[1]朱万泽,马胜兰,等.土壤微生物碳利用效率研究进展[J].山地学报,2023,(1):1-18.[doi:10.16089/j.cnki.1008-2786.000726]
 ZHU Wanze,MA Shenglan,WANG Wenwu,et al.Research Advances in Soil Microbial Carbon Use Efficiency[J].Mountain Research,2023,(1):1-18.[doi:10.16089/j.cnki.1008-2786.000726]
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土壤微生物碳利用效率研究进展
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《山地学报》[ISSN:1008-2186/CN:51-1516]

卷:
期数:
2023年第1期
页码:
1-18
栏目:
山地环境
出版日期:
2023-01-20

文章信息/Info

Title:
Research Advances in Soil Microbial Carbon Use Efficiency
文章编号:
1008-2786-(2023)1-001-18
作者:
朱万泽1马胜兰1 2王文武1 2李 霞1 2盛哲良1 2
(1.中国科学院、水利部成都山地灾害与环境研究所,成都 610299; 2. 中国科学院大学,北京 100049)
Author(s):
ZHU Wanze1 MA Shenglan1 2 WANG Wenwu1 2 LI Xia1 2 SHENG Zheliang1 2
(1. Institute of Mountain Hazards and Environment, Chinese Academy of Sciences and Ministry of Water Resources, Chengdu 610299, China; 2. University of Chinese Academy of scienecs, Beijing 100049, China)
关键词:
碳利用效率 土壤微生物 测定方法 动态变化 影响因子
Keywords:
carbon use efficiency soil microorganism dynamic variation measurement approach influencing factor
分类号:
S714.3
DOI:
10.16089/j.cnki.1008-2786.000726
文献标志码:
A
摘要:
土壤微生物碳利用效率(CUE)指微生物生长与碳吸收的比率,反映了受微生物群落影响的土壤有机碳代谢过程,是理解和模拟全球变化下土壤碳储存和碳循环的关键生理生态参数。量化土壤微生物CUE有助于理解土壤微生物生物量、土壤潜在碳储量、呼吸碳消耗之间的分异,以及土壤长期碳储存对全球变化的响应。土壤微生物CUE及其对环境变化的响应已受到土壤碳循环、全球变化生态学、陆地生态系统模型等研究的广泛关注。我国土壤微生物CUE研究是近几年才兴起的。本文分析了碳同位素法、氧同位素法、量热呼吸法、代谢通量分析法、化学计量法五种微生物CUE测定方法的优劣及适应性,阐释了土壤微生物CUE随生态系统、植被演替、季节的动态变化特征,剖析了微生物群落组成、底物质量和营养可利用性、温度、土壤pH值、土壤水分、土壤团聚体与质地、土层深度、人为干扰等生物和非生物因子对土壤微生物CUE的影响,并指出了当前土壤微生物CUE研究存在的问题,以及今后关注的重点:(1)加强森林生态系统土壤微生物CUE研究;(2)综合探讨环境和生物多要素交互影响下土壤微生物CUE的响应过程与机制,尤其是全球变化下根系分泌物对土壤微生物CUE及长期碳固持的影响;(3)从生态系统视角探讨土壤微生物CUE;(4)采用不同测定方法估算土壤微生物CUE;(5)探讨不同土层深度微生物CUE及其温度敏感性对长期碳储存影响。
Abstract:
Soil microbial carbon use efficiency(CUE)is a critical physiological and ecological parameter in measuring soil C cycle and stock under the global change scenarios. It is defined usually as the ratio between carbon(C)allocated to growth and C taken up by microorganisms. It expresses the processes of C retention, turnover, soil mineralization, and greenhouse gas emission. CUE serves as a key regulator of microbial biomass turnover and soil C sequestration. Understanding the variation of soil microbial CUE and its influence mechanism in the context of global environmental change is critical for a better understanding of the partitioning of C between microbial biomass, and soil stock potential, and respiration, and the response of long-term C stock in soil to global changes. Soil microbial CUE and its response to environmental changes have received increasing attention from studies on soil carbon cycle, global change ecology, and terrestrial ecosystem models. In this review, it evaluated the advantages and adaptability of five microbial CUE measurement methods including 13C(or 14C)and 18O isotope tracing approaches, calorespirometry, metabolic flux analysis, and stoichiometric modeling; it summarized the dynamic characteristics of soil microbial CUE with ecosystems, vegetation succession and different seasons; it analyzed the effects of the biological and abiotic factors including microbial community composition, substrate quality and nutrient availability, temperature, soil pH, soil moisture, soil aggregates and texture, soil layer depth, and anthropogenic disturbances on soil microbial CUE. According to the overview of CUE, the research prospect should be extended to:(1)Strengthen the soil microbial CUE research of forest ecosystems;(2)Explore the response process and mechanism of soil microbial CUE under the interaction of environmental and biological factors, especially for the effects of root exudates on soil microbial CUE and long-term carbon sequestration under the global changes;(3)Explore the dynamic of soil microbial CUE from microorganism's ecosystem perspective;(4)Cross-compare CUE estimates by integrating different methods to capture different aspects of microbial metabolism and improve our understanding of processes controlling CUE variability;(5)Analyze dynamics of microbial CUE at the different soil layers and the influence of the CUE temperature sensitivity on long-term carbon stock in soil.

参考文献/References:

[1] MANZONI S, TAYLOR P, RICHTER A, et al. Environmental and stoichiometric controls on microbial carbon-use efficiency in soils [J]. New Phytologist, 2012, 196: 79-91. DOI: 10. 111/j.1469-8137.2012.04225.x
[2] 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. DOI: 10.1016/j.soilbio.2018.09.036
[3] QIAO Yang, WANG Jing, LIANG Guopeng, et al. Global variation of soil microbial carbon-use efficiency in relation to growth temperature and substrate supply [J]. Scientific Reports, 2019, 9: 5621. DOI: 10.1038/s41598-019-42145-6
[4] 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: 930-939. DOI: 10.1111/ele.12113
[5] 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. DOI: 10.1016/j.soilbio.2016.01.016
[6] SPOHN M, PÖTSCH 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. DOI: 10.1016/j.soilbio.2016.03.008
[7] FREY S D, LEE J, MELILLO J M, et al. The temperature response of soil microbial efficiency and its feedback to climate [J]. Nature Climate Change, 2013, 3: 395-398. DOI: 10.1038/NCLIMATE1796
[8] TUCKER C L, BELL J, PENDALL E, et al. Does declining carbon-use efficiency explain thermal acclimation of soil respiration with warming? [J]. Global Change Biology, 2013, 19: 252-263. DOI: 10.1111/gcb.12036
[9] ALLISON S D.Modeling adaptation of carbon use efficiency in microbial communities [J]. Frontiers in Microbiology, 2014, 5: 571. DOI: 10.3389/fmicb.2014.00571
[10] HAGERTY S B, GROENIGEN K J, ALLISON S D, et al. Accelerated microbial turnover but constant growth efficiency with warming in soil [J]. Nature Climate Change, 2014, 4: 903-906. DOI: 10.1038/NCLIMATE2361
[11] ADINGO S, RU J R, LIU X L, et al. Variation of soil microbial carbon use efficiency(CUE)and its influence mechanism in the context of global environmental change: A review [J]. Peer J, 2021, 9: e12131. DOI: 10.7717/peerj.12131
[12] SINSABAUGH R L, MOORHEAD D L, XU X F, et al. Plant, microbial and ecosystem carbon use efficiencies interact to stabilize microbial growth as a fraction of gross primary production [J]. New Phytologist, 2017, 214: 1518-1526. DOI: 10.1111/nph.14485
[13] DAVIDSON E A, SAVAGE K E, FINZI A C. A big-microsite framework for soil carbon modeling [J]. Global Change Biology, 2014, 20: 3610-3620. DOI: 10.1111/gcb.12718
[14] MCGEE K M, EATON W D, SHOKRALLA S, et al. Determinants of soil bacterial and fungal community composition toward carbon-use efficiency across primary and secondary forests in a Costa Rican conservation area [J]. Microbial Ecology, 2019, 77: 148-167. DOI: 10.1007/s00248-018-1206-0
[15] GEYER K M, KYKER-SNOWMAN E, GRANDY A S, et al. Microbial carbon use efficiency: Accounting for population, community, and ecosystem-scale controls over the fate of metabolized organic matter [J]. Biogeochemistry, 2016, 127: 173-188. DOI: 10.1007/s10533-016-0191-y
[16] 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. DOI: 10.1890/15-2110.1
[17] HARARUK O, SMITH M J, LUO Y Q. Microbial models with data-driven parameters predict stronger soil carbon responses to climate change [J]. Global Change Biology, 2015, 21: 2439-2453. DOI: 10.1111/gcb.12827
[18] BRADFORD M A, WIEDER W R, BONAN G B, et al. Managing uncertainty in soil carbon feedbacks to climate change [J]. Nature Climate Change, 2016, 6: 751-758. DOI: 10.1038/NCLIMATE3071
[19] LI J W, WANG G S, MAYES M A, et al. Reduced carbon use efficiency and increased microbial turnover with soil warming [J]. Global Change Biology, 2019, 25: 900-910. DOI: 10.1111/gcb.14517
[20] SIMON E, CANARINI A, MARTIN V, et al. Microbial growth and carbon use efficiency show seasonal responses in a multifactorial climate change experiment [J]. Communications Biology, 2020, 3(1): 584-584. DOI: 10.1038/s42003-020-01317-1
[21] 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: 107815. DOI: 10.1016/j.soilbio.2020.107815
[22] WANG G S, POST W M, MAYES M A. Development of microbial-enzyme-mediated decomposition model parameters through steady-state and dynamic analyses [J]. Ecological Applications, 2013, 23(1): 255-272. DOI: 10.2307/23440831
[23] WIEDER W R, GRANDY A S, KALLENBACH C M, et al. Integrating microbial physiology and physio-chemical principles in soils with the microbial-mineral carbon stabilization(MIMICS)model [J]. Biogeosciences, 2014, 11: 3899-3917. DOI: 10.5194/bg-11-3899-2014
[24] 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): 1223. DOI: 10.1038/s41467-017-01116-z
[25] 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: 3591. DOI: 10.1038/s41467-018-05980-1
[26] WIEDER W R, BONAN G B, ALLISON S D. Global soil carbon projections are improved by modelling microbial processes [J]. Nature Climate Change, 2013, 3: 909-912. DOI: 10.1038/NCLIMATE1951
[27] JONES D L, OLIVERA-ARDID S, KLUMPP E, et al. Moisture activation and carbon use efficiency of soil microbial communities along an aridity gradient in the Atacama Desert [J]. Soil Biology and Biochemistry, 2018, 117: 68-71. DOI: 10.1016/j.soilbio.2017.10.026
[28] DAVIDSON E A, JANSSENS I A. Temperature sensitivity of soil carbon decomposition and feedbacks to climate change [J]. Nature, 2006, 440: 165-173. DOI: 10.1038/nature04514
[29] BRADFORD M A, DAVIES C A, FREY S D, et al. Thermal adaptation of soil microbial respiration to elevated temperature [J]. Ecology Letters, 2008, 11: 1316-1327. DOI: 10.1111/j.1461-0248.2008.01251.x
[30] HEIMANN M, REICHSTEIN M. Terrestrial ecosystem carbon dynamics and climate feedbacks [J]. Nature, 2008, 451: 289-292. DOI: 10.1038/nature06591
[31] MILCU A, LUKAC M, SUBKE J A, et al. Biotic carbon feedbacks in a materially closed soil-vegetation-atmosphere system [J]. Nature Climate Change, 2012, 2: 291-294. DOI: 10.1038/NCLIMATE1448
[32] LI J W, WANG G S, ALLISON S D, et al. Soil carbon sensitivity to temperature and carbon use efficiency compared across microbial-ecosystem models of varying complexity [J]. Biogeochemistry, 2014, 119: 67-84. DOI: 10.1007/s10533-013-9948-8
[33] GRAHAM E B, KNELMAN J E, SCHINDLBACHER A. Microbes as engines of ecosystem function: When does community structure enhance predictions of ecosystem processes? [J]. Frontiers in Microbiology, 2016, 7: 214. DOI: 10.3389/fmicb.2016.00214
[34] HAGENBO A, HADDEN D, CLEMMENSEN K E, et al. Carbon use efficiency of mycorrhizal fungal mycelium increases during the growing season but decreases with forest age across a Pinus sylvestris chronosequence [J]. Journal of Ecology, 2019, 107: 2808-2822. DOI: 10.1111/1365-2745.13209
[35] 吴建平, 王思敏, 蔡慕天, 等. 植物与微生物碳利用效率及影响因子研究进展[J]. 生态学报, 2019, 39(20): 7771-7779. [WU Jianping, WANG Simin, CAI Mutian, et al. Review on carbon use efficiency of plants and microbes and its influencing factors [J]. Acta Ecologica Sinica, 2019, 39(20): 7771-7779]DOI: 10.5846/stxb201812072685
[36] COTRUFO M F, SOONG J L, HORTON A J, et al. Formation of soil organic matter via biochemical and physical pathways of litter mass loss [J]. Nature Geoscience, 2015, 8: 776-779. DOI: 10.1038/ngeo2520
[37] YIN L M, CORNEO P E, RICHTER A, et al. Variation in rhizosphere priming and microbial growth and carbon use efficiency caused by wheat genotypes and temperatures [J]. Soil Biology and Biochemistry, 2019, 134: 54-61. DOI: 10.1016/j.soilbio.2019.03.019
[38] 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 and Development, 2021, 32: 199-207. DOI: 10.1002/ldr.3708
[39] FANG Y Y, SINGH B P, COLLINS D, et al. Nutrient supply enhanced wheat residue-carbon mineralization, microbial growth, and microbial carbon-use efficiency when residues were supplied at high rate in contrasting soils [J]. Soil Biology and Biochemistry, 2018, 126: 168-178. DOI: 10.1016/j.soilbio.2018.09.003
[40] LIANG C, AMELUNG W, LEHMANN J, et al. Quantitative assessment of microbial necromass contribution to soil organic matter [J]. Global Change Biology, 2019, 25(11): 3578-3590. DOI: 10.1111/gcb.14781
[41] BARROS N, HANSEN L D, PINEIRO V, et al. Factors influencing the calorespirometric ratios of soil microbial metabolism [J]. Soil Biology and Biochemistry, 2016, 92: 221-229. DOI: 10.1016/j.soilbio.2015.10.007
[42] MANZONI S, CAPEK P, MOOSHAMMER M, et al. Optimal metabolic regulation along resource stoichiometry gradients [J]. Ecology Letters, 2017, 20: 1182-1191. DOI: 10.1111/ele.12815
[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: 107802. DOI: 10.1016/j.soilbio.2020.107802
[44] SCHWARTZ E. Characterization of growing microorganisms in soil by stable isotope probing with H218O [J]. Applied and Environmental Microbiology, 2007, 73: 2541-2546. DOI: 10.1128/AEM.02021-06
[45] BLAZEWICZ S J, SCHWARTZ E. Dynamics of 18O incorporation from H218O into soil microbial DNA [J]. Microbial Ecology, 2011, 61: 911-916. DOI: 10.1007/s00248-011-9826-7
[46] ANDERSON T H, MARTENS R. DNA determinations during growth of soil microbial biomasses [J]. Soil Biology and Biochemistry, 2013, 57: 487-495. DOI: 10.1016/j.soilbio.2012.09.031
[47] 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: 5333-5341. DOI: 10.1111/gcb.15168
[48] 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: 2023-2031. DOI: 10.1016/j.soilbio.2011.05.018
[49] STERNER R W, ELSER J J. Stoichiometry in microbial communities: Dynamics and interactions [M]. Princeton: Princeton University Press, 2002.
[50] CHERIF M, LOREAU M. Stoichiometric constraints on resource use, competitive interactions, and elemental cycling in microbial decomposers [J]. American Naturalist, 2007, 169(6): 709-724. DOI: 10.1086/516844
[51] SINSABAUGH R L, FOLLSTAD SHAH J J. Ecoenzymatic stoichiometry and ecological theory [J]. Annual Review of Ecology, Evolution and Systematics, 2012, 43: 313-343. DOI: 10.1146/annurev-ecolsys-071112-124414
[52] AGUMAS B, BLAGODATSKY S, BALUME I, et al. Microbial carbon use efficiency during plant residue decomposition: Integrating multi-enzyme stoichiometry and C balance approach [J]. Applied Soil Ecology, 2021, 159: 103820. DOI: 10.1016/j.apsoil.2020.103820
[53] 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: 555-569. DOI: 10.2136/sssaj2004.0347
[54] CONANT R T, RYAN M G, ÅGREN G I, et al. Temperature and soil organic matter decomposition rates - synthesis of current knowledge and a way forward [J]. Global Change Biology, 2011, 17: 3392-3404. DOI: 10.1111/j.1365-2486.2011.02496.x
[55] 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. DOI: 10.1111/j.1469-8137.2012.04225.x
[56] COTRUFO M F, WALLENSTEIN M D, BOOT C M, et al. The Microbial Efficiency-Matrix Stabilization(MEMS)framework integrates plant litter decomposition with soil organic matter stabilization: Do labile plant inputs form stable soil organic matter? [J]. Global Change Biology, 2013, 19(4): 988-995. DOI: 10.1111/gcb.12113
[57] FISK M, SANTANGELO S, MINICK K. Carbon mineralization is promoted by phosphorus and reduced by nitrogen addition in the organic horizon of northern hardwood forests [J]. Soil Biology and Biochemistry, 2015, 81: 212-218. DOI: 10.1016/j.soilbio.2014.11.022
[58] LIANG C, SCHIMEL J P, JASTROW J D. The importance of anabolism in microbial control over soil carbon storage [J]. Nature Microbiology, 2017, 2: 17105. DOI: 10.1038/nmicrobiol.2017.105
[59] LIU Weixing, QIAO Chunlian, YANG Sen, et al. Microbial carbon use efficiency and priming effect regulate soil carbon storage under nitrogen deposition by slowing soil organic matter decomposition [J]. Geoderma, 2018, 332: 37-44. DOI: 10.1016/j.geoderma.2018.07.008
[60] POEPLAU C, HELFRICH M, DECHOW R, et al. Increased microbial anabolism contributes to soil carbon sequestration by mineral fertilization in temperate grasslands [J]. Soil Biology and Biochemistry, 2019, 130: 167-176. DOI: 10.1016/j.soilbio.2018.12.019
[61] YE J S, BRADFORD M A, DACAL M. Increasing microbial carbon use efficiency with warming predicts soil heterotrophic respiration globally [J]. Global Change Biology, 2019, 25: 3354-3364. DOI: 10.1111/GCB.14738
[62] KIVLIN S N, WARING B G, AVERILL C, et al. Tradeoffs in microbial carbon allocation may mediate soil carbon storage in future climates [J]. Frontiers in Microbiology, 2013, 4: 261. DOI: 10.3389/fmicb.2013.00261
[63] ALLISON S D, WALLENSTEIN M D, BRADFORD M A. Soil-carbon response to warming dependent on microbial physiology [J]. Nature Geoscience, 2010, 3: 336-340. DOI: 10.1038/NGEO846
[64] 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.[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]DOI: 10.1360/SSTe-2020-0213
[65] 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: 1262-1269. DOI: 10.1016/j.soilbio.2009.03.010
[66] TAKRITI M, WILD B, SCHNECKER J, et al. Soil organic matter quality exerts a stronger control than stoichiometry on microbial substrate use efficiency along a latitudinal transect [J]. Soil Biology and Biochemistry, 2018, 121: 212-220. DOI: 10.1016/j.soilbio.2018.02.022
[67] WALKER T W N, KAISER C, STRASSER F, et al. Microbial temperature sensitivity and biomass change explain soil carbon loss with warming [J]. Nature Climate Change, 2018, 8: 885-889. DOI: 10.1038/s41558-018-0259-x
[68] ZHENG Qing, HU Yuntao, ZHANG Shasha, et al. Growth explains microbial carbon use efficiency across soils differing in land use and geology [J]. Soil Biology and Biochemistry, 2019, 128: 45-55. DOI: 10.1016/j.soilbio.2018.10.006
[69] BÖLSCHER T, WADSÖ L, BÖRJESSON G, et al. Differences in substrate use efficiency: Impacts of microbial community composition, land use management, and substrate complexity [J]. Biology and Fertility of Soils, 2016, 52: 547-559. DOI: 10.1007/s00374-016-1097-5
[70] SOARES M, ROUSK J. Microbial growth and carbon use efficiency in soil: Links to fungal-bacterial dominance, SOC-quality and stoichiometry [J]. Soil Biology and Biochemistry, 2019, 131: 195-205. DOI: 10.1016/j.soilbio.2019.01.010
[71] WANG Simin, CHEN Xiaoyun, LI Debao, et al. Effects of soil organism interactions and temperature on carbon use efficiency in three different forest soils [J]. Soil Ecology Letters, 2021, 3(2): 156-166. DOI: 10.1007/s42832-020-0067-x
[72] OLIVER E E, HOULTON B Z, LIPSON D A. Controls on soil microbial carbon use efficiency over long-term ecosystem development [J]. Biogeochemistry, 2021, 152: 309-325. DOI: 10.1007/s10533-021-00758-y
[73] BRADFORD M A, CROWTHER T W. Carbon use efficiency and storage in terrestrial ecosystems [J]. New Phytologist, 2013, 199: 7-9. DOI: 10.1111/nph.12334
[74] LEE Z M, SCHMIDT T M. Bacterial growth efficiency varies in soils under different land management practices [J]. Soil Biology and Biochemistry, 2014, 69: 282-290. DOI: 10.1016/j.soilbio.2013.11.012
[75] LIPSON D A, MONSON R K, SCHMIDT S K, et al. The trade-off between growth rate and yield in microbial communities and the consequences for under-snow soil respiration in a high elevation coniferous forest [J]. Biogeochemistry, 2009, 95: 23-35. DOI: 10.1007/s10533-008-9252-1
[76] MAYNARD D S, CROWTHER T W, BRADFORD M A. Fungal interactions reduce carbon use efficiency [J]. Ecology Letters, 2017, 20: 1034-1042. DOI: 10.1111/ele.12801
[77] STEINWEG J M, PLANTE A F, CONANT R T, et al. Patterns of substrate utilization during long-term incubations at different temperatures [J]. Soil Biology and Biochemistry, 2008, 40: 2722-2728. DOI: 10.1016/j.soilbio.2008.07.002
[78] 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: 430-440. DOI: 10.1111/j.1574-6941.2010.00912.x
[79] ÖQUIST M G, ERHAGEN B, HAEI M, et al. The effect of temperature and substrate quality on the carbon use efficiency of saprotrophic decomposition [J]. Plant and Soil, 2017, 414: 113-125. DOI: 10.1007/s11104-016-3104-x
[80] 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: G01011. DOI: 10.1029/2010JG001434
[81] DOMEIGNOZ-HORTA L A, POLD G, LIU X J A, et al. Microbial diversity drives carbon use efficiency in a model soil [J]. Nature Communications, 2020, 11: 3684. DOI: 10.1038/s41467-020-17502-z
[82] MALIK A A, CHOWDHURY S, SCHLAGER V, et al. Soil fungal: Bacterial ratios are linked to altered carbon cycling [J]. Frontiers in Microbiology, 2016, 7: 1247. DOI: 10.3389/fmicb.2016.01247
[83] BAILEY V L, SMITH J L, BOLTON H. Fungal-to-bacterial ratios in soils investigated for enhanced C sequestration [J]. Soil Biology and Biochemistry, 2002, 34: 997-1007. DOI: 10.1016/s0038-0717(02)00033-0
[84] ROELS J A. Application of macroscopic principles to microbial metabolism [J]. Biotechnology and Bioengineering, 1980, 22(12): 2457-2514. DOI: 10.1002/bit.260221202
[85] GOMMERS P J F, VAN SCHIE B J, VAN DIJKEN J P, et al. Biochemical limits to microbial growth yields: An analysis of mixed subtrate utilization [J]. Biotechnology and Bioengineering, 1988, 32: 86-94. DOI: 10.1002/bit.260320112
[86] SAIFUDDIN M, BHATNAGAR J M, SEGRE D, et al. Microbial carbon use efficiency predicted from genome-scale metabolic models [J]. Nature Communications, 2019, 10: 3568. DOI: 10.1038/s41467-019-11488-z
[87] ZELLER V, BARDGETT R D, TAPPEINER U. Site and management effects on soil microbial properties of subalpine meadows: A study of land abandonment along a north-south gradient in the European Alps [J]. Soil Biology and Biochemistry, 2001, 33: 639-649. DOI: 10.1016/s0038-0717(00)00208-x
[88] LUIS P, WALTHER G, KELLNER H, et al. Diversity of laccase genes from basidiomycetes in a forest soil [J]. Soil Biology and Biochemistry, 2004, 36: 1025-1036. DOI: 10.1016/j.soilbio.2004.02.017
[89] DE BOER W, FOLMAN L B, SUMMERBELL R C, et al. Living in a fungal world: Impact of fungi on soil bacterial niche development [J]. FEMS Microbiology Reviews, 2005, 29: 795-811. DOI: 10.1016/j.femsre.2004.11.005
[90] TALBOT J M, ALLISON S D, TRESEDER K K. Decomposers in disguise: Mycorrhizal fungi as regulators of soil C dynamics in ecosystems under global change [J]. Functional Ecology, 2008, 22(6): 955-963. DOI: 10.1111/j.1365-2435.2008.01402.x
[91] SINSABAUGH R L. Phenol oxidase, peroxidase and organic matter dynamics of soil [J]. Soil Biology and Biochemistry, 2010, 42: 391-404. DOI: 10.1016/j.soilbio.2009.10.014
[92] EATON W D, ANDERSON C, SAUNDERS E F, et al. The impact of Pentaclethra macroloba on soil microbial nitrogen fixing communities and nutrients within developing secondary forests in the Northern Zone of Costa Rica [J]. Tropical Ecology, 2012, 53(2): 207-214.
[93] HAFICH K, PERKINS E J, HAUGE J B, et al. Implications of land management on soil microbial communities and nutrient cycle dynamics in the lowland tropical forest of northern Costa Rica [J]. Tropical Ecology, 2012, 53(2): 215-224.
[94] KIVLIN S N, HAWKES C V. Tree species, spatial heterogeneity, and seasonality drive soil fungal abundance, richness, and composition in Neotropical rainforests [J]. Environmental Microbiology, 2016, 18: 4662-4673. DOI: 10.1111/1462-2920.13342
[95] HÖGBERG M N, HÖGBERG P. Extramatrical ectomycorrhizal mycelium contributes one-third of microbial biomass and produces, together with associated roots, half the dissolved organic carbon in a forest soil [J]. New Phytologist, 2002, 154: 791-795. DOI: 10.1046/j.1469-8137.2002.00417.x
[96] EATON W D, MCGEE K M, DONNELLY R, et al. Differences in the soil microbial community and carbon-use efficiency following development of Vochysia guatemalensis tree plantations in unproductive pastures in Costa Rica [J]. Restoration Ecology, 2019, 27(6): 1263-1273. DOI: 10.1111/rec.12978/suppinfo
[97] WARDLE D A. The influence of biotic interactions on soil biodiversity [J]. Ecology Letters, 2006, 9: 870-886. DOI: 10.1111/j.1461-0248.2006.00931.x
[98] CROWTHER T W, SOKOL N W, OLDFIELD E E, et al. Environmental stress response limits microbial necromass contributions to soil organic carbon [J]. Soil Biology and Biochemistry, 2015, 85: 153-161. DOI: 10.1016/j.soilbio.2015.03.002
[99] CROWTHER T W, THOMAS S M, MAYNARD D S, et al. Biotic interactions mediate soil microbial feedbacks to climate change [J]. Proceedings of the National Academy of Sciences, 2015, 112: 7033-7038. DOI: 10.1073/pnas.1502956112
[100] STRICKLAND M S, ROUSK J. Considering fungal: Bacterial dominance in soils-methods, controls, and ecosystem implications [J]. Soil Biology and Biochemistry, 2010, 42: 1385-1395. DOI: 10.1016/j.soilbio.2010.05.007
[101] WARING B G, AVERILL C, HAWKES C V. Differences in fungal and bacterial physiology alter soil carbon and nitrogen cycling: Insights from meta-analysis and theoretical models [J]. Ecology Letters, 2013, 16: 887-894. DOI: 10.1111/ele.12125
[102] HERRMANN A M, COUCHENEY E, NUNAN N. Isothermal microcalorimetry provides new insight into terrestrial carbon cycling [J]. Environmental Science and Technology, 2014, 48: 4344-4352. DOI: 10.1021/es403941h
[103] 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. DOI: 10.1016/j.soilbio.2016.04.023
[104] PAUSCH J, KRAMER S, SCHARROBA A, et al. Small but active-pool size does not matter for carbon incorporation in below-ground food webs [J]. Functional Ecology, 2016, 30: 479-489. DOI: 10.1111/1365-2435.12512
[105] 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: 13630. DOI: 10.1038/ncomms13630
[106] THIET R K, FREY S D, SIX J. Do growth yield efficiencies differ between soil microbial communities differing in fungal: Bacterial ratios? Reality check and methodological issues [J]. Soil Biology and Biochemistry, 2006, 38: 837-844. DOI: 10.1016/j.soilbio.2005.07.010
[107] SINSABAUGH R L, FOLLSTAD SHAH J J, FINDLAY S G, et al. Scaling microbial biomass, metabolism and resource supply [J]. Biogeochemistry, 2015, 122: 175-190. DOI: 10.1007/s10533-014-0058-z
[108] ROUSK J, BAATH E. Fungal and bacterial growth in soil with plant materials of different C/N ratios [J]. FEMS Microbiology Ecology, 2007, 62: 258-267. DOI: 10.1111/j.1574-6941.2007.00398.x
[109] LAUBER C L, STRICKLAND M S, BRADFORD M A, et al. The influence of soil properties on the structure of bacterial and fungal communities across land-use types [J]. Soil Biology and Biochemistry, 2008, 40: 2407-2415. DOI: 10.1016/j.soilbio.2008.05.021
[110] HAGERTY S B, ALLISON S D, SCHIMEL J P. Evaluating soil microbial carbon use efficiency explicitly as a function of cellular processes: Implications for measurements and models [J]. Biogeochemistry, 2018, 140: 269-283. DOI: 10.1007/s10533-018-0489-z
[111] MOOSHAMMER M, WANEK W, ZECHMEISTER-BOLTENSTERN S, et al. Stoichiometric imbalances between terrestrial decomposer communities and their resources: Mechanisms and implications of microbial adaptations to their resources [J]. Frontiers in Microbiology, 2014, 5: 22. DOI: 10.3389/fmicb.2014.00022
[112] MEHNAZ K R, CORNEO P E, KEITEL C, et al. Carbon and phosphorus addition effects on microbial carbon use efficiency, soil organic matter priming, gross nitrogen mineralization and nitrous oxide emission from soil [J]. Soil Biology and Biochemistry, 2019, 134: 175-186. DOI: 10.1016/j.soilbio.2019.04.003
[113] BICHARANLOO B, SHIRVAN M B, KEITEL C, et al. Rhizodeposition mediates the effect of nitrogen and phosphorous availability on microbial carbon use efficiency and turnover rate [J]. Soil Biology and Biochemistry, 2020, 142: 107705. DOI: 10.1016/j.soilbio.2020.107705
[114] PEI Junmin, LI Jinquan, MIA Shamim, et al. Biochar aging increased microbial carbon use efficiency but decreased biomass turnover time [J]. Geoderma, 2021, 382: 114710. DOI: 10.1016/j.geoderma.2020.114710
[115] BOSSUYT H, DENEF K, SIX J, et al. Influence of microbial populations and residue quality on aggregate stability [J]. Applied Soil Ecology, 2001, 16: 195-208. DOI: 10.1016/s0929-1393(00)00116-5
[116] MANZONI S, JACKSON R B, TROFYMOW J A, et al. The global stoichiometry of litter nitrogen mineralization [J]. Science, 2008, 321: 684-686. DOI: 10.1126/science.1159792
[117] ZHOU Zhiyong, ZHANG Huan, YUAN Zhen, 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]. Journal of Soils and Sediments, 2020, 20: 352-364. DOI: 10.1007/s11368-019-02423-2
[118] ZECHMEISTER-BOLTENSTERN S, KEIBLINGER K M, MOOSHAMMER M, et al. The application of ecological stoichiometry to plant-microbial-soil organic matter transformations [J]. Ecological Monographs, 2015, 185(2): 133-155. DOI: 10.1890/14-0777.1
[119] SCHIMEL J P, WEINTRAUB M N. The implications of exoenzyme activity on microbial carbon and nitrogen limitation in soil: A theoretical model [J]. Soil Biology and Biochemistry, 2003, 35: 549-563. DOI: 10.1016/s0038-0717(03)00015-4
[120] CRAINE J M, MORROW C, FIERER N. Microbial nitrogen limitation increases decomposition [J]. Ecology, 2007, 88(8): 2105-2113. DOI: 10.2307/27651341
[121] FANG Y Y, SINGH B P, COWIE A, et al. Balancing nutrient stoichiometry facilitates the fate of wheat residue-carbon in physically defined soil organic matter fractions [J]. Geoderma, 2019, 354: 113883. DOI: 10.1016/j.geoderma.2019.113883
[122] WEI Xiaomeng, ZHU Zhenke, LIU Yi, et al. C: N: P stoichiometry regulates soil organic carbon mineralization and concomitant shifts in microbial community composition in paddy soil [J]. Biology and Fertility of Soils, 2020, 56: 1093-1107. DOI: 10.1007/s00374-020-01468-7
[123] KYASCHENKO J, CLEMMENSEN K E, HAGENBO A, et al. Shift in fungal communities and associated enzyme activities along an age gradient of managed Pinus sylvestris stands [J]. The ISME Journal, 2017, 11: 863-874. DOI: 10.1038/ismej.2016.184
[124] MANZONI S, PORPORATO A. Soil carbon and nitrogen mineralization: Theory and models across scales [J]. Soil Biology and Biochemistry, 2009, 41: 1355-1379. DOI: 10.1016/j.soilbio.2009.02.031
[125] ÅGREN G I, BOSATTA N. Theoretical analysis of the long-term dynamics of carbon and nitrogen in soils [J]. Ecology, 1987, 68(5): 1181-1189. DOI: 10.2307/1939202
[126] ROLLER B R K, SCHMIDT T M. The physiology and ecological implications of efficient growth [J]. The ISME Journal, 2015, 9: 1481-1487. DOI: 10.1038/ismej.2014.235
[127] KHAN K S, JOERGENSEN R G. Stoichiometry of the soil microbial biomass in response to amendments with varying C/N/P/S ratios [J]. Biology and Fertility of Soils, 2019, 55: 265-274. DOI: 10.1007/s00374-019-01346-x
[128] SILVA-SANCHEZ 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. DOI: 10.1016/j.soilbio.2019.03.008
[129] FANG Y Y, NAZARIES L, SINGH B K, et al. Microbial mechanisms of carbon priming effects revealed during the interaction of crop residue and nutrient inputs in contrasting soils [J]. Global Change Biology, 2018, 24: 2775-2790. DOI: 10.1111/gcb.14154
[130] LI Tianpeng, WANG Ruzhen, CAI Jiangping, et al. Enhanced carbon acquisition and use efficiency alleviate microbial carbon relative to nitrogen limitation under soil acidification [J]. Ecological Processes, 2021, 10(1): 32. DOI: 10.1186/s13717-021-00309-1
[131] 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: 107764. DOI: 10.1016/j.soilbio.2020.107764
[132] 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: 107584. DOI: 10.1016/j.soilbio.2019.107584
[133] FIERER N, BRADFORD M A, JACKSON R B. Toward an ecological classification of soil bacteria [J]. Ecology, 2007, 88(6): 1354-1364. DOI: 10.2307/27651243
[134] ELSER J J, DOBBERFUHL D R, MACKAY N A, et al. Organism size, life history, and N:P stoichiometry [J]. Bioscience, 1996, 46(9): 674-684. DOI: 10.2307/1312897
[135] ELSER J J, STERNER R W, GOROKHOVA E, et al. Biological stoichiometry from genes to ecosystems [J]. Ecology Letters, 2000, 3: 540-550. DOI: 10.1111/j.1461-0248.2000.00185.x
[136] FINN D, PAGE K, CATTON K, et al. Effect of added nitrogen on plant litter decomposition depends on initial soil carbon and nitrogen stoichiometry [J]. Soil Biology and Biochemistry, 2015, 91: 160-168. DOI: 10.1016/j.soilbio.2015.09.001
[137] XIAO Qiong, HUANG Yaping, WU Lei, 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. DOI: 10.1007/s00374-021-01583-z
[138] MIAO Yuncai, NIU Yuhui, LUO Ruyi, et al. Lower microbial carbon use efficiency reduces cellulose-derived carbon retention in soils amended with compost versus mineral fertilizers [J]. Soil Biology and Biochemistry, 2021, 156: 108227. DOI: 10.1016/j.soilbio.2021.108227
[139] LI J Q, YAN D, PENDALL E, et al. Depth dependence of soil carbon temperature sensitivity across Tibetan permafrost regions [J]. Soil Biology and Biochemistry, 2018, 126: 82-90. DOI: 10.1016/j.soilbio.2018.08.015
[140] SCHINDLBACHER A, SCHNECKER J, TAKRITI M, et al. Microbial physiology and soil CO2 efflux after 9 years of soil warming in a temperate forest - no indications for thermal adaptations [J]. Global Change Biology, 2015, 21: 4265-4277. DOI: 10.1111/gcb.12996
[141] WANG Chao, QU Lingrui, YANG Liuming, et al. Large-scale importance of microbial carbon use efficiency and necromass to soil organic carbon [J]. Global Change Biology, 2021, 27: 2039-2048. DOI: 10.1111/gcb.15550
[142] KIRSCHBAUM M U F. The temperature dependence of soil organic matter decomposition, and the effect of glo

备注/Memo

备注/Memo:
收稿日期(Received date): 2022-09-20; 改回日期(Accepted date): 2023-02-10
基金项目(Foundation item): 四川省环境治理与生态保护重大科技专项(2018SZDZX0031); 中科院成都山地所“一三五”方向性项目(SDS-135-1707)[key Environmental Protection and Ecological Improvement Program of Sichuan Province(2018SZDZX0031); “One-Three-Five” Directional Project of Chengdu Institute of Mountain Hazards and Environment, CAS(SDS-135-1707)]
作者简介(Biography): 朱万泽(1965-),男,四川大竹人,博士,研究员,研究方向:森林生态学、经济林。[ZHU Wanze(1965-), male, born in Dazhu, Sichuan province, Ph. D., professor of research, research on forest ecology and cash forest] E-mail: wzzhu@imde.ac.cn

更新日期/Last Update: 2023-01-30