Different responses of priming effects in long-term nitrogen- and phosphorus-fertilized soils to exogenous carbon inputs

Wenkuan Qin1, Jiguang Feng1, Qiufang Zhang1, Xiuliang Yuan2, Fei Ren3, Huakun Zhou4, Biao Zhu1
1Institute of Ecology and Ministry of Education Key Laboratory for Earth Surface Processes, College of Urban and Environmental Sciences, Peking University, Beijing, 100871, China
2College of Life and Environmental Sciences, Hangzhou Normal University, Hangzhou 311121, China
3State Key Laboratory of Plateau Ecology and Agriculture, Qinghai University, Xining, 810000, China
4Qinghai Provincial Key Laboratory of Restoration Ecology of Cold Area, Northwest Institute of Plateau Biology, Chinese Academy of Sciences, Xining, 810008, China

Tóm tắt

Từ khóa


Tài liệu tham khảo

Bastida F, García C, Fierer N, Eldridge DJ, Bowker MA, Abades S, Alfaro FD, Berhe AA, Cutler NA, Gallardo A, García-Velázquez L, Hart SC, Hayes PE, Hernández T, Hseu Z-Y, Jehmlich N, Kirchmair M, Lambers H, Neuhauser S, Peña-Ramírez VM, Pérez CA, Reed SC, Santos F, Siebe C, Sullivan BW, Trivedi P, Vera A, Williams MA, Moreno JL, Delgado-Baquerizo M (2019) Global ecological predictors of the soil priming effect. Nat Comm 10:1–9. https://doi.org/10.1038/s41467-019-11472-7

Bernard L, Basile-Doelsch I, Derrien D, Fanin N, Fontaine S, Guenet B, Karimi B, Marsden C, Maron P-A (2022) Advancing the mechanistic understanding of the priming effect on soil organic matter mineralisation. Funct Ecol 36:1355–1377. https://doi.org/10.1111/1365-2435.14038

Bindraban PS, Dimkpa CO, Pandey R (2020) Exploring phosphorus fertilizers and fertilization strategies for improved human and environmental health. Biol Fertil Soils 56:299–317. https://doi.org/10.1007/s00374-019-01430-2

Blagodatskaya E, 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 45:115–131. https://doi.org/10.1007/s00374-008-0334-y

Blagodatskaya E, Yuyukina T, Blagodatsky S, Kuzyakov Y (2011) Three-source-partitioning of microbial biomass and of CO2 efflux from soil to evaluate mechanisms of priming effects. Soil Biol Biochem 43:778–786. https://doi.org/10.1016/j.soilbio.2010.12.011

Blagodatsky S, Blagodatskaya E, Yuyukina T, Kuzyakov Y (2010) Model of apparent and real priming effects: linking microbial activity with soil organic matter decomposition. Soil Biol Biochem 42:1275–1283. https://doi.org/10.1016/j.soilbio.2010.04.005

Bossio DA, Scow KM (1998) Impacts of carbon and flooding on soil microbial communities: phospholipid fatty acid profiles and substrate utilization patterns. Microb Ecol 35:265–278. https://doi.org/10.1007/s002489900082

Chang XF, Zhu XX, Wang SP, Cui SJ, Luo CY, Zhang ZH, Wilkes A (2014) Impacts of management practices on soil organic carbon in degraded alpine meadows on the Tibetan Plateau. Biogeosciences 11:3495–3503. https://doi.org/10.5194/bg-11-3495-2014

Chen C, Xiao W (2023) The global positive effect of phosphorus addition on soil microbial biomass. Soil Biol Biochem 176:108882. https://doi.org/10.1016/j.soilbio.2022.108882

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 Change Biol 20:2356–2367. https://doi.org/10.1111/gcb.12475

Chen LY, Liu L, Mao C, Qin SQ, Liu FT, Blagodatsky S, Yang GB, Zhang QW, Zhang DY, Yu JC, Yang YH (2018) Nitrogen availability regulates topsoil carbon dynamics after permafrost thaw by altering microbial metabolic efficiency. Nat Commun 9:3951. https://doi.org/10.1038/s41467-018-06232-y

Chen H, Yin C, Fan X, Ye M, Liang Y (2021) Effect of P availability on straw-induced priming effect was mainly regulated by fungi in croplands. Appl Microbiol Biotechnol 105:9403–9418. https://doi.org/10.1007/s00253-021-11691-3

Cheng W, Parton WJ, Gonzalez-Meler MA, Phillips R, Asao S, McNickle GG, Brzostek E, Jastrow JD (2014) Synthesis and modeling perspectives of rhizosphere priming. New Phytol 201:31–44. https://doi.org/10.1111/nph.12440

Craine JM, Morrow C, Fierer N (2007) Microbial nitrogen limitation increases decomposition. Ecology 88:2105–2113. https://doi.org/10.1890/06-1847.1

Deng L, Peng C, Zhu G, Chen L, Liu Y, Shangguan Z (2018) Positive responses of belowground C dynamics to nitrogen enrichment in China. Sci Total Environ 616–617:1035–1044. https://doi.org/10.1016/j.scitotenv.2017.10.215

Di Lonardo DP, De Boer W, Gunnewiek PJAK, Hannula SE, Van der Wal A (2017) Priming of soil organic matter: chemical structure of added compounds is more important than the energy content. Soil Biol Biochem 108:41–54. https://doi.org/10.1016/j.soilbio.2017.01.017

Dong K, Li W, Tang Y, Ma S, Jiang M (2023) Co-limitation of N and P is more prevalent in the Qinghai-Tibetan Plateau grasslands. Front Plant Sci 14:1140462. https://doi.org/10.3389/fpls.2023.1140462

Du E, Terrer C, Pellegrini AFA, Ahlström A, van Lissa CJ, Zhao X, Xia N, Wu X, Jackson RB (2020) Global patterns of terrestrial nitrogen and phosphorus limitation. Nat Geosci 13:221–226. https://doi.org/10.1038/s41561-019-0530-4

Elser JJ, Bracken MES, Cleland EE, Gruner DS, Harpole WS, Hillebrand H, Ngai JT, Seabloom EW, Shurin JB, Smith JE (2007) Global analysis of nitrogen and phosphorus limitation of primary producers in freshwater, marine and terrestrial ecosystems. Ecol Lett 10:1135–1142. https://doi.org/10.1111/j.1461-0248.2007.01113.x

Feng J, Zhu B (2021) Global patterns and associated drivers of priming effect in response to nutrient addition. Soil Biol Biochem 153:108118. https://doi.org/10.1016/j.soilbio.2020.108118

Feng J, Tang M, Zhu B (2021) Soil priming effect and its responses to nutrient addition along a tropical forest elevation gradient. Glob Change Biol 27:2793–2806. https://doi.org/10.1111/gcb.15587

Feng J, Song Y, Zhu B (2023) Ecosystem-dependent responses of soil carbon storage to phosphorus enrichment. New Phytol 238(6):2363–2374. https://doi.org/10.1111/nph.18907

Fu G, Shen Z-X (2017) Response of alpine soils to nitrogen addition on the Tibetan Plateau: a meta-analysis. Appl Soil Ecol 114:99–104. https://doi.org/10.1016/j.apsoil.2017.03.008

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. https://doi.org/10.1016/j.soilbio.2011.11.002

Griffiths BS, Spilles A, Bonkowski M (2012) C:N: P stoichiometry and nutrient limitation of the soil microbial biomass in a grazed grassland site under experimental P limitation or excess. Ecol Process 1:6. https://doi.org/10.1186/2192-1709-1-6

Guo JH, Liu XJ, Zhang Y, Shen JL, Han WX, Zhang WF, Christie P, Goulding KWT, Vitousek PM, Zhang FS (2010) Significant acidification in major Chinese croplands. Science 327:1008–1010. https://doi.org/10.1126/science.1182570

Harpole WS, Sullivan LL, Lind EM, Firn J, Adler PB, Borer ET, Chase J, Fay PA, Hautier Y, Hillebrand H, MacDougallm AS, Seabloom EW, Williams R, Bakker JD, Cadotte MW, Chaneton EJ, Chu CJ, Cleland EE, D’Antonio C, Davies KF, Gruner DS, Hagenah N, Kirkman K, Knops JMH, La Pierre KJ, McCulley RL, Moore JL, Morgan JW, Prober SM, Risch AC, Schuetz M, Stevens CJ, Wragg PD (2016) Addition of multiple limiting resources reduces grassland diversity. Nature 537:93–96. https://doi.org/10.1038/nature19324

He D, Xiang X, He J, Wang C, Cao G, Adams J, Chu H (2016) Composition of the soil fungal community is more sensitive to phosphorus than nitrogen addition in the alpine meadow on the Qinghai-Tibetan Plateau. Biol Fertil Soils 52:1059–1072. https://doi.org/10.1007/s00374-016-1142-4

Hessen DO, Ågren GI, Anderson TR, Elser JJ, de Ruiter PC (2004) carbon sequestration in ecosystems: the role of stoichiometry. Ecology 85:1179–1192. https://doi.org/10.1890/02-0251

Hicks LC, Meir P, Nottingham AT, Reay DS, Stott AW, Salinas N, Whitaker J (2019) Carbon and nitrogen inputs differentially affect priming of soil organic matter in tropical lowland and montane soils. Soil Biol Biochem 129:212–222. https://doi.org/10.1016/j.soilbio.2018.10.015

Hicks Pries CE, Ryals R, Zhu B, Min K, Cooper A, Goldsmith S, Pett-Ridge J, Torn M, Berhe AA (2023) The deep soil organic carbon response to global change. Annu Rev Ecol Evol Syst 54:375–401. https://doi.org/10.1146/annurev-ecolsys-102320-085332

Hou E, Luo Y, Kuang Y, Chen C, Lu X, Liang L, Luo X, Wen D (2020) Global meta-analysis shows pervasive phosphorus limitation of aboveground plant production in natural terrestrial ecosystems. Nat Commun 11:637. https://doi.org/10.1038/s41467-020-14492-w

Humbert J-Y, Dwyer JM, Andrey A, Arlettaz R (2016) Impacts of nitrogen addition on plant biodiversity in mountain grasslands depend on dose, application duration and climate: a systematic review. Glob Change Biol 22:110–120. https://doi.org/10.1111/gcb.12986

Jenkinson DS, Brookes PC, Powlson DS (2004) Measuring soil microbial biomass. Soil Biol Biochem 36:5–7. https://doi.org/10.1016/j.soilbio.2003.10.002

Jia Y, Yu G, He N, Zhan X, Fang H, Sheng W, Zuo Y, Zhang D, Wang Q (2014) Spatial and decadal variations in inorganic nitrogen wet deposition in China induced by human activity. Sci Rep 4:3763. https://doi.org/10.1038/srep03763

Jia J, Feng X, He J-S, He H, Lin L, Liu Z (2017) Comparing microbial carbon sequestration and priming in the subsoil versus topsoil of a Qinghai-Tibetan alpine grassland. Soil Biol Biochem 104:141–151. https://doi.org/10.1016/j.soilbio.2016.10.018

Jing X, Yang X, Ren F, Zhou H, Zhu B, He J (2016) Neutral effect of nitrogen addition and negative effect of phosphorus addition on topsoil extracellular enzymatic activities in an alpine grassland ecosystem. Appl Soil Ecol 107:205–213. https://doi.org/10.1016/j.apsoil.2016.06.004

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. https://doi.org/10.1016/j.scitotenv.2017.07.060

Joergensen RG (2022) Phospholipid fatty acids in soil—drawbacks and future prospects. Biol Fertil Soils 58:1–6. https://doi.org/10.1007/s00374-021-01613-w

Keiluweit M, Bougoure J, Nico P, Pett-Ridge J, Weber PK, Kleber M (2015) Mineral protection of soil carbon counteracted by root exudates. Nature Clim Change 5:588–595. https://doi.org/10.1038/nclimate2580

Kuzyakov Y (2010) Priming effects: interactions between living and dead organic matter. Soil Biol Biochem 42:1363–1371. https://doi.org/10.1016/j.soilbio.2010.04.003

Kuzyakov Y, Friedel JK, Stahr K (2000) Review of mechanisms and quantification of priming effects. Soil Biol Biochem 32:1485–1498. https://doi.org/10.1016/S0038-0717(00)00084-5

Lefcheck JS (2016) piecewiseSEM: piecewise structural equation modelling in r for ecology, evolution, and systematics. Methods Ecol Evol 7:573–579. https://doi.org/10.1111/2041-210X.12512

Leff JW, Jones SE, Prober SM, Barberán A, Borer ET, Firn JL, Harpole WS, Hobbie SE, Hofmockel KS, Knops JMH, McCulley RL, La Pierre K, Risch AC, Seabloom EW, Schütz M, Steenbock C, Stevens CJ, Fierer N (2015) Consistent responses of soil microbial communities to elevated nutrient inputs in grasslands across the globe. Proc Natl Acad Sci USA 112:10967–10972. https://doi.org/10.1073/pnas.1508382112

Lehmann J, Kleber M (2015) The contentious nature of soil organic matter. Nature 528:60–68. https://doi.org/10.1038/nature16069

Li L, Qu Z, Jia R, Wang B, Wang Y, Qu D (2017) Excessive input of phosphorus significantly affects microbial Fe(III) reduction in flooded paddy soils by changing the abundances and community structures of Clostridium and Geobacteraceae. Sci Total Environ 607–608:982–991. https://doi.org/10.1016/j.scitotenv.2017.07.078

Li JH, Han YW, Ye LF, Deng HD, Gao XT, Soromotin AV, Kuzyakov Y, Knops JMH, Abbott LK (2023) Effects of nitrogen and phosphorus fertilization on soil organic matter priming and net carbon balance in alpine meadows. Land Degrad Dev 34(9):2681–2692. https://doi.org/10.1002/ldr.4642

Liu C, Zhang S (2019) Nitrogen addition shapes soil enzyme activity patterns by changing pH rather than the composition of the plant and microbial communities in an alpine meadow soil. Plant Soil 440:11–24. https://doi.org/10.1007/s11104-019-04054-5

Liu H, Mi Z, Lin L, Wang Y, Zhang Z, Zhang F, Wang H, Liu L, Zhu B, Cao G, Zhao X, Sanders NJ, Classen AT, Reich PB, He J-S (2018a) Shifting plant species composition in response to climate change stabilizes grassland primary production. Proc Natl Acad Sci USA 115:4051–4056. https://doi.org/10.1073/pnas.1700299114

Liu W, Qiao C, Yang S, Bai W, Liu L (2018b) Microbial carbon use efficiency and priming effect regulate soil carbon storage under nitrogen deposition by slowing soil organic matter decomposition. Geoderma 332:37–44. https://doi.org/10.1016/j.geoderma.2018.07.008

Luo R, Fan J, Wang W, Luo J, Kuzyakov Y, He J-S, Chu H, Ding W (2019) Nitrogen and phosphorus enrichment accelerates soil organic carbon loss in alpine grassland on the Qinghai-Tibetan Plateau. Sci Total Environ 650:303–312. https://doi.org/10.1016/j.scitotenv.2018.09.038

Luo R, Kuzyakov Y, Liu D, Fan J, Luo J, Lindsey S, He J, Ding W (2020) Nutrient addition reduces carbon sequestration in a Tibetan grassland soil: disentangling microbial and physical controls. Soil Biol Biochem 144:107764. https://doi.org/10.1016/j.soilbio.2020.107764

Malik AA, Martiny JBH, Brodie EL, Martiny AC, Treseder KK, Allison SD (2020) Defining trait-based microbial strategies with consequences for soil carbon cycling under climate change. ISME J 14:1–9. https://doi.org/10.1038/s41396-019-0510-0

Mason-Jones K, Schmücker N, Kuzyakov Y (2018) Contrasting effects of organic and mineral nitrogen challenge the N-mining hypothesis for soil organic matter priming. Soil Biol Biochem 124:38–46. https://doi.org/10.1016/j.soilbio.2018.05.024

Mehnaz KR, Corneo PE, Keitel C, Dijkstra FA (2019) Carbon and phosphorus addition effects on microbial carbon use efficiency, soil organic matter priming, gross nitrogen mineralization and nitrous oxide emission from soil. Soil Biol Biochem 134:175–186. https://doi.org/10.1016/j.soilbio.2019.04.003

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 119:152–161. https://doi.org/10.1016/j.soilbio.2018.01.024

Niu G, Wang Y. Wang R, Ning Q, Guan H, Yang J, Lu X, Han X, Huang J (2022) Intensity and duration of nitrogen addition jointly alter soil nutrient availability in a temperate grassland. J Geophys Res-Biogeosc 127:e2021JG006698. https://doi.org/10.1029/2021JG006698

Parajuli B, Ye R, Szogi A (2022) Mineral N suppressed priming effect while increasing microbial C use efficiency and N2O production in sandy soils under long-term conservation management. Biol Fertil Soils 58:903–915. https://doi.org/10.1007/s00374-022-01665-6

Perveen N, Barot S, Maire V, Cotrufo MF, Shahzad T, Blagodatskaya E, Stewart CE, Ding W, Siddiq MR, Dimassi B, Mary B, Fontaine S (2019) Universality of priming effect: an analysis using thirty-five soils with contrasted properties sampled from five continents. Soil Biol Biochem 134:162–171. https://doi.org/10.1016/j.soilbio.2019.03.027

Phillips DL, Newsome SD, Gregg JW (2005) Combining sources in stable isotope mixing models: alternative methods. Oecologia 144:520–527. https://doi.org/10.1007/s00442-004-1816-8

Raven JA, Lambers H, Smith SE, Westoby M (2018) Costs of acquiring phosphorus by vascular land plants: patterns and implications for plant coexistence. New Phytol 217:1420–1427. https://doi.org/10.1111/nph.14967

Shi J, Zhao B, Zheng S, Zhang X, Wang X, Dong W, Xie Q, Wang G, Xiao Y, Chen F, Yu N, Wang E (2021) A phosphate starvation response-centered network regulates mycorrhizal symbiosis. Cell 184:5527–5540. https://doi.org/10.1016/j.cell.2021.09.030

Song M, Guo Y, Yu F, Zhang X, Cao G, Cornelissen JHC (2018) Shifts in priming partly explain impacts of long-term nitrogen input in different chemical forms on soil organic carbon storage. Glob Change Biol 24:4160–4172. https://doi.org/10.1111/gcb.14304

Sun Y, Wang C, Chen HYH, Ruan H (2020) Responses of C: N stoichiometry in plants, soil, and microorganisms to nitrogen addition. Plant Soil 456:277–287. https://doi.org/10.1007/s11104-020-04717-8

Tan H, Barret M, Mooij MJ, Rice O, Morrissey JP, Dobson A, Griffiths B, O Gara F (2013) Long-term phosphorus fertilisation increased the diversity of the total bacterial community and the phoD phosphorus mineraliser group in pasture soils. Biol Fertil Soils 49:661–672. https://doi.org/10.1007/s00374-012-0755-5

Tunlid A, Hoitink HAJ, Low C, White DC (1989) Characterization of bacteria that suppress rhizoctonia damping-off in bark compost media by analysis of fatty acid biomarkers. Appl Environ Microbiol 55:1368–1374. https://doi.org/10.1128/AEM.55.6.1368-1374.1989

Vance ED, Brookes PC, Jenkinson DS (1987) An extraction method for measuring soil microbial biomass C. Soil Biol Biochem 19:703–707. https://doi.org/10.1016/0038-0717(87)90052-6

Wang S, Huang M, Shao X, Mickler RA, Li K, Ji J (2004) Vertical distribution of soil organic carbon in China. Environ Manage 33:S200–S209. https://doi.org/10.1007/s00267-003-9130-5

Wang D, Zhu Z, Shahbaz M, Chen L, Liu S, Inubushi K, Wu J, Ge T (2019) Split N and P addition decreases straw mineralization and the priming effect of a paddy soil: a 100-day incubation experiment. Biol Fertil Soils 55:701–712. https://doi.org/10.1007/s00374-019-01383-6

Wang X, Li S, Zhu B, Homyak PM, Chen G, Yao X, Wu D, Yang Z, Lyu M, Yang Y (2023a) Long-term nitrogen deposition inhibits soil priming effects by enhancing phosphorus limitation in a subtropical forest. Glob Change Biol 29:4081–4093. https://doi.org/10.1111/gcb.16718

Wang XD, Feng JG, Ao GKL, Qin WK, Han MG, Shen YW, Liu ML, Chen Y, Zhu B (2023b) Globally nitrogen addition alters soil microbial community structure, but has minor effects on soil microbial diversity and richness. Soil Biol Biochem 179:108982. https://doi.org/10.1016/j.soilbio.2023.108982

Waring BG, Averill C, Hawkes CV (2013) Differences in fungal and bacterial physiology alter soil carbon and nitrogen cycling: insights from meta-analysis and theoretical models. Ecol Lett 16:887–894. https://doi.org/10.1111/ele.12125

Wieder W, Cleveland C, Smith W, Todd-Brown K (2015) Future productivity and carbon storage limited by terrestrial nutrient availability. Nature Geosci 8:441–444. https://doi.org/10.1038/ngeo2413

Wollum AG II, Gomez JE (1970) A conductivity method for measuring microbially evolved carbon dioxide. Ecology 51:155–156. https://doi.org/10.2307/1933610

Yang Y, Fang J, Tang Y, Ji C, Zheng C, He J, Zhu B (2008) Storage, patterns and controls of soil organic carbon in the Tibetan grasslands. Glob Change Biol 14:1592–1599. https://doi.org/10.1111/j.1365-2486.2008.01591.x

You M, Li L-J, Tian Q, He P, He G, Hao X-X, Horwath WR (2020) 2020 residue decomposition and priming of soil organic carbon following different NPK fertilizer histories. Soil Sci Soc Am J 84:1898–1909. https://doi.org/10.1002/saj2.20142

Yuan X, Knelman JE, Gasarch E, Wang D, Nemergut DR, Seastedt TR (2016) Plant community and soil chemistry responses to long-term nitrogen inputs drive changes in alpine bacterial communities. Ecology 97:1543–1554. https://doi.org/10.1890/15-1160.1

Yuan X, Qin WK, Xu H, Zhang ZH, Zhou HK, Zhu B (2020) Sensitivity of soil carbon dynamics to nitrogen and phosphorus enrichment in an alpine meadow. Soil Biol Biochem 150:107984. https://doi.org/10.1016/j.soilbio.2020.107984

Zamanian K, Zarebanadkouki M, Kuzyakov Y (2018) Nitrogen fertilization raises CO2 efflux from inorganic carbon: a global assessment. Glob Change Biol 24:2810–2817. https://doi.org/10.1111/gcb.14148

Zhang K, Ni Y, Liu X, Chu H (2020) Microbes changed their carbon use strategy to regulate the priming effect in an 11-year nitrogen addition experiment in grassland. Sci Total Environ 727:138645. https://doi.org/10.1016/j.scitotenv.2020.138645

Zheng T, Miltner A, Liang C, Nowak KM, Kästner M (2023) Turnover of bacterial biomass to soil organic matter via fungal biomass and its metabolic implications. Soil Biol Biochem 180:108995. https://doi.org/10.1016/j.soilbio.2023.108995

Zhou Z, Wang C, Zheng M, Jiang L, Luo Y (2017) Patterns and mechanisms of responses by soil microbial communities to nitrogen addition. Soil Biol Biochem 115:433–441. https://doi.org/10.1016/j.soilbio.2017.09.015

Zhu J, Wang Q, He N, Smith MD, Elser JJ, Du J, Yuan G, Yu G, Yu Q (2016) Imbalanced atmospheric nitrogen and phosphorus depositions in China: implications for nutrient limitation. J Geophys Res-Biogeosci 121:1605–1616. https://doi.org/10.1002/2016JG003393