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Stoichiometric responses of soil microflora to nutrient additions for two temperate forest soils

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Abstract

The ratios of soil carbon (C) to nitrogen (N) and C to phosphorus (P) are much higher in Chinese temperate forest soils than in other forest soils, implying that N and P might limit microbial growth and activities. The objective of this study was to assess stoichiometric responses of microbial biomass, enzyme activities, and respiration to N and P additions. We conducted a nutrient (N, P, and N + P) addition experiment in two temperate soils under Korean pine (Pinus koraiensis) plantation and natural broadleaf forest in Northeast China and measured the microbial biomass C, N, P; the activities of β-glucosidase (BG), N-acetyl-β-glucosaminidase (NAG), and acid and alkaline phosphomonoesterase (AP); and the microbial respiration in the two soils. Nitrogen addition increased microbial biomass N and decreased microbial biomass C-to-N ratio and microbial respiration in the two soils. Nitrogen addition decreased NAG activity to microbial biomass N ratio, P addition decreased AP activity to microbial biomass P ratio, and N, P, and N + P additions all increased BG activity to microbial biomass C ratio. These results suggest that microbial stoichiometry is not strictly homeostatic in response to nutrient additions, especially for N addition. The responses of enzyme activities to nutrient additions support the resource allocation theory. The N addition induced a decline in microbial respiration, implying that atmospheric N deposition may reduce microbial respiration, and consequently increase soil C sequestration in the temperate region.

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References

  • Allison SD, Weintraub MN, Gartner TB, Waldrop MP (2010) Evolutionary-economic principles as regulators of soil enzyme production and ecosystem function. In: Shukla G, Varma A (eds) Soil enzymology. Springer, Berlin, pp 229–243

    Chapter  Google Scholar 

  • Blagodatskaya EV, Anderson TH (1998) Interactive effects of pH and substrate quality on the fungal-to-bacterial ratio and qCO2 of microbial communities in forest soils. Soil Biol Biochem 30:1269–1274

    Article  CAS  Google Scholar 

  • Brookes PC, Landman A, Pruden G, Jenkinson DS (1985) Chloroform fumigation and the release of soil nitrogen: a rapid direct extraction method to measure microbial biomass nitrogen in soil. Soil Biol Biochem 17:837–842

    Article  CAS  Google Scholar 

  • Buchkowski RW, Schmitz OJ, Bradford MA (2015) Microbial stoichiometry overrides biomass as a regulator of soil carbon and nitrogen cycling. Ecology 964:1139–1149

    Article  Google Scholar 

  • Chen XW, Li BL (2003) Change in soil carbon and nutrient storage after human disturbance of a primary Korean pine forest in Northeast China. Forest Ecol Manag 186:197–206

    Article  Google Scholar 

  • Chen YL, Chen LY, Peng YF, Ding JZ, Li F, Yang GB, Kou D, Liu L, Fang K, Zhang BB, Wang J, Yang YH (2016) Linking microbial C:N:P stoichiometry to microbial community and abiotic factors along a 3500-km grassland transect on the Tibetan Plateau. Glob Ecol Biogeogr 25:1416–1427

    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 

  • Conrad R (1996) Soil microorganisms as controllers of atmospheric trace gases (H2, CO, CH4, OCS, N2O, and NO). Microbiol Rev 60:609–640

    CAS  PubMed  PubMed Central  Google Scholar 

  • Fanin N, Fromin N, Buatois B, Hättenschwiler S (2013) An experimental test of the hypothesis of non-homeostatic consumer stoichiometry in a plant litter-microbe system. Ecol Lett 16:764–772

    Article  PubMed  Google Scholar 

  • Fierer N, Strickland MS, Liptzin D, Bradford MA, Cleveland CC (2009) Global patterns in belowground communities. Ecol Lett 12:1238–1249

    Article  PubMed  Google Scholar 

  • Fisk M, Santangelo S, Minick K (2015) Carbon mineralization is promoted by phosphorus and reduced by nitrogen addition in the organic horizon of northern hardwood forests. Soil Biol Biochem 81:212–218

    Article  CAS  Google Scholar 

  • Godwin CM, Cotner JB (2015) Aquatic heterotrophic bacteria have highly flexible phosphorus content and biomass stoichiometry. The ISME J 9:2324–2327

    Article  CAS  PubMed  Google Scholar 

  • Hartman WH, Richardson CJ (2013) Differential nutrient limitation of soil microbial biomass and metabolic quotients (qCO2): is there a biological stoichiometry of soil microbes? PLoS One 8:e57127

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • van der Heijden MG, Bardgett RD, van Straalen NM (2008) The unseen majority: soil microbes as drivers of plant diversity and productivity in terrestrial ecosystems. Ecol Lett 11:296–310

    Article  PubMed  Google Scholar 

  • Heuck C, Weig A, Spohn M (2015) Soil microbial biomass C:N:P stoichiometry and microbial use of organic phosphorus. Soil Biol Biochem 85:119–129

    Article  CAS  Google Scholar 

  • Jenkinson DS, Brookes PC, Powlson DS (2004) Measuring soil microbial biomass. Soil Biol Biochem 36:5–7

    Article  CAS  Google Scholar 

  • Kaiser C, Franklin O, Dieckmann U, Richter A (2014) Microbial community dynamics alleviate stoichiometric constraints during litter decay. Ecol Lett 17:680–690

    Article  PubMed  PubMed Central  Google Scholar 

  • Keuskamp JA, Feller IC, Laanbroek HJ, Verhoeven JT, Hefting MM (2015) Short-and long-term effects of nutrient enrichment on microbial exoenzyme activity in mangrove peat. Soil Biol Biochem 81:38–47

    Article  CAS  Google Scholar 

  • Landi L, Renella G, Moreno JL, Falchini L, Nannipieri P (2000) Influence of cadmiuum on the metabolic quotient, L-:D-glutamic acid respiration ratio and enzyme activity: microbial biomass ratio under laboratory conditions. Biol Fertil Soils 32:8–16

    Article  CAS  Google Scholar 

  • Li P, Yang YH, Han WX, Fang JY (2014) Global patterns of soil microbial nitrogen and phosphorus stoichiometry in forest ecosystems. Glob Ecol Biogeogr 23:979–987

    Article  Google Scholar 

  • Li J, Li ZA, Wang FM, Zou B, Chen Y, Zhao J, Mo QF, Li YW, Li XB, Xia HP (2015) Effects of nitrogen and phosphorus addition on soil microbial community in a secondary tropical forest of China. Biol Fertil Soils 51:207–215

    Article  CAS  Google Scholar 

  • Ling N, Sun YM, Ma JH, Guo JH, Zhu P, Peng C, Yu GH, Ran W, Guo SW, Shen QR (2014) Response of the bacterial diversity and soil enzyme activity in particle-size fractions of Mollisol after different fertilization in a long-term experiment. Biol Fertil Soil 50:901–911

    Article  CAS  Google Scholar 

  • Liu LL, Greaver TL (2010) A global perspective on belowground carbon dynamics under nitrogen enrichment. Ecol Lett 13:819–828

    Article  PubMed  Google Scholar 

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

    Article  CAS  PubMed  Google Scholar 

  • Martens DA, Johanson JB, Frankenberger WT Jr (1992) Production and persistence of soil enzymes with repeated addition of organic residues. Soil Sci 153:53–61

    Article  CAS  Google Scholar 

  • McGroddy ME, Daufresne T, Hedin LO (2004) Scaling of C: N: P stoichiometry in forests worldwide: implications of terrestrial Redfield-type ratios. Ecology 85:2390–2401

    Article  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 

  • Mooshammer M, Wanek W, Zechmeister-Boltenstern S, Richter A (2014) Stoichiometric imbalances between terrestrial decomposer communities and their resources: mechanisms and implications of microbial adaptations to their resources. Front Microbiol 5:22

    Article  PubMed  PubMed Central  Google Scholar 

  • Nannipieri P, Ascher J, Ceccherini MT, Landi L, Pietramellara G, Renella G (2003) Microbial diversity and soil functions. Eur J Soil Sci 54:655–670

    Article  Google Scholar 

  • Nannipieri P, Giagnoni L, Landi L, Renella G (2011) Role of phosphatase enzymes in soil. In: Bunemann EK, Obreson A, Frossard E (eds) Phosphorus in action. Springer, Berlin, pp 215–243

    Chapter  Google Scholar 

  • Nannipieri P, Giagnoni 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 

  • Nguyen TT, Marschner P (2016) Soil respiration, microbial biomass and nutrient availability in soil after repeated addition of low and high C/N plant residues. Biol Fertil Soils 52:165–176

    Article  CAS  Google Scholar 

  • Ramirez KS, Craine JM, Fierer N (2012) Consistent effects of nitrogen amendments on soil microbial communities and processes across biomes. Glob Chang Biol 18:1918–1927

    Article  Google Scholar 

  • Reed SC, Vitousek PM, Cleveland CC (2011) Are patterns in nutrient limitation belowground consistent with those aboveground: results from a 4 million year chronosequence. Biogeochemistry 106:323–336

    Article  CAS  Google Scholar 

  • Sakamoto K, Oba Y (1994) Effect of fungal to bacterial biomass on the relationship between CO2 evolution and total soil microbial biomass. Biol Fertil Soils 17:39–44

    Article  Google Scholar 

  • Schimel JP, Weintraub MN (2003) The implications of exoenzyme activity on microbial carbon and nitrogen limitation in soil: a theoretical model. Soil Biol Biochem 35:549–563

    Article  CAS  Google Scholar 

  • Sinsabaugh R, Follstad Shah JJ (2012) Ecoenzymatic stoichiometry and ecological theory. Annu Rev Ecol Evol S 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, 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 

  • Spohn M (2015) Microbial respiration per unit microbial biomass depends on litter layer carbon-to-nitrogen ratio. Biogeosciences 12:817–823

    Article  Google Scholar 

  • Spohn M, Chodak M (2015) Microbial respiration per unit biomass increases with carbon-to-nutrient ratios in forest soils. Soil Biol Biochem 81:128–133

    Article  CAS  Google Scholar 

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

    Google Scholar 

  • Tian HQ, Chen GS, Zhang C, Melillo JM, Hall CA (2010) Pattern and variation of C: N: P ratios in China’s soils: a synthesis of observational data. Biogeochemistry 98:139–151

    Article  CAS  Google Scholar 

  • Tian JH, Wei K, Condron LM, Chen ZH, Xu ZW, Chen LJ (2016) Impact of land use and nutrient addition on phosphatase activities and their relationships with organic phosphorus turnover in semi-arid grassland soils. Biol Fertil Soils 52:675–683

    Article  CAS  Google Scholar 

  • Treseder KK (2008) Nitrogen additions and microbial biomass: a meta-analysis of ecosystem studies. Ecol Lett 11:1111–1120

    Article  PubMed  Google Scholar 

  • Wang CK, Han Y, Chen JQ, Wang XC, Zhang QZ, Bond-Lamberty B (2013) Seasonality of soil CO2 efflux in a temperate forest: biophysical effects of snowpack and spring freeze-thaw cycles. Agric For Meteorol 177:83–92

    Article  Google Scholar 

  • Waring BG, Weintraub SR, Sinsabaugh RL (2014) Ecoenzymatic stoichiometry of microbial nutrient acquisition in tropical soils. Biogeochemistry 117:101–113

    Article  CAS  Google Scholar 

  • Warton DI, Wright IJ, Falster DS, Westoby M (2006) Bivariate line-fitting methods for allometry. Biol Rev 81:259–291

    Article  PubMed  Google Scholar 

  • Weedon JT, Cornwell WK, Cornelissen JHC, Zanne AE, Wirth C, Coomes DA (2009) Global meta analysis of wood decomposition rates: a role for trait variation among tree species? Ecol Lett 12:45–56

    Article  PubMed  Google Scholar 

  • Xu XF, Thornton PE, Post WM (2013) A global analysis of soil microbial biomass carbon, nitrogen and phosphorus in terrestrial ecosystems. Glob Ecol Biogeogr 22:737–749

    Article  Google Scholar 

  • Yuan ZY, Chen HYH, Reich PB (2011) Global scale latitudinal patterns of plant fine-root nitrogen and phosphorus. Nat Commun 2:344

    Article  CAS  PubMed  Google Scholar 

  • Zechmeister-Boltenstern 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 

  • Zhong Y, Yan W, Shangguan Z (2015) Impact of long-term N additions upon coupling between soil microbial community structure and activity, and nutrient-use efficiencies. Soil Biol Biochem 91:151–159

    Article  CAS  Google Scholar 

  • Zhou ZH, Wang CK (2015) Reviews and syntheses: soil resources and climate jointly drive variations in microbial biomass carbon and nitrogen in China's forest ecosystems. Biogeosciences 12:6751–6760

    Article  Google Scholar 

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Acknowledgments

We thank Dr. Paolo Nannipieri and two anonymous reviewers for their constructive comments, Taidong Zhang for his field assistance, and the Maoershan Forest Ecosystem Research Station for field logistic support. This work was financially supported by the National Key Research and Development Program of China (2016YFD0600201) and the Program for Changjiang Scholars and Innovative Research Team in University (IRT_15R09) to C.K. Wang and the Fundamental Research Funds for the Central Universities (2572016AA08) to Z.H. Zhou.

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Correspondence to Chuankuan Wang.

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Zhou, Z., Wang, C. & Jin, Y. Stoichiometric responses of soil microflora to nutrient additions for two temperate forest soils. Biol Fertil Soils 53, 397–406 (2017). https://doi.org/10.1007/s00374-017-1188-y

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  • DOI: https://doi.org/10.1007/s00374-017-1188-y

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