Effects of nitrogen addition on DOM-induced soil priming effects in a subtropical plantation forest and a natural forest

  • Yuexin Fan
  • Xiaojian Zhong
  • Teng-Chiu Lin
  • Maokui Lyu
  • Minhuang Wang
  • Weifang Hu
  • Zhijie Yang
  • Guangshui Chen
  • Jianfen GuoEmail author
  • Yusheng YangEmail author
Original Paper


Dissolved organic matter (DOM) plays a key role in soil organic matter (SOM) decomposition via the priming effect (PE). The DOM-induced soil PE is closely related to nutrient availability, especially nitrogen (N). Regardless of the widespread of chronic N addition, how elevated N deposition affects DOM-induced PEs remains poorly understood. To fill this knowledge gap, we studied the effects of N addition, 13C-labeled leaf-DOM (herein DOM) addition, and leaf-DOM plus N addition (DOM+N) on soil PEs in soils of a subtropical Chinese-fir (Cunninghamia lanceolata) plantation and a natural Castanopsis carlesii forest (hereafter referred to as Chinese-fir soil and Castanopsis soil, respectively). Soil properties (e.g., soil organic C, total N, available phosphorus, and ratio of C and N), dissolved organic C (DOC), soil microbial biomass C (MBC), phospholipid fatty acid (PLFA), and enzyme activities were also investigated, because these parameters predominantly affect the intensity and direction of soil priming. The addition of DOM induced positive PEs in the Castanopsis soil but negative PEs in the Chinese-fir soil. In addition, DOM addition increased MBC and fungal abundance and the activities of phenol oxidase (PhOx) and peroxidase (Perox) in the Castanopsis soil but not in the Chinese-fir soil. Compared with DOM-only addition, DOM+N addition significantly enhanced PEs in the Chinese-fir soil but not in the Castanopsis soil. Furthermore, compared with DOM-only addition, DOM+N addition significantly increased MBC, abundance of fungi and AMF, fungi to bacteria ratio (F:B), and activities of four enzymes [β-glucosidase (βG), N-acetyl glucosaminidase (NAG), PhOx, and Perox] in the Chinese-fir soil but not in the Castanopsis soil. The DOM+N addition also had a significant effect on composition of main microbial groups in the Chinese-fir soil but not in the Castanopsis soil. These results suggest the enhanced PE following DOM+N in the Chinese-fir soil was likely mediated by enhanced enzyme production associated with increased fungal abundance. Our study highlights that the effects of increases of DOM on soil C cycling is largely affected by N availability and mediated by the effects on the abundance of soil microbial groups and enzyme activities. Our result also demonstrated a case in which effects of DOM and N addition on soil C cycling differ between a Castanopsis forest and a Chinese-fir plantation forest, with Chinese-fir soil being more sensitive to N addition. This is an important finding that needs to be taken into consideration in estimating the soil C pools.


Enzyme activities Fungi Phospholipid fatty acid Microbial biomass carbon Dissolved organic carbon 



We are grateful to Prof Paolo Nannipieri and the three anonymous reviewers for their valuable comments and suggestions. We also thank Chengfang Lin, Xiaofei Liu, Decheng Xiong, Chao Xu, and Zheng Zhang for field sampling and chemical analysis.

Funding information

This research was supported by Joint Fund for Promotion of Cross-strait Cooperation in Science and Technology (U1505233), the National Basic Research Program of China (973 Program) (No. 2014CB954003), and National Natural Science Foundation of China (No. 31830014, 41977090, and 31370615).

Supplementary material

374_2019_1416_MOESM1_ESM.docx (90 kb)
ESM 1 (DOCX 90 kb)


  1. Blagodatskaya Е, Kuzyakov Y (2008) Mechanisms of real and apparent priming effects and their dependence on soil microbial biomass and community structure: critical review. Biol Fertil Soils 45:115–131CrossRefGoogle Scholar
  2. Boot CM, Hall EK, Denef K, Baron JS (2016) Long-term reactive nitrogen loading alters soil carbon and microbial community properties in a subalpine forest ecosystem. Soil Biol Biochem 92:211–220CrossRefGoogle Scholar
  3. Carreiro M, Sinsabaugh R, Repert D, Parkhurst D (2000) Microbial enzyme shifts explain litter decay responses to simulated nitrogen deposition. Ecology 81:2359–2365CrossRefGoogle Scholar
  4. 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 20:2356–2367PubMedCrossRefGoogle Scholar
  5. Chen Y, Chen G, Robinson D, Yang Z, Guo J, Xie J, Fu S, Zhou L, Yang Y (2016) Large amounts of easily decomposable carbon stored in subtropical forest subsoil are associated with r-strategy-dominated soil microbes. Soil Biol Biochem 95:233–242CrossRefGoogle Scholar
  6. Cleveland CC, Nemergut DR, Schmidt SK, Townsend AR (2007) Increases in soil respiration following labile carbon additions linked to rapid shifts in soil microbial community composition. Biogeochemistry 82:229–240CrossRefGoogle Scholar
  7. Craine JM, Morrow C, Fierer N (2007) Microbial nitrogen limitation increases decomposition. Ecology 88:2105–2113PubMedCrossRefGoogle Scholar
  8. De Graaff MA, Classen AT, Castro HF, Schadt CW (2010) Labile soil carbon inputs mediate the soil microbial community composition and plant residue decomposition rates. New Phytol 188:1055–1064PubMedCrossRefGoogle Scholar
  9. De Kauwe MG, Keenan TF, Medlyn BE, Prentice IC, Terrer C (2016) Satellite based estimates underestimate the effect of CO2 fertilization on net primary productivity. Nat Clim Chang 6:892–893CrossRefGoogle Scholar
  10. DeLucia EH, Hamilton JG, Naidu SL, Thomas RB, Andrews JA, Finzi A, Lavine M, Matamala R, Mohan JE, Hendrey GR (1999) Net primary production of a forest ecosystem with experimental CO2 enrichment. Science 284:1177–1179PubMedCrossRefPubMedCentralGoogle Scholar
  11. Fan Y, Lin F, Yang L, Zhong X, Wang M, Zhou J, Chen Y, Yang Y (2018) Decreased soil organic P fraction associated with ectomycorrhizal fungal activity to meet increased P demand under N application in a subtropical forest ecosystem. Biol Fertil Soils 54:149–161CrossRefGoogle Scholar
  12. Fan Y, Zhong X, Lin F, Liu C, Yang L, Wang M, Chen G, Chen Y, Yang Y (2019) Responses of soil phosphorus fractions after nitrogen addition in a subtropical forest ecosystem: insights from decreased Fe and Al oxides and increased plant roots. Geoderma 337:246–255CrossRefGoogle Scholar
  13. Fang Y, Nazaries L, Singh BK, Singh BP (2018) Microbial mechanisms of carbon priming effects revealed during the interaction of crop residue and nutrient inputs in contrasting soils. Glob Chang Biol 24:2775–2790PubMedCrossRefGoogle Scholar
  14. Fontaine S, Mariotti A, Abbadie L (2003) The priming effect of organic matter: a question of microbial competition? Soil Biol Biochem 35:837–843CrossRefGoogle Scholar
  15. Fontaine S, Bardoux G, Abbadie L, Mariotti A (2004) Carbon input to soil may decrease soil carbon content. Ecol Lett 7:314–320CrossRefGoogle Scholar
  16. Fontaine S, Henault C, Aamor A, Bdioui N, Bloor JMG, Maire V, Mary B, Revaillot S, Maron PA (2011) Fungi mediate long term sequestration of carbon and nitrogen in soil through their priming effect. Soil Biol Biochem 43:86–96CrossRefGoogle Scholar
  17. Frostegård Å, Tunlid A, Bååth E (2011) Use and misuse of PLFA measurements in soils. Soil Biol Biochem 43:1621–1625CrossRefGoogle Scholar
  18. Gershenson A, Bader NE, Cheng W (2009) Effects of substrate availability on the temperature sensitivity of soil organic matter decomposition. Glob Chang Biol 15:176–183CrossRefGoogle Scholar
  19. Ghani A, Sarathchandra U, Ledgard S, Dexter M, Lindsey S (2013) Microbial decomposition of leached or extracted dissolved organic carbon and nitrogen from pasture soils. Biol Fertil Soils 49:747–755CrossRefGoogle Scholar
  20. Girardin C, Rasse DP, Biron P, Ghashghaie J, Chenu C (2009) A method for 13C-labeling of metabolic carbohydrates within French bean leaves (Phaseolus vulgaris L.) for decomposition studies in soils. Rapid Commun Mass Sp 23:1792–1800CrossRefGoogle Scholar
  21. Gregorich E, Beare M, Stoklas U, St-Georges P (2003) Biodegradability of soluble organic matter in maize-cropped soils. Geoderma 113:237–252CrossRefGoogle Scholar
  22. Guo J, Yang Z, Lin C, Liu X, Chen G, Yang Y (2016) Conversion of a natural evergreen broadleaved forest into coniferous plantations in a subtropical area: effects on composition of soil microbial communities and soil respiration. Biol Fertil Soils 52:799–809CrossRefGoogle Scholar
  23. Hagedorn F, van Hees PAW, Handa IT, Hättenschwiler S (2008) Elevated atmospheric CO2 fuels leaching of old dissolved organic matter at the alpine treeline. Global Biogeochem Cy 22Google Scholar
  24. Hessen DO, Ågren GI, Anderson TR, Elser JJ, De Ruiter PC (2004) Carbon sequestration in ecosystems: the role of stoichiometry. Ecology 85:1179–1192CrossRefGoogle Scholar
  25. Jia Y, Yu G, Gao Y, He N, Wang Q, Jiao C, Zuo Y (2016) Global inorganic nitrogen dry deposition inferred from ground- and space-based measurements. Sci Rep 6:19810PubMedPubMedCentralCrossRefGoogle Scholar
  26. Kalbitz K, Solinger S, Park J-H, Michalzik B, Matzner E (2000) Controls on the dynamics of dissolved organic matter in soils: a review. Soil Sci 165:277–304CrossRefGoogle Scholar
  27. Kuzyakov Y (2010) Priming effects: interactions between living and dead organic matter. Soil Biol Biochem 42:1363–1371CrossRefGoogle Scholar
  28. Kuzyakov Y, Bol R (2006) Sources and mechanisms of priming effect induced in two grassland soils amended with slurry and sugar. Soil Biol Biochem 38:747–758CrossRefGoogle Scholar
  29. Kuzyakov Y, Friedel JK, Stahr K (2000) Review of mechanisms and quantification of priming effects. Soil Biol Biochem 32:1485–1498CrossRefGoogle Scholar
  30. Lee MH, Park J-H, Matzner E (2018) Sustained production of dissolved organic carbon and nitrogen in forest floors during continuous leaching. Geoderma 310:163–169CrossRefGoogle Scholar
  31. Li LJ, Zhu-Barker X, Ye R, Doane TA, Horwath WR (2018) Soil microbial biomass size and soil carbon influence the priming effect from carbon inputs depending on nitrogen availability. Soil Biol Biochem 119:41–49CrossRefGoogle Scholar
  32. Liu X, Lin TC, Yang Z, Vadeboncoeur MA, Lin C, Xiong D, Lin W, Chen G, Xie J, Li Y, Yang Y (2017) Increased litter in subtropical forests boosts soil respiration in natural forests but not plantations of Castanopsis carlesii. Plant Soil 418:141–151CrossRefGoogle Scholar
  33. Liu W, Qiao C, Yang S, Bai W, Liu L (2018) Microbial carbon use efficiency and priming effect regulate soil carbon storage under nitrogen deposition by slowing soil organic matter decomposition. Geoderma 332:37–44CrossRefGoogle Scholar
  34. Lyu M, Xie J, Wang C, Guo J, Wang M, Liu X, Chen Y, Chen G, Yang Y (2015) Forest conversion stimulated deep soil C losses and decreased C recalcitrance through priming effect in subtropical China. Biol Fertil Soils 51:857–867CrossRefGoogle Scholar
  35. Lyu M, Xie J, Vadeboncoeur MA, Wang M, Qiu X, Ren Y, Jiang M, Yang Y, Kuzyakov Y (2018) Simulated leaf litter addition causes opposite priming effects on natural forest and plantation soils. Biol Fertil Soils 54:925–934CrossRefGoogle Scholar
  36. Matson PA, McDowell WH, Townsend AR, Vitousek PM (1999) The globalization of N deposition: ecosystem consequences in tropical environments. Biogeochemistry 46:67–83Google Scholar
  37. Meyer N, Welp G, Rodionov A, Borchard N, Martius C, Amelung W (2018) Nitrogen and phosphorus supply controls soil organic carbon mineralization in tropical topsoil and subsoil. Soil Biol Biochem 119:152–161CrossRefGoogle Scholar
  38. Milcu A, Heim A, Ellis RJ, Scheu S, Manning P (2011) Identification of general patterns of nutrient and labile carbon control on soil carbon dynamics across a successional gradient. Ecosystems 14:710–719CrossRefGoogle Scholar
  39. Nadelhoffer KJ, Emmett BA, Gundersen P, Kjønaas OJ, Koopmans CJ, Schleppi P, Tietema A, Wright RF (1999) Nitrogen deposition makes a minor contribution to carbon sequestration in temperate forests. Nature 398:145–148CrossRefGoogle Scholar
  40. 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 48:743–762CrossRefGoogle Scholar
  41. Nannipieri P, Trasar-Cepeda C, Dick RP (2018) Soil enzyme activity: a brief history and biochemistry as a basis for appropriate interpretations and meta-analysis. Biol Fertil Soils 54:11–19CrossRefGoogle Scholar
  42. Nogués S, Tcherkez G, Cornic G, Ghashghaie J (2004) Respiratory carbon metabolism following illumination in intact French bean leaves using 13C/12C isotope labeling. Plant Physiol 136:3245–3254PubMedPubMedCentralCrossRefGoogle Scholar
  43. Nottingham AT, Turner BL, Chamberlain PM, Stott AW, Tanner EV (2012) Priming and microbial nutrient limitation in lowland tropical forest soils of contrasting fertility. Biogeochemistry 111:219–237CrossRefGoogle Scholar
  44. Nottingham AT, Hicks LC, Ccahuana AJQ, Salinas N, Bååth E, Meir P (2018) Nutrient limitations to bacterial and fungal growth during cellulose decomposition in tropical forest soils. Biol Fertil Soils 54:219–228CrossRefGoogle Scholar
  45. Olsson PA (1999) Signature fatty acids provide tools for determination of the distribution and interactions of mycorrhizal fungi in soil. FEMS Microbiol Ecol 29:303–310CrossRefGoogle Scholar
  46. Payne RJ, Dise NB, Field CD, Dore AJ, Caporn SJM, Stevens CJ (2017) Nitrogen deposition and plant biodiversity: past, present, and future. Front Ecol Environ 15:431–436CrossRefGoogle Scholar
  47. Phoenix GK, Hicks WK, Cinderby S, Kuylenstierna JCI, Stock WD, Dentener FJ, Giller KE, Austin AT, Lefroy RDB, Gimeno BS, Ashmore MR, Ineson P (2006) Atmospheric nitrogen deposition in world biodiversity hotspots: the need for a greater global perspective in assessing N deposition impacts. Glob Chang Biol 12:470–476CrossRefGoogle Scholar
  48. Qiao N, Schaefer D, Blagodatskaya E, Zou X, Xu X, Kuzyakov Y (2014) Labile carbon retention compensates for CO2 released by priming in forest soils. Glob Chang Biol 20:1943–1954PubMedCrossRefGoogle Scholar
  49. Qiu Q, Wu L, Ouyang Z, Li B, Xu Y, Wu S, Gregorich EG (2015) Effects of plant-derived dissolved organic matter (DOM) on soil CO2 and N2O emissions and soil carbon and nitrogen sequestrations. Appl Soil Ecol 96:122–130CrossRefGoogle Scholar
  50. Qiu Q, Wu L, Ouyang Z, Li B, Xu Y (2016) Different effects of plant-derived dissolved organic matter (DOM) and urea on the priming of soil organic carbon. Environ Sci Proc Imp 18:330–341Google Scholar
  51. Saiya-Cork K, Sinsabaugh R, Zak D (2002) The effects of long term nitrogen deposition on extracellular enzyme activity in an Acer saccharum forest soil. Soil Biol Biochem 34:1309–1315CrossRefGoogle Scholar
  52. Sauvadet M, Lashermes G, Alavoine G, Recous S, Chauvat M, Maron PA, Bertrand I (2018) High carbon use efficiency and low priming effect promote soil C stabilization under reduced tillage. Soil Biol Biochem 123:64–73CrossRefGoogle Scholar
  53. Schmidt BH, Wang CP, Chang SC, Matzner E (2010) High precipitation causes large fluxes of dissolved organic carbon and nitrogen in a subtropical montane Chamaecyparis forest in Taiwan. Biogeochemistry 101:243–256CrossRefGoogle Scholar
  54. Sinsabaugh RL (2010) Phenol oxidase, peroxidase and organic matter dynamics of soil. Soil Biol Biochem 42:391–404CrossRefGoogle Scholar
  55. Sinsabaugh R, Carreiro M, Repert D (2002) Allocation of extracellular enzymatic activity in relation to litter composition, N deposition, and mass loss. Biogeochemistry 60:1–24CrossRefGoogle Scholar
  56. Stark S, Männistö MK, Eskelinen A (2014) Nutrient availability and pH jointly constrain microbial extracellular enzyme activities in nutrient-poor tundra soils. Plant Soil 383:373–385CrossRefGoogle Scholar
  57. Swallow M, Quideau S, MacKenzie M, Kishchuk B (2009) Microbial community structure and function: the effect of silvicultural burning and topographic variability in northern Alberta. Soil Biol Biochem 41:770–777CrossRefGoogle Scholar
  58. Taketani F, Aita MN, Yamaji K, Sekiya T, Ikeda K, Sasaoka K, Hashioka T, Honda MC, Matsumoto K, Kanaya Y (2018) Seasonal response of north western Pacific marine ecosystems to deposition of atmospheric inorganic nitrogen compounds from East Asia. Sci Rep 8:9324PubMedPubMedCentralCrossRefGoogle Scholar
  59. Thiessen S, Gleixner G, Wutzler T, Reichstein M (2013) Both priming and temperature sensitivity of soil organic matter decomposition depend on microbial biomass – an incubation study. Soil Biol Biochem 57:739–748CrossRefGoogle Scholar
  60. Vitousek PM, Porder S, Houlton BZ, Chadwick OA (2010) Terrestrial phosphorus limitation: mechanisms, implications, and nitrogen-phosphorus interactions. Ecol Appl 20:5–15PubMedCrossRefPubMedCentralGoogle Scholar
  61. Wan X, Huang Z, He Z, Yu Z, Wang M, Davis MR, Yang Y (2015) Soil C: N ratio is the major determinant of soil microbial community structure in subtropical coniferous and broadleaf forest plantations. Plant Soil 387:103–116CrossRefGoogle Scholar
  62. Wang Q, Wang S, He T, Liu L, Wu J (2014) Response of organic carbon mineralization and microbial community to leaf litter and nutrient additions in subtropical forest soils. Soil Biol Biochem 71:13–20CrossRefGoogle Scholar
  63. Wang H, Xu W, Hu G, Dai W, Jiang P, Bai E (2015) The priming effect of soluble carbon inputs in organic and mineral soils from a temperate forest. Oecologia 178:1239–1250PubMedCrossRefPubMedCentralGoogle Scholar
  64. Xiao C, Guenet B, Zhou Y, Su J, Janssens IA (2015) Priming of soil organic matter decomposition scales linearly with microbial biomass response to litter input in steppe vegetation. Oikos 124:649–657CrossRefGoogle Scholar
  65. Yang Y, Guo J, Chen G, Xie J, Cai L, Lin P (2004) Litterfall, nutrient return, and leaf-litter decomposition in four plantations compared with a natural forest in subtropical China. Ann Forest Sci 61:465–476CrossRefGoogle Scholar
  66. Yang Y, Guo J, Chen G, Yin Y, Gao R, Lin C (2009) Effects of forest conversion on soil labile organic carbon fractions and aggregate stability in subtropical China. Plant Soil 323:153–162CrossRefGoogle Scholar
  67. Yang Y, Donohue RJ, McVicar TR, Roderick ML, Beck HE (2016) Long-term CO2 fertilization increases vegetation productivity and has little effect on hydrological partitioning in tropical rainforests. J Geophys Res-Biogeo 121:2125–2140CrossRefGoogle Scholar

Copyright information

© Springer-Verlag GmbH Germany, part of Springer Nature 2019

Authors and Affiliations

  • Yuexin Fan
    • 1
    • 2
  • Xiaojian Zhong
    • 1
    • 2
  • Teng-Chiu Lin
    • 3
  • Maokui Lyu
    • 2
  • Minhuang Wang
    • 2
  • Weifang Hu
    • 2
  • Zhijie Yang
    • 1
    • 2
  • Guangshui Chen
    • 1
    • 2
  • Jianfen Guo
    • 1
    • 2
    Email author
  • Yusheng Yang
    • 1
    • 2
    • 4
    Email author
  1. 1.State Key Laboratory for Subtropical Mountain Ecology of the Ministry of Science and Technology and Fujian ProvinceFujian Normal UniversityFuzhouChina
  2. 2.School of Geographical SciencesFujian Normal UniversityFuzhouChina
  3. 3.Department of Life ScienceNational Taiwan Normal UniversityTaipeiTaiwan
  4. 4.Institute of GeographyFujian Normal UniversityFuzhouChina

Personalised recommendations