土壤增温对亚热带杉木幼树不同深度土壤微生物胞外酶活性的影响
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摘要
土壤微生物胞外酶可有效反映气候变暖对土壤微生物功能和土壤有机质分解的影响.目前关于气候变暖对土壤微生物胞外酶活性(EEAs)影响的相关研究主要关注有机碳含量较丰富的表层土壤(0～20 cm),而对深层土壤(>20 cm)EEAs的研究仍较缺乏.因此,本研究关注土壤增温对亚热带不同深度(0～10 cm、10～20 cm、20～40 cm和40～60 cm)EEAs的影响及主要调控因素,其中微生物胞外酶包括参与碳循环的β-葡萄糖苷酶(BG)、纤维二糖水解酶(CBH)、酚氧化酶(PHO)和过氧化物氧化酶(PEO).结果表明:土壤增温提高了0～10 cm和10～20 cm土壤所有胞外酶的活性(18%～69%).在20 cm以下的深层土壤中,土壤增温仅显著提高了20～40 cm的PHO(10%),而对其余胞外酶的活性无显著影响或有一定的抑制作用(13%～31%).冗余分析(RDA)结果表明:在微生物可利用有机碳较丰富的表层土壤中,铵态氮(NH_4~+-N)和土壤含水率(M)是调控EEAs的主要因素,增温增强了微生物与植物之间的养分竞争,因而提高EEAs以获取微生物所需的养分NH_4~+-N;而在微生物底物有效性较低的深层土壤中,EEAs主要受可溶性有机质(可溶性有机碳和可溶性有机氮)和微生物生物量(MBC)的影响,增温提高深层土壤可溶性有机质的含量,为微生物提供更多的底物,减少微生物对EEAs的需求,进而降低EEAs.本研究发现,不同深度EEAs对土壤增温具有不同响应,且土壤增温条件下表层和深层土壤的EEAs具有明显不同的调控因素.因此,加强不同深度土壤微生物的研究对于准确评估生态系统碳循环对全球变暖的响应具有重要意义.
Extracellular enzyme activitie(EEAs) are a sensitive indicator of microbial function and soil organic matter decomposition in response to climate warming. Up to now, most studies of climate warming and their effects on EEAs have been restricted on the relatively carbon rich topsoil(the upper 20 cm of the soil), whereas little is known about EEAs in subsoil(below 30 cm depth). This study focused on the responses of EEAs to soil warming in a subtropical forest at depths of 0-10 cm, 10-20 cm, 20-40 cm and 40-60 cm. The examined extracellular enzymes included β-glucosidase(BG), cellobiohydrolase(CBH), phenoloxidase(PHO) and peroxidase(PEO), all being involved in the C-cycle. The results showed that, 1) warming significantly increased all EEAs(18%-69%) at the depth of 0-10 cm and 10-20 cm. Below the depth of 20 cm, warming did no affect or suppressed EEAs(13%-31%), except increasing PHO(10%) at 20-40 cm. 2) Results from the redundancy analysis showed that the EEAs were mainly driven by ammonium nitrogen(NH_4~+-N) and soil moisture(M) in organic carbon rich topsoil. Warming enhanced nutrient competition between soil microorganisms and plants. Thus, it increased EEAs to meet NH_4~+-N demands of microorganisms. In subsoil with relatively low substrate availability, the EEAs were dominated by dissolved organic matter and microbial biomass(MBC). Warming increased dissolved organic matter and thus provided more substrates for microorganisms, which relieved the dependence of microbes on EEAs. Consequently, warming diminished EEAs in subsoils. Our results suggested that EEAs at the four depths showed different responses to warming. In addition, environmental factors accounting for the variances in EEAs under soil warming condition were different at topsoil and subsoil. Paying more attention to microbes at different soil depths has important implications to precisely predict ecosystem C cycling in response to global warming.
Extracellular enzyme activitie(EEAs) are a sensitive indicator of microbial function and soil organic matter decomposition in response to climate warming. Up to now, most studies of climate warming and their effects on EEAs have been restricted on the relatively carbon rich topsoil(the upper 20 cm of the soil), whereas little is known about EEAs in subsoil(below 30 cm depth). This study focused on the responses of EEAs to soil warming in a subtropical forest at depths of 0-10 cm, 10-20 cm, 20-40 cm and 40-60 cm. The examined extracellular enzymes included β-glucosidase(BG), cellobiohydrolase(CBH), phenoloxidase(PHO) and peroxidase(PEO), all being involved in the C-cycle. The results showed that, 1) warming significantly increased all EEAs(18%-69%) at the depth of 0-10 cm and 10-20 cm. Below the depth of 20 cm, warming did no affect or suppressed EEAs(13%-31%), except increasing PHO(10%) at 20-40 cm. 2) Results from the redundancy analysis showed that the EEAs were mainly driven by ammonium nitrogen(NH_4~+-N) and soil moisture(M) in organic carbon rich topsoil. Warming enhanced nutrient competition between soil microorganisms and plants. Thus, it increased EEAs to meet NH_4~+-N demands of microorganisms. In subsoil with relatively low substrate availability, the EEAs were dominated by dissolved organic matter and microbial biomass(MBC). Warming increased dissolved organic matter and thus provided more substrates for microorganisms, which relieved the dependence of microbes on EEAs. Consequently, warming diminished EEAs in subsoils. Our results suggested that EEAs at the four depths showed different responses to warming. In addition, environmental factors accounting for the variances in EEAs under soil warming condition were different at topsoil and subsoil. Paying more attention to microbes at different soil depths has important implications to precisely predict ecosystem C cycling in response to global warming.
引文
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[14] Eusterhues K, Rumpel C, K?gel-Knabner I. Composition and radiocarbon age of HF-resistant soil organic matter in a Podzol and a Cambisol. Organic Geochemistry, 2007, 38: 1356-1372
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[17] Allison SD. Cheaters, diffusion and nutrients constrain decomposition by microbial enzymes in spatially structured environments. Ecology Letters, 2005, 8: 626-635
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[19] Lewis SL, Lloyd J, Sitch S, et al. Changing ecology of tropical forests: Evidence and drivers. Annual Review of Ecology, Evolution and Systematics, 2009, 40: 529-549
[20] Cox PM, Pearson D, Booth BB, et al. Sensitivity of tropical carbon to climate change constrained by carbon dioxide variability. Nature, 2013, 494: 341
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[22] Cavaleri MA, Reed SC, Smith WK, et al. Urgent need for warming experiments in tropical forests. Global Change Biology, 2015, 21: 2111-2121
[23] Piao SL, Fang JY, Ciais P, et al. The carbon balance of terrestrial ecosystems in China. Nature, 2009, 458: 1009-1013
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[26] Scott-Denton LE, Rosenstiel TN, Monson RK. Differential controls by climate and substrate over the heterotrophic and rhizospheric components of soil respiration. Global Change Biology, 2006, 12: 205-216
[27] Xu Z-F (徐振锋), Tang Z (唐正), Wan C (万川), et al. Effects of simulated warming on soil enzyme activities in two subalpine coniferous forests in west Sichuan. Chinese Journal of Applied Ecology (应用生态学报), 2010, 21(11): 2727-2733 (in Chinese)
[28] Sardans J, Peňuelas J. Drought decreases soil enzyme activity in a Mediterranean Quercus ilex L. forest. Soil Biology and Biochemistry, 2005, 37: 455-461
[29] Wallenstein MD, McMahon SK, Schimel JP. Seasonal variation in enzyme activities and temperature sensitivities in Arctic tundra soils. Global Change Biology, 2009, 15: 1631-1639
[30] Zhang QF, Xie JS, Lyu MK, et al. Short-term effects of soil warming and nitrogen addition on the N:P stoichiome-try of Cunninghamia lanceolata in subtropical regions. Plant and Soil, 2017, 411: 395-407
[31] Bell TH, Henry HAL. Fine scale variability in soil extracellular enzyme activity is insensitive to rain events and temperature in a mesic system. Pedobiologia, 2011, 54: 141-146
[32] Liu WX, Zhang Z, Wan SQ. Predominant role of water in regulating soil and microbial respiration and their responses to climate change in a semiarid grassland. Global Change Biology, 2009, 15: 184-195
[33] Zhang NL, Wan SQ, Guo JX, et al. Precipitation modifies the effects of warming and nitrogen addition on soil microbial communities in northern Chinese grasslands. Soil Biology and Biochemistry, 2015, 89: 12-23
[34] Llorens L, Pe?Uelas J, Estiarte M, et al. Contrasting growth changes in two dominant species of a Mediterranean shrubland submitted to experimental drought and warming. Annals of Botany, 2004, 94: 843-853
[35] Allison SD, Wallenstein MD, Bradford MA. Soil-carbon response to warming dependent on microbial physiology. Nature Geoscience, 2010, 3: 336-340
[36] Carlyle CN, Fraser LH, Turkington R. Tracking soil temperature and moisture in a multi-factor climate experi-ment in temperate grassland: Do climate manipulation methods produce their intended effects? Ecosystems, 2011, 14: 489-502
[37] Wallenstein MD, Haddix ML, Lee DD, et al. A litter-slurry technique elucidates the key role of enzyme production and microbial dynamics in temperature sensitivity of organic matter decomposition. Soil Biology and Biochemistry, 2012, 47: 18-26
[38] Wallenstein MD, Allison SD, Ernakovich J, et al. Controls on the Temperature Sensitivity of Soil Enzymes: A Key Driver of In Situ Enzyme Activity Rates. Berlin: Springer, 2011: 245-258
[39] Mikutta R, Mikutta C, Kalbitz K, et al. Biodegradation of forest floor organic matter bound to minerals via different binding mechanisms. Geochimica et Cosmochimica Acta, 2007, 71: 2569-2590
[40] Conant RT, Ryan MG, ?gren GI, et al. Temperature and soil organic matter decomposition rates: Synthesis of current knowledge and a way forward. Global Change Biology, 2011, 17: 3392-3404
[41] Sinsabaugh RL, Lauber CL, Weintraub MN, et al. Stoichiometry of soil enzyme activity at global scale. Ecology Letters, 2008, 11: 1252-1264
[42] Salom? CM, Nunan N, Pouteau VR, et al. Carbon dynamics in topsoil and in subsoil may be controlled by different regulatory mechanisms. Global Change Biology, 2010, 16: 416-426
[43] Hu J-W (胡举伟), Zhu W-X (朱文旭), Zhang H-H (张会慧), et al. Effects of mulberry/soybean intercropping on the plant growth and rhizosphere soil microbial number and enzyme activities. Chinese Journal of Applied Ecology (应用生态学报), 2013, 24(5): 1423-1427 (in Chinese)
[44] Henry HAL, Juarez JD, Field CB, et al. Interactive effects of elevated CO2, N deposition and climate change on extracellular enzyme activity and soil density fractionation in a California annual grassland. Global Change Biology, 2005, 11: 1808-1815
[45] Liu YC, Liu SR, Wan SQ, et al. Effects of experimental throughfall reduction and soil warming on fine root biomass and its decomposition in a warm temperate oak forest. Science of the Total Environment, 2017, 574: 1448-1455
[46] Guo Z-M (郭志明), Zhang X-Y (张心昱), Li D-D (李丹丹), et al. Characteristics of soil organic carbon and related exo-enzyme activities at different altitudes in temperate forests. Chinese Journal of Applied Ecology (应用生态学报), 2017, 28(9): 2888-2896 (in Chinese)
[47] Schimel J, Balser TC, Wallenstein M. Microbial stress-response physiology and its implications for ecosystem function. Ecology, 2007, 88: 1386-1394
[48] Freeman C, Ostle N, Kang H. An enzymic ‘latch’ on a global carbon store. Nature, 2001, 409: 149
[49] Fontaine S, Barot S, Barré P, et al. Stability of organic carbon in deep soil layers controlled by fresh carbon supply. Nature, 2007, 450: 277-280
[50] Allison SD, Jastrow JD. Activities of extracellular enzymes in physically isolated fractions of restored grassland soils. Soil Biology and Biochemistry, 2006, 38: 3245-3256
[51] Xiong DC, Yang ZJ, Chen GS, et al. Interactive effects of warming and nitrogen addition on fine root dynamics of a young subtropical plantation. Soil Biology and Biochemistry, 2018, 123: 180-189
[2] Horwath WR. Carbon Cycling and Formation of Soil Organic Matter. Dordrecht: Springer, 2008: 91-97
[3] Sinsabaugh RL, Hill BH, Follstad Shah JJ. Ecoenzyma-tic stoichiometry of microbial organic nutrient acquisition in soil and sediment. Nature, 2009, 462: 795
[4] Allison SD, Treseder KK. Warming and drying suppress microbial activity and carbon cycling in boreal forest soils. Global Change Biology, 2008, 14: 2898-2909
[5] Zhou XQ, Chen CG, Wang YF, et al. Warming and increased precipitation have differential effects on soil extracellular enzyme activities in a temperate grassland. Science of the Total Environment, 2013, 444: 552-558
[6] Souza RC, Solly EF, Dawes MA, et al. Responses of soil extracellular enzyme activities to experimental warming and CO2 enrichment at the alpine treeline. Plant and Soil, 2017, 416: 527-537
[7] Janzen H. Soil carbon: A measure of ecosystem response in a changing world? Canadian Journal of Soil Science, 2005, 85: 467-480
[8] Jobbágy EG, Jackson RB. The vertical distribution of soil organic carbon and its relation to climate and vegetation. Ecological Applications, 2000, 10: 423-436
[9] Blume E, Bischoff M, Reichert J, et al. Surface and subsurface microbial biomass, community structure and metabolic activity as a function of soil depth and season. Applied Soil Ecology, 2002, 20: 171-181
[10] Gelsomino A, Azzellino A. Multivariate analysis of soils: Microbial biomass, metabolic activity, and bacterial-community structure and their relationships with soil depth and type. Journal of Plant Nutrition and Soil Science, 2011, 174: 381-394
[11] Fang C, Moncrieff JB. The variation of soil microbial respiration with depth in relation to soil carbon composition. Plant and Soil, 2005, 268: 243-253
[12] Lützow MV, K?gel-Knabner I, Ekschmitt K, et al. Stabilization of organic matter in temperate soils: Mechanisms and their relevance under different soil conditions: A review. European Journal of Soil Science, 2006, 57: 426-445
[13] Rumpel C, K?gel-Knabner I. Deep soil organic matter: A key but poorly understood component of terrestrial C cycle. Plant and Soil, 2011, 338: 143-158
[14] Eusterhues K, Rumpel C, K?gel-Knabner I. Composition and radiocarbon age of HF-resistant soil organic matter in a Podzol and a Cambisol. Organic Geochemistry, 2007, 38: 1356-1372
[15] Rumpel C, Chaplot V, Chabbi A, et al. Stabilisation of HF soluble and HCl resistant organic matter in sloping tropical soils under slash and burn agriculture. Geoderma, 2008, 145: 347-354
[16] Rasmussen C, Torn MS, Southard RJ. Mineral assemblage and aggregates control carbon dynamics in a California conifer forest. Soil Science Society of America Journal, 2005, 69: 1711-1721
[17] Allison SD. Cheaters, diffusion and nutrients constrain decomposition by microbial enzymes in spatially structured environments. Ecology Letters, 2005, 8: 626-635
[18] Tarnocai C, Canadell JG, Schuur EAG, et al. Soil organic carbon pools in the northern circumpolar permafrost region. Global Biogeochemical Cycles, 2009, 23: GB2023
[19] Lewis SL, Lloyd J, Sitch S, et al. Changing ecology of tropical forests: Evidence and drivers. Annual Review of Ecology, Evolution and Systematics, 2009, 40: 529-549
[20] Cox PM, Pearson D, Booth BB, et al. Sensitivity of tropical carbon to climate change constrained by carbon dioxide variability. Nature, 2013, 494: 341
[21] Randerson JT. Global warming and tropical carbon. Nature, 2013, 494: 319
[22] Cavaleri MA, Reed SC, Smith WK, et al. Urgent need for warming experiments in tropical forests. Global Change Biology, 2015, 21: 2111-2121
[23] Piao SL, Fang JY, Ciais P, et al. The carbon balance of terrestrial ecosystems in China. Nature, 2009, 458: 1009-1013
[24] Food and Agriculture Organization of the United Nations. Global forest resources assessment 2010: Progress towards sustainable forest management. Rome: FAO, 2010: 163
[25] Zhang X (章宪), Liu X-F (刘小飞), Chen S-D (陈仕东), et al. Effects of soil warming on the tempera-ture of soil in different depths. Journal of Subtropical Resources and Environment (亚热带资源与环境学报), 2014, 9(1): 89-91 (in Chinese)
[26] Scott-Denton LE, Rosenstiel TN, Monson RK. Differential controls by climate and substrate over the heterotrophic and rhizospheric components of soil respiration. Global Change Biology, 2006, 12: 205-216
[27] Xu Z-F (徐振锋), Tang Z (唐正), Wan C (万川), et al. Effects of simulated warming on soil enzyme activities in two subalpine coniferous forests in west Sichuan. Chinese Journal of Applied Ecology (应用生态学报), 2010, 21(11): 2727-2733 (in Chinese)
[28] Sardans J, Peňuelas J. Drought decreases soil enzyme activity in a Mediterranean Quercus ilex L. forest. Soil Biology and Biochemistry, 2005, 37: 455-461
[29] Wallenstein MD, McMahon SK, Schimel JP. Seasonal variation in enzyme activities and temperature sensitivities in Arctic tundra soils. Global Change Biology, 2009, 15: 1631-1639
[30] Zhang QF, Xie JS, Lyu MK, et al. Short-term effects of soil warming and nitrogen addition on the N:P stoichiome-try of Cunninghamia lanceolata in subtropical regions. Plant and Soil, 2017, 411: 395-407
[31] Bell TH, Henry HAL. Fine scale variability in soil extracellular enzyme activity is insensitive to rain events and temperature in a mesic system. Pedobiologia, 2011, 54: 141-146
[32] Liu WX, Zhang Z, Wan SQ. Predominant role of water in regulating soil and microbial respiration and their responses to climate change in a semiarid grassland. Global Change Biology, 2009, 15: 184-195
[33] Zhang NL, Wan SQ, Guo JX, et al. Precipitation modifies the effects of warming and nitrogen addition on soil microbial communities in northern Chinese grasslands. Soil Biology and Biochemistry, 2015, 89: 12-23
[34] Llorens L, Pe?Uelas J, Estiarte M, et al. Contrasting growth changes in two dominant species of a Mediterranean shrubland submitted to experimental drought and warming. Annals of Botany, 2004, 94: 843-853
[35] Allison SD, Wallenstein MD, Bradford MA. Soil-carbon response to warming dependent on microbial physiology. Nature Geoscience, 2010, 3: 336-340
[36] Carlyle CN, Fraser LH, Turkington R. Tracking soil temperature and moisture in a multi-factor climate experi-ment in temperate grassland: Do climate manipulation methods produce their intended effects? Ecosystems, 2011, 14: 489-502
[37] Wallenstein MD, Haddix ML, Lee DD, et al. A litter-slurry technique elucidates the key role of enzyme production and microbial dynamics in temperature sensitivity of organic matter decomposition. Soil Biology and Biochemistry, 2012, 47: 18-26
[38] Wallenstein MD, Allison SD, Ernakovich J, et al. Controls on the Temperature Sensitivity of Soil Enzymes: A Key Driver of In Situ Enzyme Activity Rates. Berlin: Springer, 2011: 245-258
[39] Mikutta R, Mikutta C, Kalbitz K, et al. Biodegradation of forest floor organic matter bound to minerals via different binding mechanisms. Geochimica et Cosmochimica Acta, 2007, 71: 2569-2590
[40] Conant RT, Ryan MG, ?gren GI, et al. Temperature and soil organic matter decomposition rates: Synthesis of current knowledge and a way forward. Global Change Biology, 2011, 17: 3392-3404
[41] Sinsabaugh RL, Lauber CL, Weintraub MN, et al. Stoichiometry of soil enzyme activity at global scale. Ecology Letters, 2008, 11: 1252-1264
[42] Salom? CM, Nunan N, Pouteau VR, et al. Carbon dynamics in topsoil and in subsoil may be controlled by different regulatory mechanisms. Global Change Biology, 2010, 16: 416-426
[43] Hu J-W (胡举伟), Zhu W-X (朱文旭), Zhang H-H (张会慧), et al. Effects of mulberry/soybean intercropping on the plant growth and rhizosphere soil microbial number and enzyme activities. Chinese Journal of Applied Ecology (应用生态学报), 2013, 24(5): 1423-1427 (in Chinese)
[44] Henry HAL, Juarez JD, Field CB, et al. Interactive effects of elevated CO2, N deposition and climate change on extracellular enzyme activity and soil density fractionation in a California annual grassland. Global Change Biology, 2005, 11: 1808-1815
[45] Liu YC, Liu SR, Wan SQ, et al. Effects of experimental throughfall reduction and soil warming on fine root biomass and its decomposition in a warm temperate oak forest. Science of the Total Environment, 2017, 574: 1448-1455
[46] Guo Z-M (郭志明), Zhang X-Y (张心昱), Li D-D (李丹丹), et al. Characteristics of soil organic carbon and related exo-enzyme activities at different altitudes in temperate forests. Chinese Journal of Applied Ecology (应用生态学报), 2017, 28(9): 2888-2896 (in Chinese)
[47] Schimel J, Balser TC, Wallenstein M. Microbial stress-response physiology and its implications for ecosystem function. Ecology, 2007, 88: 1386-1394
[48] Freeman C, Ostle N, Kang H. An enzymic ‘latch’ on a global carbon store. Nature, 2001, 409: 149
[49] Fontaine S, Barot S, Barré P, et al. Stability of organic carbon in deep soil layers controlled by fresh carbon supply. Nature, 2007, 450: 277-280
[50] Allison SD, Jastrow JD. Activities of extracellular enzymes in physically isolated fractions of restored grassland soils. Soil Biology and Biochemistry, 2006, 38: 3245-3256
[51] Xiong DC, Yang ZJ, Chen GS, et al. Interactive effects of warming and nitrogen addition on fine root dynamics of a young subtropical plantation. Soil Biology and Biochemistry, 2018, 123: 180-189