefGoogle Scholar
  11. Dickie IA, Richardson SJ, Wiser SK (2009) Ectomycorrhizal fungal communities and soil chemistry in harvested and unharvested temperate Nothofagus rainforests. Can J Forest Res 39:1069–1079CrossRefGoogle Scholar
  12. Ding Q, Liang Y, Legendre P, He X, Pei K, Du X, Ma K (2011) Diversity and composition of ectomycorrhizal community on seedling roots: the role of host preference and soil origin. Mycorrhiza 12:669–680CrossRefGoogle Scholar
  13. Gardes M, Bruns TD (1993) ITS primers with enhanced specificity for Basidiomycetes—application to the identification of mycorrhizae and rusts. Mol Ecol 2:113–118CrossRefPubMedGoogle Scholar
  14. Goodman DM, Durall DM, Trofymow JA, Berch SM (1996) A manual of concise descriptions of North American Ectomycorrhizae. Mycologue Publications, Sydney, 3A1–3A5Google Scholar
  15. Grønflaten LK, Steinnes E, Örlander G (2008) Effect of conventional and while-tree clear-cutting on concentrations of some micronutrients in coniferous soil and plants. For Studies (Metsanduslikud Uurimused) 48:5–16Google Scholar
  16. Hagerman SH, Jones MD, Bradfield GE, Gillespie M, Durall DM (1999) Effects of clear-cut logging on the diversity and persistence of ectomycorrhizas at a subalpine forest. Can J Forest Res 29:124–134CrossRefGoogle Scholar
  17. Hannam KD, Prescott CE (2003) Soluble organic nitrogen in forests and adjacent clearcuts in British Columbia, Canada. Can J Forest Res 33:1709–1718CrossRefGoogle Scholar
  18. Jones MD, Durall DM, Cairney JGW (2003) Ectomycorrhizal fungal communities in young stands regenerating after clearcut logging. New Phytol 157:399–422CrossRefGoogle Scholar
  19. Jones MD, Grenon F, Peat H, Fitzgerald M, Holt L, Philip LJ, Bradley R (2009) Differences in 15N uptake among spruce seedlings colonized by three pioneer ectomycorrhizal fungi in the field. Fungal Ecol 2:110–120CrossRefGoogle Scholar
  20. Jones MD, Tweig BD, Ward V, Barker J, Durall DM, Simard SW (2010) Functional complementarity of Douglas-fir ectomycorrhizas for extracellular enzyme activity after wildfire or clearcut logging. Funct Ecol 24:1139–1151CrossRefGoogle Scholar
  21. Jones MD, Phillips LA, Treu R, Ward V, Berch SM (2012) Functional responses of ectomycorrhizal fungal communities to long-term fertilization of lodgepole pine (Pinus contorta Dougl. Ex Loud. Var. latifola Engelm.) stands in central British Columbia. Appl Soil Ecol 60:29–40CrossRefGoogle Scholar
  22. Jonsson LM, Nilsson M-C, Wardle DA, Zackrisson O (2001) Context dependent effets of ectomycorrhizal species richness on tree seedling productivity. Oikos 93:352–364CrossRefGoogle Scholar
  23. Kranabetter JM, Friesen J (2002) Ectomycorrhizal community structure on western hemlock (Tsuga heterophylla) seedlings transplanted from forests into openings. Can J Bot 80:861–868CrossRefGoogle Scholar
  24. Lennon JT, Aanderud ZT, Lehmkuhl BK, Schoolmaster DR Jr (2012) Mapping the niche space of soil organisms using taxonomy and traits. Ecology 93:1867–1879CrossRefPubMedGoogle Scholar
  25. Olander LP, Vitousek PM (2000) Regulation of soil phosphatase and chitinase activity by N and P availability. Biogeochemistry 49:175–191CrossRefGoogle Scholar
  26. Phillips LA, Ward V, Jones MJ (2014) Ectomycorrhizal fungi contribute to soil organic matter cycling in sub-boreal forests. ISME 8:699–713CrossRefGoogle Scholar
  27. Pritsch K, Raidl S, Marksteiner E, Agerer R, Blaschke H, Schloter M, Hartmann A (2004) A rapid and highly sensitive method fro measuring enzyme activities in single mycorrhizal tips using 4-methylumbelliferone-labelled fluorogenic substrates in a microplate system. J Microbiol Methods 58:233–241CrossRefPubMedGoogle Scholar
  28. Read DJ, Perez-Moreno J (2003) Mycorrhizas and nutrient cycling in ecosystems—a journey towards relevance? New Phytol 157:475–492CrossRefGoogle Scholar
  29. Rineau F, Courty PE (2011) Secreted enzymatic activities of ectomycorrhizas as a case study of functional diversity and functional redundancy. Ann Forest Sci 68:69–80CrossRefGoogle Scholar
  30. Rineau F, Garbaye J (2009) Does forest liming impact the enzymatic profiles of ectomycorrhizal communities through specialized fungal symbionts? Mycorrhiza 19:493–500CrossRefPubMedGoogle Scholar
  31. Rineau F, Roth D, Shah F, Smits M, Johansson T, Canbäck B, Olsen PB, Persson P, Grell MN, Lindquist E, Grigoriev IV, Lange L, Tunlid A (2012) The ectomycorrhizal fungus Paxillus involutus converts organic matter in plant litter using a trimmed brown-rot mechanism involving Fenton chemistry. Environ Microbiol 14:1477–1487CrossRefPubMedPubMedCentralGoogle Scholar
  32. Sinsabaugh RL, Lauber CL, Weintraub MN, Ahmed B, Allison SD, Crenshaw C, Contosa AR et al (2008) Stoichiometry of soil enzyme activity at global scale. Ecol Lett 11:1252–1264PubMedGoogle Scholar
  33. Smith SE, Read DJ (2008) Mycorrhizal symbiosis, 3rd edn. Academic Press, LondonGoogle Scholar
  34. Talbot JM, Bruns TD, Smith DP, Branco S, Glassman SI, Erlandson S, Vilgalys R, Peay KG (2013) Independent roles of ectomycorrhizal and saprotrophic communities in soil organic matter decomposition. Soil Biol Biochem 57:282–291CrossRefGoogle Scholar
  35. Tarafdar JC, Claassen N (1988) Organic phosphorus compounds as a phosphorus source for higher plants through the activity of phosphatase produced by plant roots and microorganisms. Biol Fertil Soils 5:308–312CrossRefGoogle Scholar
  36. Vyse A (1997) The Sicamous Creek Silvicultural Systems Project: how the project came to be and what it aims to accomplish. In: Hollstedt C, Vyse A. (Eds.) Sicamous Creek Silvicultural Systems Project: Workshop proceedings, April 24–25, 1996, Kamloops, Work Pap. 24/1997. Res. Br., B.C. Min. For., VictoriaGoogle Scholar
  37. Walker JKM, Jones MJ (2013) Little evidence for niche partitioning among ectomycorrhizal fungi on spruce seedlings planted in decayed wood versus mineral soil microsites. Oecologia 173:1499–1511CrossRefPubMedGoogle Scholar
  38. Walker JKM, Cohen H, Higgins LM, Kennedy PG (2014) Testing the link between community structure and function for ectomycorrhizal fungi involved in a global tripartite symbiosis. New Phytol 202:287–296CrossRefPubMedGoogle Scholar
  39. White TJ, Bruns T, Lee S, Taylor JW (1990) Amplification and direct sequencing of fungal ribosomal RNA genes for phylogenetics. In: Innis MA, Gelfand DH, Sninsky JJ, White TJ (eds) PCR protocols: a guide to methods and applications. Academic Press, New York, pp 315–322Google Scholar

Copyright information

© Springer-Verlag Berlin Heidelberg 2015

Authors and Affiliations

  • Jennifer K. M. Walker
    • 1
    • 2
  • Valerie Ward
    • 1
  • Melanie D. Jones
    • 1
  1. 1.Biology DepartmentUniversity of British Columbia, Okanagan Campus, Science BuildingKelownaCanada
  2. 2.Hawkesbury Institute for the EnvironmentUniversity of Western SydneyPenrithAustralia

Personalised recommendations