Skip to main content
Log in

Microbial Community Structure and Oxidative Enzyme Activity in Nitrogen-amended North Temperate Forest Soils

  • Published:
Microbial Ecology Aims and scope Submit manuscript

Abstract

Large regions of temperate forest are subject to elevated atmospheric nitrogen (N) deposition which can affect soil organic matter dynamics by altering mass loss rates, soil respiration, and dissolved organic matter production. At present there is no general model that links these responses to changes in the organization and operation of microbial decomposer communities. Toward that end, we studied the response of litter and soil microbial communities to high levels of N amendment (30 and 80 kg ha−1 yr−1) in three types of northern temperate forest: sugar maple/basswood (SMBW), sugar maple/red oak (SMRO), and white oak/black oak (WOBO). We measured the activity of extracellular enzymes (EEA) involved directly in the oxidation of lignin and humus (phenol oxidase, peroxidase), and indirectly, through the production of hydrogen peroxide (glucose oxidase, glyoxal oxidase). Community composition was analyzed by extracting and quantifying phospholipid fatty acids (PLFA) from soils. Litter EEA responses at SMBW sites diverged from those at oak-bearing sites (SMRO, BOWO), but the changes were not statistically significant. For soil, EEA responses were consistent across forests types: phenol oxidase and peroxidase activities declined as a function of N dose (33–73% and 5–41%, respectively, depending on forest type); glucose oxidase and glyoxal oxidase activities increased (200–400% and 150–300%, respectively, depending on forest type). Principal component analysis (PCA) ordinated forest types and treatment responses along two axes; factor 1 (44% of variance) was associated with phenol oxidase and peroxidase activities, factor 2 (31%) with glucose oxidase. Microbial biomass did not respond to N treatment, but nine of the 23 PLFA that formed >1 mol% of total biomass showed statistically significant treatment responses. PCA ordinated forest types and treatment responses along three axes (36%, 26%, 12% of variance). EEA factors 1 and 2 correlated negatively with PLFA factor 1 (r = −0.20 and −0.35, respectively, n = 108) and positively with PLFA factor 3 (r = +0.36 and +0.20, respectively, n = 108). In general, EEA responses were more strongly tied to changes in bacterial PLFA than to changes in fungal PLFA. Collectively, our data suggests that N inhibition of oxidative activity involves more than the repression of ligninase expression by white-rot basidiomycetes.

This is a preview of subscription content, log in via an institution to check access.

Access this article

Price excludes VAT (USA)
Tax calculation will be finalised during checkout.

Instant access to the full article PDF.

Figure 1
Figure 2
Figure 3
Figure 4
Figure 5

Similar content being viewed by others

References

  1. Albert, DA, Denton, SR, Barnes, BV (1986) Regional Landscape Ecosystems of Michigan. School of Natural Resources, University of Michigan, Ann Arbor.

  2. P Ander L Marzullo (1997) ArticleTitleSugar oxidoreductases and veratryl alcohol oxidase as related to lignin degradation. J Biotechnol 53 115–131

    Google Scholar 

  3. L Banci S Ciofi-Baffoni M Tien (1999) ArticleTitleLignin and Mn peroxidase-catalyzed oxidation of phenolic lignin oligomers. Biochemistry 38 3205–3210 Occurrence Handle10.1021/bi982139g Occurrence Handle1:CAS:528:DyaK1MXosV2qsg%3D%3D Occurrence Handle10074376

    Article  CAS  PubMed  Google Scholar 

  4. L Banci (1997) ArticleTitleStructural properties of peroxidases. J Biotechnol 53 253–263

    Google Scholar 

  5. B Berg E Matzner (1997) ArticleTitleEffect of N deposition on decomposition of plant litter and soil organic matter in forest systems. Environ Rev 5 1–25

    Google Scholar 

  6. MM Carreiro RL Sinsabaugh DA Repert DF Parkhurst (2000) ArticleTitleMicrobial enzyme shifts explain litter decay responses to simulated nitrogen deposition. Ecology 81 2359–2365

    Google Scholar 

  7. DeForest, JL, Zak, DR, Pregitzer, KS, Burton, AJ (2002) Anthropogenic NO 3 deposition alters microbial community function in northern hardwood forests. Submitted.

  8. K Fog (1988) ArticleTitleThe effect of added nitrogen on the rate of decomposition of organic matter. Biol Rev 63 433–462

    Google Scholar 

  9. JN Galloway WH Schlesinger H Levy A Michaels JL Schnoor (1995) ArticleTitleNitrogen fixation: Anthropogenic enhancement-environmental response. Glob Biogeochem Cy 9 235–252 Occurrence Handle10.1029/95GB00158 Occurrence Handle1:CAS:528:DyaK2MXmtlWlt7g%3D

    Article  CAS  Google Scholar 

  10. KE Hammel (1997) Fungal degradation of lignin. G Cadisch KE Giller (Eds) Driven by Nature: Plant Litter Quality and Decomposition CAB International Wallingford 33–46

    Google Scholar 

  11. KE Hammel MD Mozuch KA Jensen PJ Kersten (1994) ArticleTitleH2 O2 recycling during oxidation of the arylglycerol b-aryl ether lignin structure by lignin peroxidase and glyoxal oxidase. Biochemistry 33 13349–13354 Occurrence Handle1:CAS:528:DyaK2MXhs12jtrY%3D Occurrence Handle7947743

    CAS  PubMed  Google Scholar 

  12. SE Hobbie (2000) ArticleTitleInteractions between litter lignin and soil nitrogen availability during leaf litter decomposition in a Hawaiian montane forest. Ecosystems 3 484–494 Occurrence Handle10.1007/s100210000042 Occurrence Handle1:CAS:528:DC%2BD3cXovFWgt7s%3D

    Article  CAS  Google Scholar 

  13. SE Hobbie PM Vitousek (2000) ArticleTitleNutrient limitation of decomposition in Hawaiian forests. Ecology 81 1867–1877

    Google Scholar 

  14. WE Holmes DR Zak (1999) ArticleTitleSoil microbial control of nitrogen loss following clear-cut harvest in northern hardwood ecosystems. Ecol Appl 9 202–215

    Google Scholar 

  15. GE Host KS Pregitzer CW Ramm DP Lusch DT Cleland (1988) ArticleTitleVariation in overstory biomass among glacial landforms and ecological land units in northwestern Lower Michigan. Can J For Res 18 659–668

    Google Scholar 

  16. PJ Kersten TK Kirk (1987) ArticleTitleInvolvement of a new enzyme, glyoxal oxidase, in extracellular H2O2 production by Phanerochaete chrysosporium. J Bacteriol 169 2195–2201 Occurrence Handle1:CAS:528:DyaL2sXksFGnt7g%3D Occurrence Handle3553159

    CAS  PubMed  Google Scholar 

  17. P Keyser T Kirk JG Zeikus (1978) ArticleTitleLigninolytic enzyme system of Phanerochaete chrysosporium: synthesized in the absence of lignin in response to nitrogen starvation. J Bacteriol 135 790–797 Occurrence Handle1:CAS:528:DyaE1cXlslKis7o%3D Occurrence Handle690075

    CAS  PubMed  Google Scholar 

  18. TK Kirk RL Farrell (1987) ArticleTitleEnzymatic “combustion”: The microbial degradation of lignin. Ann Rev Microbiol 41 465–505 Occurrence Handle10.1146/annurev.mi.41.100187.002341 Occurrence Handle1:CAS:528:DyaL2sXmtlalu7o%3D

    Article  CAS  Google Scholar 

  19. A Leonowicz N-S Cho J Luterek A Wilkolazka M Wojtas-Wasilewska A Matuszewska M Hofrichter D Wesenberg J Rogalski (2001) ArticleTitleFungal laccase: properties and activity of lignin. J Basic Microbiol 41 185–227

    Google Scholar 

  20. AH Magill JD Aber (1998) ArticleTitleLong-term effects of experimental nitrogen additions on foliar litter decay and humus formation in forest ecosystems. Plant Soil 203 301–311 Occurrence Handle10.1023/A:1004367000041 Occurrence Handle1:CAS:528:DyaK1cXnvFelt7Y%3D

    Article  CAS  Google Scholar 

  21. T Mester M Tien (2000) ArticleTitleOxidation mechanism of ligninolytic enzymes involved in the degradation of environmental pollutants. Int Biodeter Biodegr 46 51–59 Occurrence Handle10.1016/S0964-8305(00)00071-8 Occurrence Handle1:CAS:528:DC%2BD3cXnsVegu7s%3D

    Article  CAS  Google Scholar 

  22. CA Metosh-Dickey RP Mason GW Winston (1998) ArticleTitleSingle electron reduction of xenobiotic compounds by glucose oxidase from Asperillus niger. Free Radical Biol Med 24 155–160 Occurrence Handle10.1016/S0891-5849(97)00207-4 Occurrence Handle1:CAS:528:DyaK2sXotVSjsr8%3D

    Article  CAS  Google Scholar 

  23. RT Myers DR Zak DC White A Peacock (2001) ArticleTitleLandscape-level patterns of microbial community composition and substrate use in upland forest ecosystems. Soil Sci Soc Am J 65 359–367 Occurrence Handle1:CAS:528:DC%2BD38Xpt1Ki

    CAS  Google Scholar 

  24. KJ Nadelhoffer BA Emmett P Gundersen OJ Kjoaas CJ Koopmans P Schleppi A Tietema RF Wright (1999) ArticleTitleNitrogen decomposition makes a minor contribution to carbon sequestration in temperate forests. Nature 398 145–148 Occurrence Handle10.1038/18205 Occurrence Handle1:CAS:528:DyaK1MXhvFKis7Y%3D

    Article  CAS  Google Scholar 

  25. AM O’Connell (1994) ArticleTitleDecomposition and nutrient content of litter in a fertilized eucalypt forest. Biol Fertil Soils 17 159–166 Occurrence Handle1:CAS:528:DyaK2cXltlejsL4%3D

    CAS  Google Scholar 

  26. KR Saiya-Cork RL Sinsabaugh DR Zak (2002) ArticleTitleThe effects of long term nitrogen deposition on extracellular enzyme activity in an Acer saccharum forest soil. Soil Biol Biochem 34 1309–1315 Occurrence Handle10.1016/S0038-0717(02)00074-3 Occurrence Handle1:CAS:528:DC%2BD38XlvVemu7w%3D

    Article  CAS  Google Scholar 

  27. RL Sinsabaugh MM Carreiro DA Repert (2002) ArticleTitleAllocation of extracellular enzymatic activity in relation to litter composition, N deposition, and mass loss. Biogeochemistry 60 1–24

    Google Scholar 

  28. PM Vitousek JD Aber RW Howarth GE Likens PA Matson DW Schindler WH Schlesinger DG Tilman (1997) ArticleTitleHuman alterations of the global nitrogen cycle: sources and consequences. Ecol Appl 7 737–750

    Google Scholar 

  29. DC White WM Davis JC Nickels JC King RJ Bobbie (1979) ArticleTitleDetermination of sedimentary microbial biomass by extractable lipid phosphate. Oecologia 40 51–62 Occurrence Handle10.1007/BF00388810

    Article  Google Scholar 

  30. DC White DB Ringelberg (1998) Signature lipid biomarker analysis. RS Burglage R Atlas D Stahl G Geesey G Sayler (Eds) Techniques in Microbial Ecology Oxford New York 255–272

    Google Scholar 

  31. DR Zak GE Host KS Pregitzer (1989) ArticleTitleRegional variability in nitrogen, nitrification, and overstory biomass in northern Lower Michigan. Can J Forest Res 19 1521–1526

    Google Scholar 

  32. DR Zak KS Pregitzer (1990) ArticleTitleSpatial and temporal variability of nitrogen cycling in northern lower Michigan. Forest Sci 36 367–380

    Google Scholar 

  33. DR Zak KS Pregitzer GE Host (1986) ArticleTitleLandscape variation in nitrogen mineralization and nitrification. Can J Forest Res 16 1258–1263

    Google Scholar 

Download references

Acknowledgments

We are grateful to David White (Univ. Tennessee) for analyzing the PLFA extracts and to Matt Tomlinson for maintaining the experimental plots. This research was supported by the Office of Science (BER), U.S. Department of Energy, Grant No. DE-FG02-03ER63591.

Author information

Authors and Affiliations

Authors

Corresponding author

Correspondence to R. L. Sinsabaugh.

Rights and permissions

Reprints and permissions

About this article

Cite this article

Gallo, M., Amonette, R., Lauber, C. et al. Microbial Community Structure and Oxidative Enzyme Activity in Nitrogen-amended North Temperate Forest Soils. Microb Ecol 48, 218–229 (2004). https://doi.org/10.1007/s00248-003-9001-x

Download citation

  • Received:

  • Accepted:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1007/s00248-003-9001-x

Keywords

Navigation