收稿日期: 2022-12-12
修回日期: 2023-08-25
网络出版日期: 2023-10-24
基金资助
国家自然科学基金项目(32271687);中国科学院青年创新促进会优秀会员项目(Y201965)
Responses of Soil Microbial Carbon Use Efficiency to Elevated Nitrogen Deposition in Forest Ecosystems
Received date: 2022-12-12
Revised date: 2023-08-25
Online published: 2023-10-24
Supported by
the National Natural Science Foundation of China(32271687);Youth Innovation Promotion Association CAS(Y201965)
大气氮沉降增加及其全球化影响了陆地生态系统碳循环模式。微生物碳利用效率是驱动土壤碳循环的重要因素，同时也是土壤碳循环模型的重要参数。然而，氮沉降对土壤微生物碳利用效率影响的结论不一致，其背后的作用机理也不清晰，这严重限制了对在大气氮沉降下土壤碳循环动态和碳储存潜力的预测。对森林生态系统土壤微生物碳利用效率的历程和方法进行了综述，并从生物因子和非生物因子两个方面归纳总结了氮沉降增加对微生物碳利用效率影响的机理。在生物因子方面，氮沉降可通过改变微生物量和群落结构以及调节微生物酶活影响微生物碳利用效率；在非生物因子方面，氮沉降可通过改变土壤氮状态、土壤化学计量学和土壤pH，以及地上植被动态（如根系分泌物、凋落物输入等）影响微生物碳利用效率。总体来看，适量氮沉降可以缓解生态系统的氮限制，提高微生物的活性，进而促进微生物碳利用效率；但过量氮沉降则会抑制微生物生长，降低微生物碳利用效率。最后，对未来研究进行了展望，强调要优化微生物碳利用效率的测定方法、从不同时间尺度和空间尺度研究多因素交互的影响等， 以期为深入研究森林生态系统碳循环过程与机制提供理论支持，同时为准确评估和预测森林生态系统土壤碳库的固碳潜力提供科学依据。
张雪冰 , 张泽和 , 鲁显楷 . 森林生态系统土壤微生物碳利用效率对氮沉降增加的响应及其机制[J]. 地球科学进展, 2023 , 38(10) : 999 -1014 . DOI: 10.11867/j.issn.1001-8166.2023.061
Globalization and elevated atmospheric Nitrogen (N) deposition have significantly altered the terrestrial carbon cycle. Soil microbial Carbon Use Efficiency (CUE) plays a key role in adjusting soil cycling rates and processes and is also an important parameter in soil C cycle models. However, the effects of elevated N deposition on soil microbial CUE are often inconsistent, which limits the reliability of predictions of both soil C cycle dynamics and C storage capacity under global changes. Here, we review advances in research on soil microbial CUE and measurement methods. We further explore the mechanisms underlying the effects of increased nitrogen deposition on CUE from both biological and abiotic perspectives in forest ecosystems. In terms of biological mechanisms, N deposition can affect CUE by changing microbial biomass and community structure and by regulating microbial enzyme activities. In terms of abiotic mechanisms, N deposition can affect CUE by changing the N addition-induced changes in the soil nitrogen state, soil stoichiometry, soil pH, and aboveground vegetation dynamics (such as root exudates and litter input), which can independently or jointly affect soil microbial CUE. In general, moderate nitrogen deposition can alleviate ecosystem nitrogen limitation and stimulate microbial activity, thus increasing soil microbial CUE. In contrast, excessive N deposition decreases microbial CUE by inhibiting microbial growth. Lastly, the potential research activities and recommendations for future research are presented. Therefore, it is imperative to optimize the determination of microbial CUE for comparative research among different ecosystems. At temporal and spatial scales, more attention should be paid to the interaction effects of multiple factors under global changes, so that there is a strong theoretical basis for evaluating and predicting the soil carbon sequestration capacity in forest ecosystems.
| 1 | FRIEDLI H， L?TSCHER H， OESCHGER H， et al. Ice core record of the 13C/12C ratio of atmospheric CO2 in the past two centuries［J］. Nature， 1986， 324（6 094）： 237-238. |
| 2 | FAN S， GLOOR M， MAHLMAN J， et al. A large terrestrial carbon sink in North America implied by atmospheric and oceanic carbon dioxide data and models ［J］. Science， 1998， 282（5 388）： 442-446. |
| 3 | KAISER J. Panel estimates possible carbon ‘sinks’［J］. Science， 2000， 288（5 468）： 942-943. |
| 4 | MONNIN E， INDERMU?HLE A， DA?LLENBACH A， et al. Atmospheric CO2 concentrations over the Last Glacial Termination［J］. Science， 2001， 291（5 501）： 112-114. |
| 5 | SCHNEIDER S H. The greenhouse effect： science and policy ［J］. Science， 1989， 243（4 892）： 771-781. |
| 6 | LASHOF D A， AHUJA D R. Relative contributions of greenhouse gas emissions to global warming ［J］. Nature， 1990， 344（6 266）： 529-531. |
| 7 | LU Xiankai， MO Jiangming， ZHANG Wei， et al. Effects of simulated atmospheric nitrogen deposition on forest ecosystems in China： an overview ［J］. Journal of Tropical and Subtropical Botany， 2019， 27（5）： 500-522. |
| 7 | 鲁显楷， 莫江明， 张炜， 等. 模拟大气氮沉降对中国森林生态系统影响的研究进展 ［J］. 热带亚热带植物学报， 2019， 27（5）： 500-522. |
| 8 | GALLOWAY J N， TOWNSEND A R， ERISMAN J W， et al. Transformation of the nitrogen cycle： recent trends， questions， and potential solutions ［J］. Science， 2008， 320（5 878）： 889-892. |
| 9 | ACKERMAN D， MILLET D B， CHEN X. Global estimates of inorganic nitrogen deposition across four decades［J］. Global Biogeochemical Cycles， 2019， 33（1）： 100-107. |
| 10 | YU G R， JIA Y L， HE N P， et al. Stabilization of atmospheric nitrogen deposition in China over the past decade［J］. Nature Geoscience， 2019， 12（6）： 424-429. |
| 11 | WANG C M， YANG X T， XU K. Effect of chronic nitrogen fertilization on soil CO2 flux in a temperate forest in North China： a 5-year nitrogen addition experiment［J］. Journal of Soils and Sediments， 2018， 18（2）： 506-516. |
| 12 | WANG Q K， ZHANG W D， SUN T， et al. N and P fertilization reduced soil autotrophic and heterotrophic respiration in a young Cunninghamia lanceolata forest［J］. Agricultural and Forest Meteorology， 2017， 232： 66-73. |
| 13 | LIU X J， ZHANG Y， HAN W X， et al. Enhanced nitrogen deposition over China［J］. Nature， 2013， 494（7 438）： 459-462. |
| 14 | CUI S H， SHI Y L， GROFFMAN P M， et al. Centennial-scale analysis of the creation and fate of reactive nitrogen in China （1910-2010）［J］. Proceedings of the National Academy of Sciences of the United States of America， 2013， 110（6）： 2 052-2 057. |
| 15 | FORNARA D A， TILMAN D. Soil carbon sequestration in prairie grasslands increased by chronic nitrogen addition ［J］. Ecology， 2012， 93（9）： 2 030-2 036. |
| 16 | LIU L L， GREAVER T L. A global perspective on belowground carbon dynamics under nitrogen enrichment［J］. Ecology Letters， 2010， 13（7）： 819-828. |
| 17 | LU X K， VITOUSEK P M， MAO Q G， et al. Nitrogen deposition accelerates soil carbon sequestration in tropical forests［J］. Proceedings of the National Academy of Sciences of the United States of America， 2021， 118（16）. DOI：10.1073/pnas.202079011 . |
| 18 | SCHIMEL J P， SCHAEFFER S M. Microbial control over carbon cycling in soil ［J］. Frontiers in Microbiology， 2012， 3. DOI：10.3389/fmicb.2012.00348 . |
| 19 | GEORGIOU K， ABRAMOFF R Z， HARTE J， et al. Microbial community-level regulation explains soil carbon responses to long-term litter manipulations［J］. Nature Communications， 2017， 8（1）. DOI：10.1038/s41467-017-01116-z . |
| 20 | MALIK A A， PUISSANT J， BUCKERIDGE K M， et al. Land use driven change in soil pH affects microbial carbon cycling processes ［J］. Nature Communications， 2018， 9. DOI：10.1038/s41467-018-05980-1 . |
| 21 | LIANG Chao， ZHU Xuefeng. The soil microbial carbon pump as a new concept for terrestrial carbon sequestration ［J］. Science China： Earth Sciences， 2021， 51（5）： 680-695. |
| 21 | 梁超， 朱雪峰. 土壤微生物碳泵储碳机制概论 ［J］. 中国科学：地球科学， 2021， 51（5）： 680-695. |
| 22 | LIANG C， SCHIMEL J P， JASTROW J D. The importance of anabolism in microbial control over soil carbon storage［J］. Nature Microbiology， 2017， 2（8）. DOI： 10.1038/nmicrobiol.2017.105 . |
| 23 | GLEIXNER G. Soil organic matter dynamics： a biological perspective derived from the use of compound-specific isotopes studies ［J］. Ecological Research， 2013， 28（5）： 683-695. |
| 24 | MANZONI S， TAYLOR P， RICHTER A， et al. Environmental and stoichiometric controls on microbial carbon-use efficiency in soils ［J］. New Phytologist， 2012， 196（1）： 79-91. |
| 25 | SINSABAUGH R L， MANZONI S， MOORHEAD D L， et al. Carbon use efficiency of microbial communities： stoichiometry， methodology and modelling ［J］. Ecology Letters， 2013， 16（7）： 930-939. |
| 26 | TAO F， HUANG Y Y， HUNGATE B A， et al. Microbial carbon use efficiency promotes global soil carbon storage［J］. Nature， 2023， 618（7 967）： 981-985. |
| 27 | KALLENBACH C M， FREY S D， GRANDY A S. Direct evidence for microbial-derived soil organic matter formation and its ecophysiological controls ［J］. Nature Communications， 2016， 7. DOI： 10.1038/ncomms13630 . |
| 28 | PROMMER J， WALKER T W N， WANEK W， et al. Increased microbial growth， biomass， and turnover drive soil organic carbon accumulation at higher plant diversity ［J］. Global Change Biology， 2020， 26（2）： 669-681. |
| 29 | del GIORGIO P A， COLE J J. Bacterial growth efficiency in natural aquatic systems［J］. Annual Review of Ecology and Systematics， 1998， 29： 503-541. |
| 30 | CHEN Zhi， YU Guirui. Advances in the soil microbial carbon use efficiency［J］. Acta Ecologica Sinica， 2020， 40（3）： 756-767. |
| 30 | 陈智， 于贵瑞. 土壤微生物碳素利用效率研究进展 ［J］. 生态学报， 2020， 40（3）： 756-767. |
| 31 | PAYNE W J， WIEBE W J. Growth yield and efficiency in chemosynthetic microorganisms ［J］. Annual Review of Microbiology， 1978， 32： 155-183. |
| 32 | ROELS J A. Application of macroscopic principles to microbial metabolism［J］. Biotechnology and Bioengineering， 1980， 22（12）： 2 457-2 514. |
| 33 | GOMMERS P J F， van SCHIE B J， van DIJKEN J P， et al. Biochemical limits to microbial growth yields： an analysis of mixed substrate utilization［J］. Biotechnology and Bioengineering， 1988， 32（1）： 86-94. |
| 34 | CRAWFORD C C， HOBBIE J E， WEBB K L. The utilization of dissolved free amino acids by estuarine microorganisms［J］. Ecology， 1974， 55（3）： 551-563. |
| 35 | RUSSELL J B， COOK G M. Energetics of bacterial growth： balance of anabolic and catabolic reactions ［J］. Microbiological Reviews， 1995， 59（1）： 48-62. |
| 36 | PARSONS T R， STRICKLAND J D H. On the production of particulate organic carbon by heterotrophic processes in sea water［J］. Deep Sea Research （1953）， 1961， 8（3/4）： 211-222. |
| 37 | HOBBIE J E， WRIGHT R T. Competition between planktonic bacteria and algae for organic solutes［M］// Primary productivity in aquatic environments. California： University of California Press， 1966： 175-186. |
| 38 | HOBBIE J E， CRAWFORD C C. Respiration corrections for bacterial uptake of dissolved organic compounds in natural waters ［J］. Limnology and Oceanography， 1969， 14（4）： 528-532. |
| 39 | PAYNE W J. Energy yields and growth of heterotrophs ［J］. Annual Review of Microbiology， 1970， 24： 17-52. |
| 40 | BRANT J B， SULZMAN E W， MYROLD D D. Microbial community utilization of added carbon substrates in response to long-term carbon input manipulation ［J］. Soil Biology and Biochemistry， 2006， 38（8）： 2 219-2 232. |
| 41 | SINSABAUGH R L， FOLLSTAD SHAH J J. Ecoenzymatic stoichiometry and ecological theory［J］. Annual Review of Ecology， Evolution， and Systematics， 2012， 43： 313-343. |
| 42 | CANARINI A， WANEK W， WATZKA M， et al. Quantifying microbial growth and carbon use efficiency in dry soil environments via 18O water vapor equilibration ［J］. Global Change Biology， 2020， 26（9）： 5 333-5 341. |
| 43 | QU L R， WANG C， BAI E. Evaluation of the 18O-H2O incubation method for measurement of soil microbial carbon use efficiency［J］. Soil Biology and Biochemistry， 2020， 145. DOI： 10.1016/j.soilbio.2020.107802 . |
| 44 | SPOHN M， KLAUS K， WANEK W， et al. Microbial carbon use efficiency and biomass turnover times depending on soil depth—implications for carbon cycling ［J］. Soil Biology and Biochemistry， 2016， 96： 74-81. |
| 45 | SPOHN M， P?TSCH E M， EICHORST S A， et al. Soil microbial carbon use efficiency and biomass turnover in a long-term fertilization experiment in a temperate grassland［J］. Soil Biology and Biochemistry， 2016， 97： 168-175. |
| 46 | GEYER K M， DIJKSTRA P， SINSABAUGH R， et al. Clarifying the interpretation of carbon use efficiency in soil through methods comparison［J］. Soil Biology and Biochemistry， 2019， 128： 79-88. |
| 47 | ZIEGLER S E， WHITE P M， WOLF D C， et al. Tracking the fate and recycling of 13C-labeled glucose in soil［J］. Soil Science， 2005， 170（10）： 767-778. |
| 48 | CREAMER C A， JONES D L， BALDOCK J A， et al. Is the fate of glucose-derived carbon more strongly driven by nutrient availability， soil texture， or microbial biomass size？［J］. Soil Biology and Biochemistry， 2016， 103： 201-212. |
| 49 | FREY S D， GUPTA V V S R， ELLIOTT E T， et al. Protozoan grazing affects estimates of carbon utilization efficiency of the soil microbial community［J］. Soil Biology and Biochemistry， 2001， 33（12/13）： 1 759-1 768. |
| 50 | CAI P， HUANG Q， ZHANG X， et al. Adsorption of DNA on clay minerals and various colloidal particles from an Alfisol［J］. Soil Biology and Biochemistry， 2006， 38（3）： 471-476. |
| 51 | LAROWE D E， van CAPPELLEN P. Degradation of natural organic matter： a thermodynamic analysis［J］. Geochimica et Cosmochimica Acta， 2011， 75（8）： 2 030-2 042. |
| 52 | B?LSCHER T， PATERSON E， FREITAG T， et al. Temperature sensitivity of substrate-use efficiency can result from altered microbial physiology without change to community composition［J］. Soil Biology and Biochemistry， 2017， 109： 59-69. |
| 53 | von STOCKAR U， LIU J S. Does microbial life always feed on negative entropy？Thermodynamic analysis of microbial growth［J］. Biochimica et Biophysica Acta （BBA）-Bioenergetics， 1999， 1 412（3）： 191-211. |
| 54 | HANSEN L D， MACFARLANE C， MCKINNON N， et al. Use of calorespirometric ratios， heat per CO2 and heat per O2， to quantify metabolic paths and energetics of growing cells［J］. Thermochimica Acta， 2004， 422（1/2）： 55-61. |
| 55 | DIJKSTRA P， SALPAS E， FAIRBANKS D， et al. High carbon use efficiency in soil microbial communities is related to balanced growth， not storage compound synthesis［J］. Soil Biology and Biochemistry， 2015， 89： 35-43. |
| 56 | DIJKSTRA P， THOMAS S C， HEINRICH P L， et al. Effect of temperature on metabolic activity of intact microbial communities： evidence for altered metabolic pathway activity but not for increased maintenance respiration and reduced carbon use efficiency［J］. Soil Biology and Biochemistry， 2011， 43（10）： 2 023-2 031. |
| 57 | MANZONI S， ?APEK P， MOOSHAMMER M， et al. Optimal metabolic regulation along resource stoichiometry gradients［J］. Ecology Letters， 2017， 20（9）： 1 182-1 191. |
| 58 | SINSABAUGH R L， TURNER B L， TALBOT J M， et al. Stoichiometry of microbial carbon use efficiency in soils ［J］. Ecological Monographs， 2016， 86（2）： 172-189. |
| 59 | HERRON P M， STARK J M， HOLT C， et al. Microbial growth efficiencies across a soil moisture gradient assessed using 13C-acetic acid vapor and 15N-ammonia gas［J］. Soil Biology and Biochemistry， 2009， 41（6）： 1 262-1 269. |
| 60 | SANTRUCKOVA H， PICEK T， TYKVA R， et al. Short-term partitioning of 14C-［U］-glucose in the soil microbial pool under varied aeration status ［J］. Biology and Fertility of Soils， 2004， 40（6）： 386-392. |
| 61 | SAIFUDDIN M， BHATNAGAR J M， SEGRè D， et al. Microbial carbon use efficiency predicted from genome-scale metabolic models［J］. Nature Communications， 2019， 10（1）. DOI：10.1038/s41467-019-11488-z . |
| 62 | FONTAINE S， MARIOTTI A， ABBADIE L. The priming effect of organic matter： a question of microbial competition？［J］. Soil Biology and Biochemistry， 2003， 35（6）： 837-843. |
| 63 | SCHWARTZ E. Characterization of growing microorganisms in soil by stable isotope probing with H2 18O ［J］. Applied and Environmental Microbiology， 2007， 73（8）： 2 541-2 546. |
| 64 | BLAZEWICZ S J， SCHWARTZ E. Dynamics of 18O Incorporation from H2 18O into soil microbial DNA ［J］. Microbial Ecology， 2011， 61（4）： 911-916. |
| 65 | POLD G， DOMEIGNOZ-HORTA L A， DEANGELIS K M. Heavy and wet： the consequences of violating assumptions of measuring soil microbial growth efficiency using the 18O water method ［J］. Elementa-Science of the Anthropocene， 2020， 8（20）： 2-13. |
| 66 | ZHANG Q F， QIN W K， FENG J G， et al. Responses of soil microbial carbon use efficiency to warming： review and prospects［J］. Soil Ecology Letters， 2022， 4（4）： 307-318. |
| 67 | BIRCH H F. The effect of soil drying on humus decomposition and nitrogen availability ［J］. Plant and Soil， 1958， 10（1）： 9-31. |
| 68 | WANG C， QU L R， YANG L M， et al. Large-scale importance of microbial carbon use efficiency and necromass to soil organic carbon［J］. Global Change Biology， 2021， 27（10）： 2 039-2 048. |
| 69 | ZHRAN M， GE T D， TONG Y Y， et al. Assessment of depth-dependent microbial carbon-use efficiency in long-term fertilized paddy soil using an 18O-H2O approach［J］. Land Degradation & Development， 2021， 32（1）： 199-207. |
| 70 | XIE W J， ZHANG Y P， LI J Y， et al. Straw application coupled with N and P supply enhanced microbial biomass， enzymatic activity， and carbon use efficiency in saline soil［J］. Applied Soil Ecology， 2021， 168. DOI：10.1016/j.apsoil.2021.104128 . |
| 71 | XIAO Q， HUANG Y P， WU L， et al. Long-term manuring increases microbial carbon use efficiency and mitigates priming effect via alleviated soil acidification and resource limitation［J］. Biology and Fertility of Soils， 2021， 57（7）： 925-934. |
| 72 | LIAO C， TIAN Q X， LIU F. Nitrogen availability regulates deep soil priming effect by changing microbial metabolic efficiency in a subtropical forest［J］. Journal of Forestry Research， 2021， 32（2）： 713-723. |
| 73 | CHEN L Y， LIU L， MAO C， et al. Nitrogen availability regulates topsoil carbon dynamics after permafrost thaw by altering microbial metabolic efficiency［J］. Nature Communications， 2018， 9（1）： 1-11. |
| 74 | CHEN Y， ZHANG Y J， BAI E， et al. The stimulatory effect of elevated CO2 on soil respiration is unaffected by N addition［J］. Science of the Total Environment， 2022， 813. DOI：10.1016/j.scitotenv.2021.151907 . |
| 75 | KUSKE C R， SINSABAUGH R L， GALLEGOS-GRAVES L V， et al. Simple measurements in a complex system： soil community responses to nitrogen amendment in a Pinus taeda forest ［J］. Ecosphere， 2019， 10（4）. DOI：10.1002/ecs2.2687 . |
| 76 | GUO X W， LUO Z K， SUN O J. Long-term litter type treatments alter soil carbon composition but not microbial carbon utilization in a mixed pine-oak forest［J］.Biogeochemistry， 2021， 152（2/3）： 327-343. |
| 77 | LI J， SANG C P， YANG J Y， et al. Stoichiometric imbalance and microbial community regulate microbial elements use efficiencies under nitrogen addition［J］. Soil Biology and Biochemistry， 2021， 156. DOI：10.1016/j.soilbio.2021.108207 . |
| 78 | SILVA-SáNCHEZ A， SOARES M， ROUSK J. Testing the dependence of microbial growth and carbon use efficiency on nitrogen availability， pH， and organic matter quality［J］. Soil Biology and Biochemistry， 2019， 134： 25-35. |
| 79 | ZIEGLER S E， BILLINGS S A. Soil nitrogen status as a regulator of carbon substrate flows through microbial communities with elevated CO2 ［J］. Journal of Geophysical Research： Biogeosciences， 2011， 116（G1）. DOI：10.1029/2010JG001434 . |
| 80 | RIGGS C E， HOBBIE S E. Mechanisms driving the soil organic matter decomposition response to nitrogen enrichment in grassland soils［J］. Soil Biology and Biochemistry， 2016， 99： 54-65. |
| 81 | WIDDIG M， SCHLEUSS P M， BIEDERMAN L A， et al. Microbial carbon use efficiency in grassland soils subjected to nitrogen and phosphorus additions［J］. Soil Biology and Biochemistry， 2020， 146. DOI：10.1016/j.soilbio.2020.107815 . |
| 82 | GUNDERSEN P， EMMETT B A， KJ?NAAS O J， et al. Impact of nitrogen deposition on nitrogen cycling in forests： a synthesis of NITREX data［J］. Forest Ecology and Management， 1998， 101（1/2/3）： 37-55. |
| 83 | ABER J， MCDOWELL W， NADELHOFFER K， et al. Nitrogen saturation in temperate forest ecosystems：hypotheses revisited ［J］. Bioscience， 1998， 48（11）： 921-934. |
| 84 | ABER J D， NADELHOFFER K J， STEUDLER P， et al. Nitrogen saturation in northern forest ecosystems［J］. BioScience， 1989， 39（6）： 378-386. |
| 85 | LEBAUER D S， TRESEDER K K. Nitrogen limitation of net primary productivity in terrestrial ecosystems is globally distributed ［J］. Ecology， 2008， 89（2）： 371-379. |
| 86 | HICKS L C， YUAN M Y， BRANGARí A， et al. Increased above- and belowground plant input can both trigger microbial nitrogen mining in subarctic tundra soils［J］. Ecosystems， 2022， 25（1）： 105-121. |
| 87 | LI J H， ZHANG R， CHENG B H， et al. Effects of nitrogen and phosphorus additions on decomposition and accumulation of soil organic carbon in alpine meadows on the Tibetan Plateau［J］. Land Degradation & Development， 2021， 32（3）： 1 467-1 477. |
| 88 | LUO R Y， KUZYAKOV Y， LIU D Y， et al. Nutrient addition reduces carbon sequestration in a Tibetan grassland soil： disentangling microbial and physical controls［J］. Soil Biology and Biochemistry， 2020， 144. DOI：10.1016/j.soilbio.2020.107764 . |
| 89 | TANG H M， LI C， WEN L， et al. Microbial carbon source utilization in rice rhizosphere and non-rhizosphere soils in a 34-year fertilized paddy field［J］. Journal of Basic Microbiology， 2020， 60（11/12）： 1 004-1 013. |
| 90 | ZHAO X， LU X Y， YANG J Y， et al. Effects of nitrogen addition on microbial carbon use efficiency of soil aggregates in abandoned grassland on the loess plateau of China［J］. Forests， 2022， 13（2）. DOI：10.3390/f13020276 . |
| 91 | CLEVELAND C C， LIPTZIN D. C∶N∶P stoichiometry in soil： is there a “redfield ratio” for the microbial biomass？ ［J］. Biogeochemistry， 2007， 85（3）： 235-252. |
| 92 | KEELER B L， HOBBIE S E， KELLOGG L E. Effects of long-term nitrogen addition on microbial enzyme activity in eight forested and grassland sites： implications for litter and soil organic matter decomposition ［J］. Ecosystems， 2009， 12（1）： 1-15. |
| 93 | KEUSKAMP J A， FELLER I C， LAANBROEK H J， et al. Short- and long-term effects of nutrient enrichment on microbial exoenzyme activity in mangrove peat ［J］. Soil Biology and Biochemistry， 2015， 81： 38-47. |
| 94 | KHALILI B， OGUNSEITAN O A， GOULDEN M L， et al. Interactive effects of precipitation manipulation and nitrogen addition on soil properties in California grassland and shrubland ［J］. Applied Soil Ecology， 2016， 107： 144-153. |
| 95 | LAGOMARSINO A， MOSCATELLI M C， ANGELIS P D， et al. Labile substrates quality as the main driving force of microbial mineralization activity in a poplar plantation soil under elevated CO2 and nitrogen fertilization［J］. Science of the Total Environment， 2006， 372（1）： 256-265. |
| 96 | JEYASINGH P D， WEIDER L J， STERNER R W. Genetically-based trade-offs in response to stoichiometric food quality influence competition in a keystone aquatic herbivore ［J］. Ecology Letters， 2009， 12（11）： 1 229-1 237. |
| 97 | PERSSON J， FINK P， GOTO A， et al. To be or not to be what you eat： regulation of stoichiometric homeostasis among autotrophs and heterotrophs ［J］. Oikos， 2010， 119（5）： 741-751. |
| 98 | XU X F， THORNTON P E， POST W M. A global analysis of soil microbial biomass carbon， nitrogen and phosphorus in terrestrial ecosystems［J］. Global Ecology and Biogeography， 2013， 22（6）： 737-749. |
| 99 | CHEN Y L， CHEN L Y， PENG Y F， et al. Linking microbial C∶N∶P stoichiometry to microbial community and abiotic factors along a 3500-km grassland transect on the Tibetan Plateau［J］. Global Ecology and Biogeography， 2016， 25（12）： 1 416-1 427. |
| 100 | CHEN R R， SENBAYRAM M， BLAGODATSKY S， et al. Soil C and N availability determine the priming effect： microbial N mining and stoichiometric decomposition theories［J］. Global Change Biology， 2014， 20（7）： 2 356-2 367. |
| 101 | CRAINE J M， MORROW C， FIERER N. Microbial nitrogen limitation increases decomposition ［J］. Ecology， 2007， 88（8）： 2 105-2 113. |
| 102 | RAZANAMALALA K， FANOMEZANA R A， RAZAFIMBELO T， et al. The priming effect generated by stoichiometric decomposition and nutrient mining in cultivated tropical soils： actors and drivers ［J］. Applied Soil Ecology， 2018， 126： 21-33. |
| 103 | SPOHN M. Element cycling as driven by stoichiometric homeostasis of soil microorganisms ［J］. Basic and Applied Ecology， 2016， 17（6）： 471-478. |
| 104 | SOONG J L， FUCHSLUEGER L， MARA?ON-JIMENEZ S， et al. Microbial carbon limitation： the need for integrating microorganisms into our understanding of ecosystem carbon cycling［J］. Global Change Biology， 2020， 26（4）： 1 953-1 961. |
| 105 | CUI Y X， ZHANG Y L， DUAN C J， et al. Ecoenzymatic stoichiometry reveals microbial phosphorus limitation decreases the nitrogen cycling potential of soils in semi-arid agricultural ecosystems［J］. Soil and Tillage Research， 2020， 197. DOI：10.1016/j.still.2019.104463 . |
| 106 | GUO J H， LIU X J， ZHANG Y， et al. Significant acidification in major Chinese Croplands ［J］. Science， 2010， 327（5 968）： 1 008-1 010. |
| 107 | PHOENIX G K， EMMETT B A， BRITTON A J， et al. Impacts of atmospheric nitrogen deposition： responses of multiple plant and soil parameters across contrasting ecosystems in long-term field experiments ［J］. Global Change Biology， 2012， 18（4）： 1 197-1 215. |
| 108 | LUCAS R W， KLAMINDER J， FUTTER M N， et al. A meta-analysis of the effects of nitrogen additions on base cations： implications for plants， soils， and streams ［J］. Forest Ecology and Management， 2011， 262（2）： 95-104. |
| 109 | JONES D L， COOLEDGE E C， HOYLE F C， et al. pH and exchangeable aluminum are major regulators of microbial energy flow and carbon use efficiency in soil microbial communities［J］. Soil Biology and Biochemistry， 2019， 138. DOI：10.1016/j.soilbio.2019.107584 . |
| 110 | MALIK A A， MARTINY J B H， BRODIE E L， et al. Defining trait-based microbial strategies with consequences for soil carbon cycling under climate change［J］. The ISME Journal， 2020， 14（1）： 1-9. |
| 111 | S?DERSTR?M B， B??TH E， LUNDGREN B. Decrease in soil microbial activity and biomasses owing to nitrogen amendments［J］. Canadian Journal of Microbiology， 1983， 29（11）： 1 500-1 506. |
| 112 | NOHRSTEDT H ?， ARNEBRANT K， B??TH E， et al. Changes in carbon content， respiration rate， ATP content， and microbial biomass in nitrogen-fertilized pine forest soils in Sweden［J］. Canadian Journal of Forest Research， 1989， 19（3）： 323-328. |
| 113 | BROADBENT F E. Effect of fertilizer nitrogen on the release of soil nitrogen ［J］. Soil Science Society of America Journal， 1965， 29（6）： 692-696. |
| 114 | B??TH E， LUNDGREN B， S?DERSTR?M B. Effects of nitrogen fertilization on the activity and biomass of fungi and bacteria in a podzolic soil［J］. Zentralblatt Für Bakteriologie Mikrobiologie Und Hygiene： I Abt Originale C： Allgemeine， Angewandte Und ?kologische Mikrobiologie， 1981， 2（1）： 90-98. |
| 115 | MAGILL A H， ABER J D， HENDRICKS J J， et al. Biogeochemical response of forest ecosystems to simulated chronic nitrogen deposition ［J］. Ecological Applications， 1997， 7（2）： 402-415. |
| 116 | ZHANG Yan， QIANG Wei， LUO Ruyi， et al. Effects of nitrogen and phosphorus addition on soil microbial growth， turnover， and carbon use efficiency： a review ［J］. Chinese Journal Applied and Environmental Biology， 2022， 28（2）： 526-534. |
| 116 | 张燕， 强薇， 罗如熠， 等. 氮磷添加对土壤微生物生长、周转及碳利用效率的影响研究进展 ［J］. 应用与环境生物学报， 2022， 28（2）： 526-534. |
| 117 | BAO Hanyang， LI Yang， DENG Xianzhi， et al. Effects of different root exudates and plant litter input on soil microbial enzyme activities and residues in alpine desertified grassland ［J］. Chinese Journal Applied and Environmental Biology， 2022， 29（3）： 546-553. |
| 117 | 包寒阳， 李杨， 邓先智， 等. 根系分泌物和凋落物对高寒沙化草地土壤微生物的影响 ［J］. 应用与环境生物学报， 2022， 29（3）： 546-553. |
| 118 | WANG C， WANG X， PEI G T， et al. Stabilization of microbial residues in soil organic matter after two years of decomposition［J］. Soil Biology and Biochemistry， 2020， 141. DOI：10.1016/j.soilbio.2019.107687 . |
| 119 | WANG X， WANG C， COTRUFO M F， et al. Elevated temperature increases the accumulation of microbial necromass nitrogen in soil via increasing microbial turnover［J］. Global Change Biology， 2020， 26（9）： 5 277-5 289. |
| 120 | DOMEIGNOZ-HORTA L A， POLD G， LIU XJ A， et al. Microbial diversity drives carbon use efficiency in a model soil ［J］. Nature Communications， 2020， 11（1）. DOI：10.1038/s41467-020-17502-z . |
| 121 | ZHAO H， SUN J， XU X L， et al. Stoichiometry of soil microbial biomass carbon and microbial biomass nitrogen in China’s temperate and alpine grasslands［J］. European Journal of Soil Biology， 2017， 83： 1-8. |
| 122 | BONNER M T L， SHOO L P， BRACKIN R， et al. Relationship between microbial composition and substrate use efficiency in a tropical soil［J］. Geoderma， 2018， 315： 96-103. |
| 123 | KEIBLINGER K M， HALL E K， WANEK W， et al. The effect of resource quantity and resource stoichiometry on microbial carbon-use-efficiency［J］. FEMS Microbiology Ecology， 2010， 73（3）： 430-440. |
| 124 | KAISER C， FRANKLIN O， DIECKMANN U， et al. Microbial community dynamics alleviate stoichiometric constraints during litter decay ［J］. Ecology Letters， 2014， 17（6）： 680-690. |
| 125 | LIPSON D A. The complex relationship between microbial growth rate and yield and its implications for ecosystem processes ［J］. Frontiers in Microbiology， 2015， 6. DOI：10.3389/fmicb.2015.00615 . |
| 126 | LI Jingjing. Effects of nitrogen addition on soil carbon and nitrogen mineralization and microbial regulation mechanism in a Pinus tabulaeformis forest ［D］. Yangling： Northwest A & F University， 2020. |
| 126 | 李晶晶. 氮添加对人工油松林土壤碳氮矿化过程及其微生物调控机制的影响 ［D］. 杨凌： 西北农林科技大学， 2020. |
| 127 | FREY S D， KNORR M， PARRENT J L， et al. Chronic nitrogen enrichment affects the structure and function of the soil microbial community in temperate hardwood and pine forests ［J］. Forest Ecology and Management， 2004， 196（1）： 159-171. |
| 128 | LIU L， ZHANG T， GILLIAM F S， et al. Interactive effects of nitrogen and phosphorus on soil microbial communities in a tropical forest［J］. PLoS ONE， 2013， 8（4）. DOI：10.1371/journal.pone.0061188 . |
| 129 | TRESEDER K K. Nitrogen additions and microbial biomass： a meta-analysis of ecosystem studies ［J］. Ecology Letters， 2008， 11（10）： 1 111-1 120. |
| 130 | ZHAO J， WAN S Z， FU S L， et al. Effects of understory removal and nitrogen fertilization on soil microbial communities in Eucalyptus plantations［J］. Forest Ecology and Management， 2013， 310： 80-86. |
| 131 | SIX J， FREY S D， THIET R K， et al. Bacterial and fungal contributions to carbon sequestration in agroecosystems ［J］. Soil Science Society of America Journal， 2006， 70（2）： 555-569. |
| 132 | ALLISON S D， WALLENSTEIN M D， BRADFORD M A. Soil-carbon response to warming dependent on microbial physiology ［J］. Nature Geoscience， 2010， 3（5）： 336-340. |
| 133 | HU J X， HUANG C D， ZHOU S X， et al. Nitrogen addition to soil affects microbial carbon use efficiency： Meta-analysis of similarities and differences in 13C and 18O approaches［J］. Global Change Biology， 2022， 28（16）： 4 977-4 988. |
| 134 | LU X K， MAO Q G， WANG Z H， et al. Long-term nitrogen addition decreases soil carbon mineralization in an N-rich primary tropical forest［J］. Forests， 2021， 12（6）. DOI：10.3390/f12060734 . |
| 135 | LU X K， MO J M， GILLIAM F S， et al. Effects of experimental nitrogen additions on plant diversity in an old-growth tropical forest［J］. Global Change Biology， 2010， 16（10）： 2 688-2 700. |
| 136 | CHEN W B， SU F L， NIE Y X， et al. Divergent responses of soil microbial functional groups to long-term high nitrogen presence in the tropical forests［J］. Science of the Total Environment， 2022， 821. DOI：10.1016/j.scitotenv.2022.153251 . |
| 137 | RILLIG M C， RYO M， LEHMANN A， et al. The role of multiple global change factors in driving soil functions and microbial biodiversity［J］. Science， 2019， 366（6 467）： 886-890. |
| 138 | CRUZ-PAREDES C， TáJMEL D， ROUSK J. Can moisture affect temperature dependences of microbial growth and respiration？［J］. Soil Biology and Biochemistry， 2021， 156. DOI：10.1016/j.soilbio.2021.108223 . |
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