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

Abstract

Microbial 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.

References 50

1. 1.

   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 ).

   Not in our library

2. 2.

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

   Not in our library

3. 3.

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

   Not in our library10.1890/11-0721.1

4. 4.

   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 ).

   Not in our library

5. 5.

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

   Not in our library

6. 6.

   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 ).

   Not in our library

7. 7.

   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 ).

   Not in our library10.1111/j.1469-8137.2012.04225.x

8. 8.

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

   Not in our library10.1155/2013/645983

9. 9.

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

   Not in our library

10. 10.

    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 ).

    Not in our library

11. 11.

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

    Not in our library10.1126/science.1159792

12. 12.

    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 ).

    Not in our library

13. 13.

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

    Not in our library

14. 14.

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

    Not in our library

15. 15.

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

    Not in our library

16. 16.

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

    Not in our library10.1890/06-2057.1

17. 17.

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

    Not in our library10.1016/s0378-1119(02)00558-9

18. 18.

    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 ).

    Not in our library10.1128/ec.5.5.816-824.2006

19. 19.

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

    Not in our library10.1111/j.1461-0248.2006.00919.x

20. 20.

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

    Not in our library

21. 21.

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

    Not in our library

22. 22.

    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 ).

    Not in our library

23. 23.

    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 ).

    Not in our library

24. 24.

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

    Not in our library

25. 25.

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

    Not in our library

26. 26.

    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 ).

    Not in our library10.1021/es071217x

27. 27.

    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 ).

    Not in our library

28. 28.

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

    Not in our library

29. 29.

    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 ).

    Not in our library

30. 30.

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

    Not in our library

31. 31.

    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 ).

    Not in our library

32. 32.

    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 ).

    Not in our library10.1111/ele.12113

33. 33.

    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 ).

    Not in our library

34. 34.

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

    Not in our library10.1038/nrmicro2504

35. 35.

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

    Not in our library

36. 36.

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

    Not in our library10.1890/06-0219

37. 37.

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

    Not in our library10.1016/j.soilbio.2013.08.004

38. 38.

    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 ).

    Not in our library10.1016/j.soilbio.2012.03.012

39. 39.

    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 ).

    Not in our library

40. 40.

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

    Not in our library

41. 41.

    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 ).

    Not in our library

42. 42.

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

    Not in our library

43. 43.

    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 ).

    Not in our library

44. 44.

    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 ).

    Not in our library

45. 45.

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

    Not in our library

46. 46.

    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 ).

    Not in our library

47. 47.

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

    Not in our library

48. 48.

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

    Not in our library

49. 49.

    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 ).

    Not in our library

50. 50.

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

    Not in our library

Cited by papers we hold 5

• Carbon availability mediates the effect of nitrogen on CO2 release from soils · 2022
  Not checked
• Microbial carbon use efficiency predicted from genome-scale metabolic models · 2019
  Not checked
• Proteolytic Activity in Meadow Soil after the Application of Phytohormones · 2019
  Not checked
• Global patterns of phosphatase activity in natural soils · 2017
  No notice
• Driving forces of soil bacterial community structure, diversity, and function in temperate grasslands and forests · 2016
  No notice

Reads

A person counts once a day per paper. We keep no cookie and no address: a reader is a hash that changes every day. Any month under five reads shows no number.