Adjustment of microbial nitrogen use efficiency to carbon:nitrogen imbalances regulates soil nitrogen cycling

Nature Communications - Tập 5 Số 1
Maria Mooshammer1, Wolfgang Wanek1, Ieda Hämmerle1, Lucia Fuchslueger1, Florian Hofhansl1, Anna Knoltsch1, Jörg Schnecker1, Mounir Takriti1, Margarete Watzka1, Birgit Wild1, Katharina Keiblinger2, Sophie Zechmeister‐Boltenstern2, Andreas Richter1
1Department of Microbiology and Ecosystem Science, Terrestrial Ecosystem Research, University of Vienna, Althanstrasse 14, 1090 Vienna, Austria.
2Department of Forest and Soil Sciences, Institute of Soil Research, University of Natural Resources and Life Sciences, Peter-Jordan-Strasse 82, 1190 Vienna, Austria.

Tóm tắt

AbstractMicrobial nitrogen use efficiency (NUE) describes the partitioning of organic N taken up between growth and the release of inorganic N to the environment (that is, N mineralization), and is thus central to our understanding of N cycling. Here we report empirical evidence that microbial decomposer communities in soil and plant litter regulate their NUE. We find that microbes retain most immobilized organic N (high NUE), when they are N limited, resulting in low N mineralization. However, when the metabolic control of microbial decomposers switches from N to C limitation, they release an increasing fraction of organic N as ammonium (low NUE). We conclude that the regulation of NUE is an essential strategy of microbial communities to cope with resource imbalances, independent of the regulation of microbial carbon use efficiency, with significant effects on terrestrial N cycling.

Từ khóa


Tài liệu tham khảo

Jan, M. T., Roberts, P., Tonheim, S. K. & Jones, D. L. Protein breakdown represents a major bottleneck in nitrogen cycling in grassland soils. Soil Biol. Biochem. 41, 2272–2282 (2009).

Schimel, J. P. & Bennett, J. Nitrogen mineralization: challenges of a changing paradigm. Ecology 85, 591–602 (2004).

Mooshammer, M. et al. Stoichiometric controls of nitrogen and phosphorus cycling in decomposing beech leaf litter. Ecology 93, 770–782 (2012).

Jones, D. L., Farrar, J. F. & Newsham, K. K. Rapid amino acid cycling in Arctic and Antarctic soils. Water Air Soil Poll. 4, 169–175 (2004).

Jones, D. L. et al. Soil organic nitrogen mineralization across a global latitudinal gradient. Global Biogeochem. Cycles 23, GB1016 (2009).

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. 70, 555–569 (2006).

Manzoni, S., Taylor, P., Richter, A., Porporato, A. & Ågren, G. I. Environmental and stoichiometric controls on microbial carbon-use efficiency in soils. New Phytol. 196, 79–91 (2012).

Shimizu, K. Metabolic regulation of a bacterial cell system with emphasis on Escherichia coli metabolism. ISRN Biochem. 2013, 645983 (2013).

Allison, S. D., Wallenstein, M. D. & Bradford, M. A. Soil-carbon response to warming dependent on microbial physiology. Nat. Geosci. 3, 336–340 (2010).

Herron, P. M., Stark, J. M., Holt, C., Hooker, T. & Cardon, Z. G. Microbial growth efficiencies across a soil moisture gradient assessed using C-13-acetic acid vapor and N-15-ammonia gas. Soil Biol. Biochem. 41, 1262–1269 (2009).

Manzoni, S., Jackson, R. B., Trofymow, J. A. & Porporato, A. The global stoichiometry of litter nitrogen mineralization. Science 321, 684–686 (2008).

Manzoni, S., Trofymow, J. A., Jackson, R. B. & Porporato, A. Stoichiometric controls on carbon, nitrogen, and phosphorus dynamics in decomposing litter. Ecol. Monogr. 80, 89–106 (2010).

del Giorgio, P. A. & Cole, J. J. Bacterial growth efficiency in natural aquatic systems. Annu. Rev. Ecol. Syst. 29, 503–541 (1998).

Sterner, R. W. & Elser, J. J. Ecological Stoichiometry: The Biology of Elements from Molecules to the Biosphere Princton Univ. Press (2002).

Manzoni, S. & Porporato, A. Soil carbon and nitrogen mineralization: Theory and models across scales. Soil Biol. Biochem. 41, 1355–1379 (2009).

LeBauer, D. S. & Treseder, K. K. Nitrogen limitation of net primary productivity in terrestrial ecosystems is globally distributed. Ecology 89, 371–379 (2008).

Magasanik, B. & Kaiser, C. A. Nitrogen regulation in Saccharomyces cerevisiae. Gene 290, 1–18 (2002).

Kingsbury, J. M., Goldstein, A. L. & McCusker, J. H. Role of nitrogen and carbon transport, regulation, and metabolism genes for Saccharomyces cerevisiae survival in vivo. Eukaryot. Cell. 5, 816–824 (2006).

Frost, P. C. et al. Threshold elemental ratios of carbon and phosphorus in aquatic consumers. Ecol. Lett. 9, 774–779 (2006).

Urabe, J. & Watanabe, Y. Possibility of N or P limitation for planktonic cladocerans: An experimental test. Limnol. Oceanogr. 37, 244–251 (1992).

Anderson, T. R. & Hessen, D. O. Carbon or nitrogen limitation in marine copepods? J. Plankton Res. 17, 317–331 (1995).

Xu, X., Thornton, P. E. & Post, W. M. A global analysis of soil microbial biomass carbon, nitrogen and phosphorus in terrestrial ecosystems. Glob. Ecol. Biogeogr. 22, 737–749 (2013).

Persson, J. et al. To be or not to be what you eat: regulation of stoichiometric homeostasis among autotrophs and heterotrophs. Oikos 119, 741–751 (2010).

Hedin, L. O., Vitousek, P. M. & Matson, P. A. Nutrient losses over four million years of tropical forest development. Ecology 84, 2231–2255 (2003).

Miltner, A., Bombach, P., Schmidt-Brucken, B. & Kastner, M. SOM genesis: microbial biomass as a significant source. Biogeochemistry 111, 41–55 (2012).

Simpson, A. J., Simpson, M. J., Smith, E. & Kelleher, B. P. Microbially derived inputs to soil organic matter: Are current estimates too low? Environ. Sci. Technol. 41, 8070–8076 (2007).

McGroddy, M. E., Daufresne, T. & Hedin, L. O. Scaling of C:N:P stoichiometry in forests worldwide: Implications of terrestrial redfield-type ratios. Ecology 85, 2390–2401 (2004).

Yuan, Z. Y. Y. & Chen, H. Y. H. Global trends in senesced-leaf nitrogen and phosphorus. Glob. Ecol. Biogeogr. 18, 532–542 (2009).

Cleveland, C. C. & Liptzin, D. C:N:P stoichiometry in soil: is there a ‘Redfield ratio’ for the microbial biomass? Biogeochemistry 85, 235–252 (2007).

Berg, B. & McClaugherty, C. Plant litter: Decomposition, Humus Formation, Carbon Sequestration Springer (2003).

Devêvre, O. C. & Horwáth, W. R. Decomposition of rice straw and microbial carbon use efficiency under different soil temperatures and moistures. Soil Biol. Biochem. 32, 1773–1785 (2000).

Sinsabaugh, R. L., Manzoni, S., Moorhead, D. L. & Richter, A. Carbon use efficiency of microbial communities: stoichiometry, methodology and modelling. Ecol. Lett. 16, 930–939 (2013).

Schimel, J. P. & Weintraub, M. N. The implications of exoenzyme activity on microbial carbon and nitrogen limitation in soil: a theoretical model. Soil Biol. Biochem. 35, 549–563 (2003).

Lennon, J. T. & Jones, S. E. Microbial seed banks: the ecological and evolutionary implications of dormancy. Nat. Rev. Microbiol. 9, 119–130 (2011).

Blagodatskaya, E. & Kuzyakov, Y. Active microorganisms in soil: critical review of estimation criteria and approaches. Soil Biol. Biochem. 67, 192–211 (2013).

Schimel, J., Balser, T. C. & Wallenstein, M. Microbial stress-response physiology and its implications for ecosystem function. Ecology 88, 1386–1394 (2007).

Wild, B. et al. Nitrogen dynamics in turbic cryosols from Siberia and Greenland. Soil Biol. Biochem. 67, 85–93 (2013).

Leitner, S. et al. Influence of litter chemistry and stoichiometry on glucan depolymerization during decomposition of beech (Fagus sylvatica L.) litter. Soil Biol. Biochem. 50, 174–187 (2012).

Wanek, W., Mooshammer, M., Blöchl, A., Hanreich, A. & Richter, A. Determination of gross rates of amino acid production and immobilization in decomposing leaf litter by a novel N-15 isotope pool dilution technique. Soil Biol. Biochem. 42, 1293–1302 (2010).

Öhlinger, R. In:Methods in Soil Biology eds Schinner F., Kandeler E., Öhlinger R., Margsin R. 58–60Springer (1996).

Hood-Nowotny, R., Hinko-Najera, U. N., Inselbacher, E., Oswald-Lachouani, P. & Wanek, W. Alternative methods for measuring inorganic, organic, and total dissolved nitrogen in soil. Soil Sci. Soc. Am. J 74, 1018–1027 (2010).

Schulten, H. R. & Schnitzer, M. The chemistry of soil organic nitrogen: a review. Biol. Fertil. Soils 26, 1–15 (1998).

Kelleher, B. P., Simpson, M. J. & Simpson, A. J. Assessing the fate and transformation of plant residues in the terrestrial environment using HR-MAS NMR spectroscopy. Geochim. Cosmochim. Acta 70, 4080–4094 (2006).

Jones, D. L., Healey, J. R., Willett, V. B., Farrar, J. F. & Hodge, A. Dissolved organic nitrogen uptake by plants—an important N uptake pathway? Soil Biol. Biochem. 37, 413–423 (2005).

Kielland, K., McFarland, J. W., Ruess, R. W. & Olson, K. Rapid cycling of organic nitrogen in taiga forest ecosystems. Ecosystems 10, 360–368 (2007).

Sorensen, P. & Jensen, E. S. Sequential diffusion of ammonium and nitrate from soil extracts to a polytetrafluoroethylene trap for 15N determination. Anal. Chim. Acta 252, 201–203 (1991).

Breiman, L., Friedman, J., Olshen, R. & Stone, C. Classification and Regression Trees Wadsworth (1984).

Toms, J. D. & Lesperance, M. L. Piecewise regression: a tool for identifying ecological thresholds. Ecology 84, 2034–2041 (2003).

R Core Team. R: a language and environment for statistical computing. R Foundation for Statistical Computing, Vienna, Austria. ISBN 3-900051-07-0, http://www.R-project.org (2012).

Therneau, T. M., Atkinson, B. & Ripley, B. rpart: recursive partitioning. version 3.1–48, http://www.CRAN.R-project.org/package=rpart (2010).