Abstract
Increased nitrogen (N) deposition caused by human activities has altered ecosystem functioning and biodiversity. To understand the effects of altered N availability, we measured the abundance of arbuscular mycorrhizal fungi (AMF) and the microbial community in northern hardwood forests exposed to long-term (12 years) simulated N deposition (30 kg N ha−1 y−1) using phospholipid fatty acid (PLFA) analysis and hyphal in-growth bags. Intra- and extraradical AMF biomass and total microbial biomass were significantly decreased by simulated N deposition by 36, 41, and 24%, respectively. Both methods of extraradical AMF biomass estimation (soil PLFA 16:1ω5c and hyphal in-growth bags) showed comparable treatment responses, and extraradical biomass represented the majority of total (intra-plus extraradical) AMF biomass. N deposition also significantly affected the microbial community structure, leading to a 10% decrease in fungal to bacterial biomass ratios. Our observed decline in AMF and total microbial biomass together with changes in microbial community structure could have substantial impacts on the nutrient and carbon cycling within northern hardwood forest ecosystems.
This is a preview of subscription content, access via your institution.




References
Allison VJ, Miller RM, Jastrow JD, Matamala R, Zak DR. 2005. Changes in soil microbial community structure in a tallgrass prairie chronosequence. Soil Sci Soc Am J 69:1412–21.
Allison SD, Czimczik CI, Treseder KK. 2008. Microbial activity and soil respiration under nitrogen addition in Alaskan boreal forest. Glob Change Biol 14:1156–68.
Anderson MJ (2004) CAP: a FORTRAN computer program for canonical analysis of principal coordinates. Department of Statistics, University of Auckland, New Zealand
Anderson MJ (2005) PERMANOVA: a FORTRAN computer program for permutational multivariate analysis of variance. Department of Statistics, University of Auckland, New Zealand
Augé RM. 2004. Arbuscular mycorrhizae and soil/plant water relations. Can J Soil Sci 84:373–81.
Balser TC, Treseder KK, Ekenler M. 2005. Using lipid analysis and hyphal length to quantify AM and saprotrophic fungal abundance along a soil chronosequence. Soil Biol Biochem 37:601–4.
Berg B, Matzner E. 1997. Effect of N deposition on decomposition of plant litter and soil organic matter in forest systems. Environ Rev 5:1–25.
Burton AJ, Pregitzer KS, Reed DD. 1991. Leaf area and foliar biomass relationships in northern hardwood forests located along an 800 km acid deposition gradient. For Sci 37:1041–59.
Burton AJ, Pregitzer KS, Crawford JN, Zogg GP, Zak DR. 2004. Simulated chronic NO3− addition reduces soil respiration in northern hardwood forests. Glob Change Biol 10:1080–91.
Compton JE, Watrud LS, Porteous LA, DeGrood S. 2004. Response of soil microbial biomass and community composition to chronic nitrogen additions at Harvard forest. For Ecol Manag 196:143–58.
Cunha A, Power SA, Ashmore MR, Green PRS, Haworth BJ, Bobbink R (2002) Whole ecosystem nitrogen manipulation: an updated review. JNCC report 331. ISSN 0963 8091.
DeForest JL, Zak DR, Pregitzer KS, Burton AJ. 2004. Atmospheric nitrate deposition, microbial community composition, and enzyme activity in northern hardwood forests. Soil Sci Soc Am J 68:132–8.
Eom A-H, Hartnett DC, Wilson GWT, Figge DAH. 1999. The effect of fire, mowing and fertilizer amendment on arbuscular mycorrhizas in tallgrass prairie. Am Midl Nat 142:55–70.
Frey SD, Knorr M, Parrent JL, Simpson RT. 2004. Chronic nitrogen enrichment affects the structure and function of the soil microbial community in temperate hardwood and pine forests. For Ecol Manag 196:159–71.
Frostegård A, Bååth E. 1996. The use of phospholipids fatty acid analysis to estimate bacterial and fungal biomass in soil. Biol Fertil Soils 22:59–65.
Garcia MO, Ovasapyan T, Greas M, Treseder KK. 2008. Mycorrhizal dynamics under elevated CO2 and nitrogen fertilization in a warm temperate forest. Plant Soil 303:301–10.
Godman RM, Yawney HW, Tubbs CH (1990) Acer saccharum Marsh. Sugar maple. In: Burns RM, Honkola BH (eds) Silvics of North America: 2. Hardwoods. Agriculture Handbook, vol 654. Forest Service, United States Department of Agriculture, Washington, DC, USA. pp 78–91.
Gryndler M, Larsen J, Hršelová H, Řezáčová V, Gryndlerová H, Kubát J. 2006. Organic and mineral fertilization, respectively, increase and decrease the development of external mycelium of arbuscular mycorrhizal fungi in a long-term field experiment. Mycorrhiza 16:159–66.
Hart SC, Gehring CA, Selmants PC, Deckert RJ. 2006. Carbon and nitrogen elemental and isotopic patterns in macrofungal sporocarps and trees in semiarid forests of the south-western USA. Funct Ecol 20:42–51.
Joergensen RG, Wichern F. 2008. Quantitative assessment of the fungal contribution to microbial tissue in soil. Soil Biol Biochem 40:2977–91.
Johnson NC, Rowland DL, Corkidi L, Egerton-Warburton LM, Allen EB. 2003. Nitrogen enrichment alters mycorrhizal allocation at five mesic to semiarid grasslands. Ecology 84:1895–908.
Leake J, Johnson D, Donnelly D, Muckle G, Boddy L, Read D. 2004. Networks of power and influence: the role of mycorrhizal mycelium in controlling plant communities and agroecosystem functioning. Can J Bot 82:1016–45.
NADP. 2006. National Atmospheric Deposition Program (NRSP-3) NADP Program Office, Illinois State Water Survey, IL, USA.
Olsson PA. 1999. Signature fatty acids provide tools for determination of the distribution and interactions of mycorrhizal fungi in soil. FEMS Microbiol Ecol 29:303–10.
Olsson PA, Johansen A. 2000. Lipid and fatty acid composition of hyphae and spores of arbuscular mycorrhizal fungi at different growth stages. Mycol Res 104:429–34.
Olsson PA, Wilhelmsson P. 2000. The growth of external AM fungal mycelium in sand dunes and in experimental systems. Plant Soil 226:161–9.
Olsson PA, Bååth E, Jakobsen I. 1997. Phosphorus effects on the mycelium and storage structures of an arbuscular mycorrhizal fungus as studied in the soil and roots by analysis of fatty acid signatures. Appl Environ Microbiol 63:3531–8.
Phillips RP, Fahey TJ. 2007. Fertilization effects on fine root biomass, rhizosphere microbes and respiratory fluxes in hardwood forest soils. New Phytol 176:655–64.
Pregitzer KS, DeForest JL, Burton AJ, Allen MF, Ruess RW, Hendrick RL. 2002. Fine root architecture of nine North American trees. Ecol Monogr 72:293–309.
Pregitzer KS, Zak DR, Burton AJ, Ashby JA, MacDonald NW. 2004. Chronic nitrate additions dramatically increase the export of carbon and nitrogen from northern hardwood ecosystems. Biogeochemistry 68:179–97.
Pregitzer KS, Burton AJ, Zak DR, Talhelm AF. 2008. Simulated chronic nitrogen deposition increases carbon storage in northern temperate forests. Glob Change Biol 14:142–53.
Rillig MC. 2004. Arbuscular mycorrhizae and terrestrial ecosystem processes. Ecol Lett 7:740–54.
Rillig MC, Wright SF, Nichols KA, Schmidt WF, Torn MS. 2001. Large contribution of arbuscular mycorrhizal fungi to soil carbon pools in tropical forest soils. Plant Soil 233:167–77.
Smith SE, Read DJ. 2008. Mycorrhizal symbiosis. 3rd edn. New York: Academic Press.
Stahl PD, Schuman GE, Frost SM, Williams SE. 1998. Arbuscular mycorrhizae and water stress tolerance of Wyoming big sagebrush seedlings. Soil Sci Soc Am J 62:1309–13.
Treseder KK. 2004. A meta-analysis of mycorrhizal responses to nitrogen, phosphorus, and atmospheric CO2 in field studies. New Phytol 164:347–55.
Treseder KK. 2008. Nitrogen additions and microbial biomass: a meta-analysis of ecosystem studies. Ecol Lett 11:1111–20.
Treseder KK, Allen MF. 2002. Direct nitrogen and phosphorus limitation of arbuscular mycorrhizal fungi: a model and field test. New Phytol 155:507–15.
Treseder KK, Turner KM. 2007. Glomalin in ecosystems. Soil Sci Soc Am J 71:1257–66.
Treseder KK, Turner KM, Mack MC. 2007. Mycorrhizal responses to nitrogen fertilization in boreal ecosystems: potential consequences for soil carbon storage. Glob Change Biol 13:78–88.
Tunlid A, White DC. 1992. Biochemical analysis of biomass, community structure, nutritional status, and metabolic activity of microbial communities in soil. Soil Biochem 7:229–62.
van der Heijden MGA, Klironomos JN, Ursic M, Moutoglis P, Streitwolf-Engel R, Boller T, Wiemken A, Sanders IR. 1998. Mycorrhizal fungal diversity determines plant biodiversity, ecosystem variability and productivity. Nature 396:69–72.
van Diepen LTA, Lilleskov EA, Pregitzer KS, Miller RM. 2007. Decline of arbuscular mycorrhizal fungi in northern hardwood forests exposed to chronic nitrogen additions. New Phytol 176:175–83.
Vitousek PM, Aber JD, Howarth RW, Likens GE, Matson PA, Schindler DW, Schlesinger WH, Tilman DG. 1997. Human alteration of the global nitrogen cycle: sources and consequences. Ecol Appl 7:737–50.
Waldrop MP, Zak DR, Sinsabaugh RL. 2004. Microbial community response to nitrogen deposition in northern forest ecosystems. Soil Biol Biochem 36:1443–51.
Wallander H, Nylund JE. 1992. Effects of excess nitrogen and phosphorus starvation on the extramatrical mycelium of ectomycorrhizas of Pinus sylvestris L. New Phytol 120:495–503.
Wallander H, Nilsson LO, Hagerberg D, Bååth E. 2001. Estimation of the biomass and seasonal growth of external mycelium of ectomycorrhizal fungi in the field. New Phytol 151:753–60.
Wallenda T, Kottke I. 1998. Nitrogen deposition and ectomycorrhizas. New Phytol 139:169–87.
Wallenstein MD, McNulty S, Fernandez IJ, Boggs J, Schlesinger WH. 2006. Nitrogen fertilization decreases forest soil fungal and bacterial biomass in three long-term experiments. For Ecol Manag 222:459–68.
Zak DR, Ringelberg DB, Pregitzer KS, Randlett DL, White DC, Curtis PS. 1996. Soil microbial communities beneath Populus grandidentata grown under elevated atmospheric CO2. Ecol Appl 6:257–62.
Zak DR, Holmes WE, Burton AJ, Pregitzer KS, Talhelm AF. 2008. Simulated atmospheric NO3 − deposition increases soil organic matter by slowing decomposition. Ecol Appl 18:2016–27.
Acknowledgments
We thank the NSF (Grant # 0614422 and 0735116) and the USDA Forest Service, Northern Research Station for their continued support of this project, and the Ecosystem Science Center from Michigan Technological University for their research grant which supported part of this project. We also thank two anonymous reviewers for their comments on a previous version of this manuscript. Further, we are thankful to Cheryl Krol for analyzing some of the PLFA samples (Argonne National Laboratory).
Author information
Authors and Affiliations
Corresponding author
Additional information
Author Contributions
LVD, EAL and KSP designed the study. EAL, KSP and RMM contributed to writing paper. LVD performed research, analyzed data and wrote the paper.
Electronic supplementary material
Rights and permissions
About this article
Cite this article
van Diepen, L.T.A., Lilleskov, E.A., Pregitzer, K.S. et al. Simulated Nitrogen Deposition Causes a Decline of Intra- and Extraradical Abundance of Arbuscular Mycorrhizal Fungi and Changes in Microbial Community Structure in Northern Hardwood Forests. Ecosystems 13, 683–695 (2010). https://doi.org/10.1007/s10021-010-9347-0
Received:
Accepted:
Published:
Issue Date:
DOI: https://doi.org/10.1007/s10021-010-9347-0
Keywords
- arbuscular mycorrhizal fungi
- phospholipid fatty acid
- nitrogen
- mycelium
- microbial community
- sugar maple (Acer saccharum)
- forest
- in-growth bags