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The nutrient release rate accounts for the effect of organic matter type on soil microbial carbon use efficiency of a Pinus tabulaeformis forest in northern China

  • Soils, Sec 3 • Remediation and Management of Contaminated or Degraded Lands • Research Article
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Abstract

Purpose

Microbial carbon use efficiency (CUE) greatly controls the magnitude of soil organic carbon turnover. This study was conducted to estimate the CUE with the additions of different organic matter (OM) to the top soil of a Pinus tabulaeformis forest and explore the variations of CUE and ecoenzyme activity with the quality of the added OM.

Materials and methods

Five types of OM, i.e., P. tabulaeformis leaves, Quercus wutaishanica leaves, maize straw, biochar, and wood, were separately crushed by a machine and then manually mixed in the top 20 cm of soil in a plot at 5 × 5 m in June 2014. Concurrently, 20 g of each OM larger than 1 cm was put in a nylon bag of 10 × 15 cm and placed above the plot ground to monitor the OM decomposition. The soil samples were taken and analyzed for the physicochemical properties, the extracellular enzyme activity, and soil microbial biomass, and the OM decomposition rate was also measured in August 2017.

Results and discussion

The OM in the litter bag absorbed nitrogen from the soil particle during the decomposition period, and the nitrogen release rates of wood debris and maize straw were significantly lower at − 625.01% and − 276.98%. The carbon targeting enzyme, i.e., α-1,4-glucosidase (AG), was also influenced by the OM addition and changed from 5.39 nmol h−1 g−1 with the Q. wutaishanica leaf addition to 14.82 nmol h−1 g−1 with the wood debris addition. Significant differences were simultaneously detected in the soil microbial biomass carbon content among different OM additions. These changes in soil biophysical properties contributed to much of the variation in CUEC:N. The CUEC:N meaning the microbial carbon assimilation at the cost of nitrogen was highest at 0.221 for wood debris addition.

Conclusions

The addition of OM differing in quality could influence the soil resource content, exo-enzyme activity, and soil microbial biomass through its nutrient release rate. The CUEC:N could act as an integrative proxy of soil biophysical properties because it also correlated with the soil nutrient content, ecoenzymatic stoichiometry and the OM nutrient release rate. The high CUEC:N value indicated a big carbon stabilization in soils with wood debris addition.

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References

  • Ågren GI, Bosatta E, Magill AH (2001) Combining theory and experiment to understand effects of inorganic nitrogen on litter decomposition. Oecologia 128:94–98

    Article  Google Scholar 

  • Allen AP, Gillooly JF (2009) Towards an integration of ecological stoichiometry and the metabolic theory of ecology to better understand nutrient cycling. Ecol Lett 12:369–384

    Article  Google Scholar 

  • Bao SD (2007) Soil agro-chemistrical analysis. China Agriculture Press, Beijing (in Chinese)

    Google Scholar 

  • Bradford MA, Crowther TW (2013) Carbon use efficiency and storage in terrestrial ecosystems. New Phytol 199:7–9

    Article  CAS  Google Scholar 

  • Chen R, Senbayram M, Blagodatsky S, Myachina O, Dittert K, Lin X, Blagodatskaya E, Kuzyakov Y (2014) Soil C and N availability determine the priming effect: microbial N mining and stoichiometric decomposition theories. Glob Chang Biol 20:2356–2367

    Article  Google Scholar 

  • Cleveland CC, Liptzin D (2007) C:N:P stoichiometry in soil: is there a “Redfield ratio” for the microbial biomass? Biogeochemistry 85:235–252

    Article  Google Scholar 

  • Eivazi F, Tabatabai MA (1977) Phosphatases in soils. Soil Biol Biochem 9:167–172

    Article  CAS  Google Scholar 

  • Fierer N, Craine JM, Mclauchlan K, Schimel JP (2005) Litter quality and the temperature sensitivity of decomposition. Ecology 86:320–326

    Article  Google Scholar 

  • Gallaher RN, Weldon CO, Boswell FC (1976) A semiautomated procedure for total nitrogen in plant and soil samples. Soil Sci Soc Am J 40:887–889

    Article  CAS  Google Scholar 

  • German DP, Weintraub MN, Grandy AS, Lauber CL, RInkes ZL, Allison SD (2011) Optimization of hydrolytic and oxidative enzyme methods for ecosystem studies. Soil Biol Biochem 43:1387–1397

    Article  CAS  Google Scholar 

  • Guo J, Wang W, Cao X, Wang Z, Lu B (1992) A study on forest soil groups of Taiyue mountain. J Beijing Forest Univ 14:134–142 (in Chinese with English abstract)

    Google Scholar 

  • Hättenschwiler S, Jørgensen HB (2010) Carbon quality rather than stoichiometry controls litter decomposition in a tropical rain forest. J Ecol 98:754–763

    Article  Google Scholar 

  • Hatton P, Castanha C, Torn MS, Bird JA (2015) Litter type control on soil C and N stabilization dynamics in a temperate forest. Glob Chang Biol 21:1358–1367

    Article  Google Scholar 

  • Jian S, Li J, Chen J, Wang G, Mayes MA, Dzantor KE, Hui D, Luo Y (2016) Soil extracellular enzyme activities, soil carbon and nitrogen storage under nitrogen fertilization: a meta-analysis. Soil Biol Biochem 101:32–43

    Article  CAS  Google Scholar 

  • Jing X, Chen X, Tang M, Ding Z, Jiang L, Li P, Ma S, Tian D, Xu L, Zhu J, Ji C, Shen H, Zheng C, Fang J, Zhu B (2017) Nitrogen deposition has minor effect on soil extracellular enzyme activities in six Chinese forests. Sci Total Environ 607-608:806–815

    Article  CAS  Google Scholar 

  • Keiblinger KM, Hall EK, Wanek W, Szukics U, Hämmerle I, Ellersdorfer G, Böck S, Strauss J, Sterflinger K, Richter A, Zechmeister-Boltenstern S (2010) The effect of resource quantity and resource stoichiometry on microbial carbon-use-efficiency. FEMS Microbiol Ecol 73:430–440

    CAS  Google Scholar 

  • Li H, Yu G, Li J, Chen Y, Liang T (2007a) Decomposition dynamics and nutrient release of litters for four artificial forests in the red soil and hilly region of subtropical China. Acta Ecol Sin 27:898–908 (in Chinese with English abstract)

    CAS  Google Scholar 

  • Li H, Yu G, Li J, Liang T, Chen Y (2007b) Dynamics of litter decomposition and phosphorus and potassium release in Jinggang Mountain region of Jiangxi Province, China. Chin J Appl Ecol 18:233–240 (in Chinese with English abstract)

    Google Scholar 

  • Loeppmann S, Blagodatskaya E, Pausch J (2016) Substrate quality affects kinetic and catalytic efficiency of exo-enzymes in rhizosphere and detritusphere. Soil Biol Biochem 92:111–118

    Article  CAS  Google Scholar 

  • Manzoni S, Jackson RB, Trofymow JA, Porporato A (2008) The global stoichiometry of litter nitrogen mineralization. Science 321:684–686

    Article  CAS  Google Scholar 

  • Manzoni S, Taylor P, Richter A, Porporato A, Ǻgren GI (2012) Environmental and stoichiometric controls on microbial carbon-use efficiency in soils. New Phytol 196:79–91

    Article  CAS  Google Scholar 

  • Moorhead DL, Sinsabaugh RL, Hill BH, Weintraub MN (2016) Vector analysis of ecoenzyme activities reveal constraints on coupled C, N and P dynamics. Soil Biol Biochem 93:1–7

    Article  CAS  Google Scholar 

  • Nannipieri P, Glagnoni L, Renella G, Puglisi E, Ceccanti B, Masciandaro G, Fornasier F, Moscatelli MC, Marinari S (2012) Soil enzymology: classical and molecular approaches. Biol Fertil Soils 48:743–762

    Article  Google Scholar 

  • Nelson DW, Sommers LE (1982) Methods of soil analysis. In: Miller RH, Keeney DR (ed) Total carbon, organic carbon, and organic matter. Agronomy Series No 9, ASA SSSA, Madison, pp 101–129

  • Ng EL, Patti AF, Rose MT, Schefe CR, Wilkinson K, Cavagnaro TR (2014) Functional stoichiometry of soil microbial communities after amendment with stabilized organic matter. Soil Biol Biochem 76:170–178

    Article  CAS  Google Scholar 

  • Sinsabaugh RL (1994) Enzymatic analysis of microbial pattern and process. Biol Fertil Soils 17:69–74

    Article  CAS  Google Scholar 

  • Sinsabaugh RL, Follsatd Shah JJ (2012) Ecoenzymatic stoichiometry and ecological theory. Annu Rev Ecol Syst 43:313–343

    Article  Google Scholar 

  • Sinsabaugh RL, Moorhead DL (1994) Resource allocation to extracellular enzyme production: a model for nitrogen and phosphorus control of litter decomposition. Soil Biol Biochem 26:1305–1311

    Article  Google Scholar 

  • Sinsabaugh RL, Findlay S, Franchini P, Fischer D (1997) Enzyme analysis of riverine bacterioplankton production. Limnol Oceanogr 42:29–38

    Article  CAS  Google Scholar 

  • Sinsabaugh RL, Lauber CL, Weintraub MN, Ahmed B, Allison SD, Crenshaw C, Contosta AR, Cusack D, Frey S, Gallo ME, Gartner TB, Hobbie SE, Holland K, Keeler BL, Powers JS, Stursova M, Takacs-Vesbach C, Waldrop MP, Wallenstein MD, Zak DR, Zeglin LH (2008) Stoichiometry of soil enzyme activity at global scale. Ecol Lett 11:1252–1264

    Article  Google Scholar 

  • Sinsabaugh RL, Hill BH, Follsatd Shah JJ (2009) Ecoenzymatic stoichiometry of microbial organic nutrient acquisition in soil and sediment. Nature 462:795–798

    Article  CAS  Google Scholar 

  • Sinsabaugh RL, Manoni S, Moorhead DL, Richter A (2013) Carbon use efficiency of microbial communities: stoichiometry, methodology and modeling. Ecol Lett 16:930–939

    Article  Google Scholar 

  • Sinsabaugh RL, Belnap J, Findlay SG, Follstad Shah JJ, Hill BH, Kuehn KA, Kuske CR, Litvak ME, Martinez NG, Moorhead DL, Warnock DD (2014) Extracellular enzyme kinetics scale with resource availability. Biogeochemistry 121:287–304

    Article  CAS  Google Scholar 

  • Sinsabaugh RL, Turner BL, Talbot JM, Waring BG, Powers JS, Kuske CR, Moorhead DL, Follstad Shah JJ (2016) Stoichiometry of microbial carbon use efficiency in soils. Ecol Monogr 86:172–189

    Article  Google Scholar 

  • Sterner RW, Elser JJ (2002) Ecological stoichiometry: the biology and elements from molecules to the biosphere. Princeton University, Princeton

    Google Scholar 

  • Takriti M, Wild B, Schnecker J, Mooshammer M, Knoltsch A, Lashchinskiy N, Alves RJE, Gentsch N, Gittel A, Mikutta R, Wanek W, Richter A (2018) Soil organic matter quality exerts a stronger control than stoichiometry on microbial substrate use efficiency along a latitudinal transect. Soil Biol Biochem 121:212–220

    Article  CAS  Google Scholar 

  • Vance ED, Brookes PC, Jenkinson DS (1987) An extraction method for measuring soil microbial biomass C. Soil Biol Biochem 19:703–707

    Article  CAS  Google Scholar 

  • Xu Z, Yu G, Zhang X, He N, Wang Q, Wang S, Wang R, Zhao N, Jia Y, Wang C (2017) Soil enzyme activity and stoichiometry in forest ecosystems along the North-South Transect in eastern China (NSTEC). Soil Biol Biochem 104:152–163

    Article  CAS  Google Scholar 

  • Yu J, Deem LM, Crow SE, Deenik JL, Penton CR (2018) Biochar application influences microbial assemblage complexity and composition due to soil and bioenergy crop type interactions. Soil Biol Biochem 117:97–107

    Article  CAS  Google Scholar 

  • Zechmeister-Boltnstern S, Keiblinger KM, Mooshammer M, Peñuelas J, Richter A, Sardans J, Wanek W (2015) The application of ecological stoichiometry to plant-microbial-soil organic matter transformations. Ecol Monogr 85:133–155

    Article  Google Scholar 

  • Zhou Z, Xu M, Kang F, Sun OJ (2015) Maximum temperature accounts for annual soil CO2 efflux in temperate forests of Northern China. Sci Rep 5:12142. https://doi.org/10.1038/srep12142

    Article  CAS  Google Scholar 

Download references

Acknowledgments

We would like to thank Bo Wang, Jiawei Shi, Yu Wang, Weicheng Sun, and Qinyang Lv for their intensive assistance with the field investigation and the laboratory analyses. We appreciate two anonymous reviewers for their effort and inspiring comments.

Funding

The financial support for this research was jointly provided by the National Key Research and Development Program of the Ministry of Science and Technology of China (No. 2016YFD0600205), the Fundamental Research Funds for the Central Universities (No. 2015ZCQ-LX-03), and the Normal Research Funds for Taiyueshan Long Term Forest Ecosystem Research Station (No. 2017-, 2018-LYPT-DW-153).

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Authors and Affiliations

  1. Key Laboratory for Forest Resources & Ecosystem Process of Beijing, the College of Forestry, Beijing Forestry University, Beijing, People’s Republic of China

    Zhiyong Zhou, Huan Zhang, Zhen Yuan & Runing Gong

  2. Taiyueshan Long-Term Forest Ecosystem Research Station, Shanxi Province, People’s Republic of China

    Zhiyong Zhou

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  1. Zhiyong Zhou
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  2. Huan Zhang
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Correspondence to Zhiyong Zhou.

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Responsible editor: Jianming Xue

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Zhou, Z., Zhang, H., Yuan, Z. et al. The nutrient release rate accounts for the effect of organic matter type on soil microbial carbon use efficiency of a Pinus tabulaeformis forest in northern China. J Soils Sediments 20, 352–364 (2020). https://doi.org/10.1007/s11368-019-02423-2

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