Skip to main content Accessibility help

We use cookies to distinguish you from other users and to provide you with a better experience on our websites. Close this message to accept cookies or find out how to manage your cookie settings.

Close cookie message
×
Hostname: page-component-745bb68f8f-kw2vx Total loading time: 0 Render date: 2025-01-27T13:06:38.247Z Has data issue: false hasContentIssue false

10 - Microbial community composition and soil nitrogen cycling: is there really a connection?

Published online by Cambridge University Press:  17 September 2009

By
Joshua P. Schimel ,
Jennifer Bennett  and
Noah Fierer
Edited by
Richard Bardgett ,
Michael Usher  and
David Hopkins
Joshua P. Schimel
Affiliation:
University of California at Santa Barbara
Jennifer Bennett
Affiliation:
North Carolina State University
Noah Fierer
Affiliation:
University of California at Santa Barbara
Richard Bardgett
Affiliation:
Lancaster University
Michael Usher
Affiliation:
University of Stirling
David Hopkins
Affiliation:
University of Stirling
Get access

Summary

SUMMARY

  1. In the classical view of nitrogen cycling, the processes that involve nitrogen inputs and outputs (e.g. fixation, denitrification) are physiologically ‘narrow’ and so should be sensitive to microbial community composition, while internal turn-over (i.e. mineralisation, immobilisation) involves ‘aggregate’ processes that should be insensitive to microbial community composition.

  2. A newly developing view of nitrogen cycling, however, identifies several ways in which mineralisation and immobilisation can be ‘disaggregated’ into individual components that may be sensitive to microbial community composition. Two of these are extracellular enzyme and microsite phenomena.

  3. Exoenzymes are critical in driving decomposition, and hence mineralisation/immobilisation. Different classes of enzymes are produced by different groups of microorganisms. Additionally, the kinetics of exoenzymes may regulate microbial carbon and nitrogen limitation and hence community composition.

  4. Microsite phenomena appear to regulate system-level nitrogen cycling (e.g. the occurrence of nitrification in nitrogen-poor soils), yet these effects scale non-linearly to the whole system. Different organisms may live and function in different types of microsites.

  5. This new view of the nitrogen cycle provides an intellectual structure for developing research linking microbial populations and the nitrogen cycling processes they carry out.

Introduction

Since the days of Winogradsky and Beijerink in the late nineteenth century, nitrogen cycling has been at the centre of soil microbiology. Since then, we have largely deciphered the microbial physiology of the important nitrogen cycling processes and have identified some of the important microbial groups involved in them.

Type
Chapter
Information
Biological Diversity and Function in Soils , pp. 171 - 188
Publisher: Cambridge University Press
Print publication year: 2005

Access options

Get access to the full version of this content by using one of the access options below. (Log in options will check for institutional or personal access. Content may require purchase if you do not have access.)

References

Aber, J. D., Melillo, J. M. & McClaugherty, C. A. (1990). Predicting long-term patterns of mass loss, nitrogen dynamics, and soil organic matter formation from initial fine litter chemistry in temperate forest ecosystems. Canadian Journal of Botany, 68, 2201–2208CrossRefGoogle Scholar
Alexander, M. (1985). Ecological constraints on nitrogen fixation in agricultural ecosystems. Advances in Microbial Ecology, 8, 163–183Google Scholar
Balser, T., Kinzig, A. & Firestone, M. (2002). The functional consequences of biodiversity. The Functional Consequences of Biodiversity (Ed. by , A. Kinzig, , S. Pacala & , D. Tilman), pp. 265–293. Princeton, NJ: Princeton University Press
Bardgett, R. D., Mawdsley, J. L., Edwards, S., et al. (1999). Plant species and nitrogen effects on soil biological properties of temperate upland grasslands. Functional Ecology, 13, 650–660CrossRefGoogle Scholar
Bayer, E. A., Shoham, Y. & Lamed, R. (2001). Cellulose-decomposing bacteria and their enzyme systems. The Prokaryotes: An Evolving Electronic Resource for the Microbiological Community, 3rd edition, release 3.7, November 2, 2001 (Ed. by , M. Dworkinet al.). New York: Springer-Verlag, www.prokaryotes.com
Beare, M. H., Coleman, D. C. & Crossley, D. A. (1995). A hierarchical approach to evaluating the significance of soil biodiversity to biogeochemical cycling. Plant and Soil, 170, 5–22CrossRefGoogle Scholar
Bending, G. D. & Read, D. J. (1996). Nitrogen mobilization from protein–polyphenol complex by ericoid and ectomycorrhizal fungi. Soil Biology and Biochemistry, 28, 1603–1612CrossRefGoogle Scholar
Bending, G. D. & Read, D. J. (1997). Lignin and soluble phenolic degradation by ectomycorrhizal and ericoid mycorrhizal fungi. Mycological Research, 101, 1348–1354CrossRefGoogle Scholar
Benson, D. R. & Silvester, W. B. (1993). Biology of Frankia strains, actinomycete symbionts of actinorhizal plants. Microbiological Reviews, 57, 293–319Google ScholarPubMed
Berg, B. (2000). Litter decomposition and organic matter turnover in northern forest soils. Forest Ecology and Management, 133, 13–22CrossRefGoogle Scholar
Berg, B. & Matzner, E. (1997). Effect of N deposition on plant litter and soil organic matter in forest systems. Ecological Reviews, 5, 1–25Google Scholar
Bergsma, T. T., Robertson, G. P. & Ostrom, N. E. (2002). Influence of soil moisture and land use history on denitrification end-products. Journal of Environmental Quality, 31, 711–717CrossRefGoogle ScholarPubMed
Bhat, M. K. & Bhat, S. (1997). Cellulose degrading enzymes and their potential industrial applications. Biotechnology Advances, 15, 583–620CrossRefGoogle ScholarPubMed
Bhat, T. K., Sing, B. & Sharma, O. P. (1998). Microbial degradation of tannins: a current perspective. Biodegradation, 9, 343–357CrossRefGoogle ScholarPubMed
Blackwood, C. B. & Paul, E. A. (2003). Eubacterial community structure and population size within the soil light fraction, rhizosphere, and heavy fraction of several agricultural systems. Soil Biology and Biochemistry, 35, 1245–1255CrossRefGoogle Scholar
Bodelier, P. L. E., Roslev, P., Henckel, T. & Frenzel, P. (2000). Stimulation by ammonium-based fertilizers of methane oxidation in soil around rice roots. Nature, 403, 421–424CrossRefGoogle ScholarPubMed
Bradley, R. L., Titus, B. D. & Preston, C. P. (2000). Changes to mineral N cycling and microbial communities in black spruce humus after additions of (NH4)2SO4 and condensed tannins extracted from Kalmia angustifolia and balsam fir. Soil Biology and Biochemistry, 32, 1227–1240CrossRefGoogle Scholar
Cavigelli, M. A. & Robertson, G. P. (2000). The functional significance of denitrifier community composition in a terrestrial ecosystem. Ecology, 81, 1402–1414CrossRefGoogle Scholar
Cavigelli, M. A. & Robertson, G. P. (2001). Role of denitrifier diversity in rates of nitrous oxide consumption in a terrestrial ecosystem. Soil Biology and Biochemistry, 33, 297–310CrossRefGoogle Scholar
Chapin, F. S. III., Matson, P. & Mooney, H. (2002). Principles of Terrestrial Ecosystem Ecology. New York: Springer-VerlagCrossRef
Chen, J. & Stark, J. (2000). Plant species effects and carbon and nitrogen cycling in a sagebrush–crested wheatgrass soil. Soil Biology and Biochemistry, 32, 47–57CrossRefGoogle Scholar
Cheng, W. (1999). Rhizosphere feedbacks in elevated CO2. Tree Physiology, 19, 313–320CrossRefGoogle Scholar
Coûteaux, M. M., Bottner, P. & Berg, B. (1995). Litter decomposition, climate and litter quality. Trends in Ecology and Evolution, 10, 63–66CrossRefGoogle Scholar
, Dakora F. D. & Phillips, D. A. (2002). Root exudates as mediators of mineral acquisition in low-nutrient environments. Plant and Soil, 245, 35–47Google Scholar
Davidson, E. A., Stark, J. M. & Firestone, M. K. (1990). Microbial production and consumption of nitrate in an annual grassland. Ecology, 71, 1968–1975CrossRefGoogle Scholar
Degens, B. P., Schipper, L. A., Sparling, G. P. & Duncan, L. C. (2001). Is the microbial community in a soil with reduced catabolic diversity less resistant to stress or disturbance?Soil Biology and Biochemistry, 33, 1143–1153CrossRefGoogle Scholar
Dick, W. A. & Tabatabai, M. A. (1993). Significance and potential uses of soil enzymes. Soil Microbial Ecology (Ed. by , F. B. Metting Jr.), pp. 95–127. New York: Marcel Dekker
Field, J. A. & Lettinga, G. (1992). Toxicity of tannin compounds to microorganisms. Plant Polyphenols (Ed. by , R. W. Hemingway & , P. E. Laks), pp. 673–692. New York: Plenum Press
Fierer, N., Schimel, J. P., Cates, R. G. & Zou, J. (2001). The influence of balsam poplar tannin fractions on carbon and nitrogen dynamics in Alaskan taiga floodplain soils. Soil Biology and Biochemistry, 33, 1827–1839CrossRefGoogle Scholar
Fog, K. (1988). The effect of added nitrogen on the rate of decomposition of organic matter. Biological Review, 63, 433–462CrossRefGoogle Scholar
Gamble, G. R., Akin, D. E., Makkar, H. P. S. & Becker, K. (1996). Biological degradation of tannins in Sericea lespedeza (Lespedeza cuneata) by the white rot fungi Ceriporiopsis subvermispora and Cyathus stercoreus analyzed by solid-state 13C nuclear magnetic resonance spectroscopy. Applied and Environmental Microbiology, 62, 3600–3604Google ScholarPubMed
Giblin, A. E., Nadelhoffer, K. J., Shaver, G. R., Laundre, J. A. & McKerrow, A. J. (1991). Biogeochemical diversity along a riverside toposequence in arctic Alaska. Ecological Monographs, 61, 415–435CrossRefGoogle Scholar
Gold, M. H. & Alic, M. (1993). Molecular biology of the lignin-degrading Basidiomycete Phanerochaete chrysosporium. Microbiological Reviews, 57, 605–622Google ScholarPubMed
Gulledge, J. M., Doyle, A. P. & Schimel, J. P. (1997). Different NH4+-inhibition patterns of soil CH4 consumption: a result of distinct CH4 oxidizer populations across sites?Soil Biology and Biochemistry, 29, 13–21CrossRefGoogle Scholar
Harrison, S. P., Jones, D. G., Schunmann, P. H. D., Forster, J. W. & Young, J. P. W. (1988). Variation in Rhizobium leguminosarum Biovar trifolii sym plasmids and the association with effectiveness of nitrogen-fixation. Journal of General Microbiology, 134, 2721–2730Google Scholar
Hart, S. C., Nason, G. E., Myrold, D. D. & Perry, D. A. (1994). Dynamics of gross nitrogen transformations in an old-growth forest: the carbon connection. Ecology, 75, 880–891CrossRefGoogle Scholar
Hart, S. C. & Stark, J. M. (1997). Nitrogen limitation of the microbial biomass in an old-growth forest soil. Ecoscience, 4, 91–98CrossRefGoogle Scholar
Jackson, L. E., Schimel, J. P. & Firestone, M. K. (1989). Short-term partitioning of ammonium and nitrate between plants and microbes in an annual grassland. Soil Biology and Biochemistry, 21, 409–415CrossRefGoogle Scholar
Jaeger, C. I., Lindow, S., Miller, W., Clark, E. & Firestone, M. K. (1999). Mapping of sugar and amino acid availability in soil around roots with bacterial sensors of sucrose and tryptophan. Applied Environmental Microbiology, 65, 2685–2690Google ScholarPubMed
Jingguo, W. & Bakken, L. (1997). Competition for nitrogen during decomposition of plant residues in soil: effect of spatial placement of N-rich and N-poor plant residues. Soil Biology and Biochemistry, 29, 153–162CrossRefGoogle Scholar
Kaal, E. E. J., DeJong, E. & Field, J. A. (1993). Stimulation of ligninolytic peroxidase-activity by nitrogen nutrients in the white-rot fungus Bjerkandera sp. strain BOS55. Applied and Environmental Microbiology, 59, 4031–4036Google ScholarPubMed
Keyser, P., Kirk, T. K. & Zeikus, J. G. (1978). Ligninolytic enzyme system of Phanerochaete chrysosporium: synthesized in absence of lignin in response to nitrogen starvation. Journal of Bacteriology, 135, 790–797Google ScholarPubMed
Kuzyakov, Y. (2002). Review: factors affecting rhizosphere priming effects. Journal of Plant Nutrition and Soil Science, 165, 382–3963.0.CO;2-#>CrossRefGoogle Scholar
Laanbroek, H. J. & Woldendorp, J. W. (1995). Activity of chemolithotrophic nitrifying bacteria under stress in natural soils. Advances in Microbial Ecology, 14, 275–304Google Scholar
Ladd, J. N., Foster, R. C. & Skjemstad, J. O. (1993). Soil structure: carbon and nitrogen metabolism. Geoderma, 56, 401–434CrossRefGoogle Scholar
Martinez-Romero, E. (2001). Dinitrogen-fixing prokaryotes. The Prokaryotes: An Evolving Electronic Resource for the Microbiological Community, 3rd edition, release 3.7, November 2, 2001 (Ed. by , M. Dworkinet al.) New York: Springer-Verlag, www.prokaryotes.com
McCaig, A. E., Phillips, C. J., Stephen, J. R., et al. (1999). Nitrogen cycling and community structure of proteobacterial beta-subgroup ammonia-oxidizing bacteria within polluted marine fish farm sediments. Applied and Environmental Microbiology, 65, 213–220Google ScholarPubMed
Moat, A. G. & Foster, J. W. (1995). Microbial Physiology, 3rd edition. New York: Wiley-LissGoogle Scholar
Nadelhoffer, K. J., Aber, J. D. & Melillo, J. M. (1984). Seasonal patterns of ammonium and nitrate uptake in nine temperate forest ecosystems. Plant and Soil, 80, 321–335CrossRefGoogle Scholar
Neff, J. C., Townsend, A. R., Gleixner, G., et al. (2002). Variable effects of nitrogen additions on the stability and turnover of soil carbon. Nature, 419, 915–917CrossRefGoogle ScholarPubMed
Parkin, T. B. (1987). Soil microsites as a source of denitrification variability. Soil Science Society of America Journal, 51, 1194–1199CrossRefGoogle Scholar
Périé, F. H. & Gold, M. H. (1991). Manganese regulation of manganese peroxidase expression and lignin degradation by the white rot fungus Dichomitus-squalens. Applied and Environmental Microbiology, 57, 2240–2245Google ScholarPubMed
Polglase, P. J., Attiwill, P. M. & Adams, M. A. (1992). Nitrogen and phosphorus cycling in relation to stand age of Eucalyptus regnans F. Muell: II. N mineralization and nitrification. Plant and Soil, 142, 167–176CrossRefGoogle Scholar
Rice, C. W. & Tiedje, J. M. (1989). Regulation of nitrate assimilation by ammonium in soils and in isolated soil-microorganisms. Soil Biology and Biochemistry, 21, 597–602CrossRefGoogle Scholar
Romero, M. D., Aguado, J., González, L. & Ladero, M. (1999). Cellulase production by Neurospora crassa on wheat straw. Enzyme and Microbial Technology, 25, 244–250CrossRefGoogle Scholar
Sarathchandra, S. U., Ghani, A., Yeates, G. W., Burch, G. & Cox, N. R. (2001). Effect of nitrogen and phosphate fertilisers on microbial and nematode diversity in pasture soils. Soil Biology and Biochemistry, 33, 953–964CrossRefGoogle Scholar
Scalbert, A. (1991). Antimicrobial properties of tannins. Phytochemistry, 30, 3875–3883CrossRefGoogle Scholar
Schimel, J. (1995). Ecosystem consequences of microbial diversity and community structure. Arctic and Alpine Biodiversity: Patterns, Causes and Ecosystem Consequences (Ed. by , F. S. Chapin & , C. Korner), pp. 239–254. Berlin: Springer-Verlag
Schimel, J. P. (2001). Biogeochemical models: implicit vs. explicit microbiology. Global Biogeochemical Cycles in the Climate System (Ed. by , E. D. Schulze, , S. P. Harrison, , M. Heimannet al.), pp. 177–183. San Diego, CA: Academic Press
Schimel, J. P. & Bennett, J. (2004). Nitrogen mineralization: challenge of a changing paradigm. Ecology, 85, 591–602CrossRefGoogle Scholar
Schimel, J. P. & Firestone, M. K. (1989). Inorganic nitrogen incorporation by coniferous forest floor material. Soil Biology and Biochemistry, 21, 41–46CrossRefGoogle Scholar
Schimel, J. P. & Weintraub, M. N. (2003). Implications of exoenzyme activity on microbial carbon and nitrogen limitation in soil: a theoretical model. Soil Biology and Biochemistry, 35, 549–563CrossRefGoogle Scholar
Schulz, J. C., Hunter, M. D. & Appel, H. M. (1992). Antimicrobial activity of polyphenols mediates plant–herbivore interactions. Plant Polyphenols (Ed. by , R. W. Hemingway & , P. E. Laks), pp. 621–637. New York: Plenum Press
Sinsabaugh, R. L. (1994). Enzymic analysis of microbial pattern and process. Biology and Fertility of Soils, 17, 69–74CrossRefGoogle Scholar
Sinsabaugh, R. L., Moorhead, D. L. & Linkins, A. E. (1994). The enzymic basis of plant litter decomposition: emergence of an ecological process. Applied Soil Ecology, 1, 97–111CrossRefGoogle Scholar
Stark, J. M. & Firestone, M. K. (1996). Kinetic characteristics of ammonium-oxidizer communities in a California oak woodland–annual grassland. Soil Biology and Biochemistry, 28, 1307–1317CrossRefGoogle Scholar
Stark, J. M. & Hart, S. C. (1997). High rates of nitrification and nitrate turnover in undisturbed coniferous forests. Nature, 385, 61–64CrossRefGoogle Scholar
Sugai, S. F. & Schimel, J. P. (1993). Decomposition and biomass incorporation of 14C-labeled glucose and phenolics in taiga forest floor: effect of substrate quality, successional state, and season. Soil Biology and Biochemistry, 25, 1379–1389CrossRefGoogle Scholar
Tempest, D. W. & Neijssel, O. M. (1992). Physiological and energetic aspects of bacterial metabolite overproduction. FEMS Microbiology Letters, 100, 169–176CrossRefGoogle ScholarPubMed
Umikalsom, M. S., Ariff, A. B., Shamsuddin, Z. H., et al. (1997). Production of cellulase by a wild strain of Chaetomium globosum using delignified oil palm empty-fruit-bunch fibre as substrate. Applied Microbiology and Biotechnology, 47, 590–595CrossRefGoogle Scholar
Wagener, S. M. & Schimel, J. P. (1998). Stratification of soil ecological processes: a study of the birch forest floor in the Alaskan taiga. Oikos, 81, 63–74CrossRefGoogle Scholar
Waksman, S. (1932). Principles of Soil Microbiology, 2nd edition. Baltimore, Md: Williams and WilkinsGoogle Scholar
Waldrop, M. P., Balser, T. C. & Firestone, M. K. (2000). Linking microbial community composition to function in a tropical soil. Soil Biology and Biochemistry, 32, 1837–1846CrossRefGoogle Scholar
Weintraub, M. N. & Schimel, J. P. (2003). Interactions between carbon and nitrogen mineralization and soil organic matter chemistry in Arctic tundra soils. Ecosystems, 6, 129–143CrossRefGoogle Scholar
Wheatley, R. E., Ritz, K., Crabb, D. & Caul, S. (2001). Temporal variations in potential nitrification dynamics in soil related to differences in rates and types of carbon and nitrogen inputs. Soil Biology and Biochemistry, 33, 2135–2144CrossRefGoogle Scholar
Zaman, M., Di, H. J., Cameron, K. C. & Frampton, C. M. (1999). Gross nitrogen mineralization and nitrification rates and their relationships to enzyme activities and the soil microbial biomass in soils treated with dairy shed effluent and ammonium fertilizer at different water potentials. Biology and Fertility of Soils, 29, 178–186CrossRefGoogle Scholar

Save book to Kindle

To save this book to your Kindle, first ensure [email protected] is added to your Approved Personal Document E-mail List under your Personal Document Settings on the Manage Your Content and Devices page of your Amazon account. Then enter the ‘name’ part of your Kindle email address below. Find out more about saving to your Kindle.

Note you can select to save to either the @free.kindle.com or @kindle.com variations. ‘@free.kindle.com’ emails are free but can only be saved to your device when it is connected to wi-fi. ‘@kindle.com’ emails can be delivered even when you are not connected to wi-fi, but note that service fees apply.

Find out more about the Kindle Personal Document Service.

Available formats
×

Save book to Dropbox

To save content items to your account, please confirm that you agree to abide by our usage policies. If this is the first time you use this feature, you will be asked to authorise Cambridge Core to connect with your account. Find out more about saving content to Dropbox.

Available formats
×

Save book to Google Drive

To save content items to your account, please confirm that you agree to abide by our usage policies. If this is the first time you use this feature, you will be asked to authorise Cambridge Core to connect with your account. Find out more about saving content to Google Drive.

Available formats
×