微生物碳氮不平衡影响罗浮栲林土壤微生物氮利用效率对氮富集的响应

doi:10.17521/cjpe.2024.0350

植物生态学报 ›› 2026, Vol. 50 ›› Issue (1): 34-44.DOI: 10.17521/cjpe.2024.0350

微生物碳氮不平衡影响罗浮栲林土壤微生物氮利用效率对氮富集的响应

皮惠之¹, 张秋芳¹^,^*(), 孙浩¹, 曾泉鑫¹, 彭园珍¹, 元晓春², 徐建国³, 陈岳民¹

¹ 福建师范大学地理科学学院, 福建省亚热带资源与环境重点实验室, 福州 350117
² 武夷学院旅游学院, 福建武夷山 354300
³ 福建戴云山国家级自然保护区管理局, 福建泉州 362500

收稿日期:2024-10-08 接受日期:2025-01-14 出版日期:2026-01-20 发布日期:2026-02-13
通讯作者: *张秋芳(qiufangzh@fjnu.edu.cn)
基金资助:
国家自然科学基金(32471684);国家自然科学基金(32371846);福建省自然科学基金(2024J01130937);福建省自然科学基金(2023R1002002)

Microbial carbon-nitrogen imbalance affects the response of microbial nitrogen use efficiency to nitrogen enrichment in Castanopsis faberi forest soils

PI Hui-Zhi¹, ZHANG Qiu-Fang¹^,^*(), SUN Hao¹, ZENG Quan-Xin¹, PENG Yuan-Zhen¹, YUAN Xiao-Chun², XU Jian-Guo³, CHEN Yue-Min¹

¹ School of Geographical Science, Fujian Provincial Key Laboratory for Subtropical Resources and Environment, Fujian Normal University, Fuzhou 350117, China
² College of Tourism, Wuyi University, Wuyishan, Fujian 354300, China
³ Daiyun Mountain National Nature Reserve Administration Bureau, Quanzhou, Fujian 362500, China

Received:2024-10-08 Accepted:2025-01-14 Online:2026-01-20 Published:2026-02-13
Contact: *ZHANG Qiu-Fang (qiufangzh@fjnu.edu.cn)
Supported by:
National Natural Science Foundation of China(32471684);National Natural Science Foundation of China(32371846);Fujian Provincial Natural Science Foundation(2024J01130937);Fujian Provincial Natural Science Foundation(2023R1002002)

摘要/Abstract

摘要：

微生物氮利用效率(NUE)描述了微生物用于生长的氮相对于吸收的总有机氮的比例, 是调节土壤氮循环的重要参数。¹⁸O-H₂O法和生态酶化学计量模型广泛应用于评估微生物NUE。然而, 目前关于氮富集对森林土壤微生物NUE影响的研究仍不充分, 这会影响对土壤氮供应的准确预测。该研究以亚热带罗浮栲(Castanopsis faberi)林土壤为研究对象, 通过施加尿素模拟大气氮沉降, 设置对照(CK, 0 kg N·hm^-2·a^-1)、低氮(LN, 40 kg N·hm^-2·a^-1)和高氮(HN, 80 kg N·hm^-2·a^-1) 3个处理, 使用¹⁸O-H₂O法和生态酶化学计量模型, 比较不同氮富集水平下土壤微生物NUE的差异。同时还测定了土壤理化性质、微生物生物量、胞外酶活性、化学计量不平衡等, 以期探究调控微生物NUE对氮富集响应的因子。结果表明, 不同方法得到的微生物NUE均随着氮富集速率的增加而降低。不同氮处理的矢量角度值均大于55°, 这表明该研究区土壤微生物整体上受到磷限制, 但氮富集并没有加剧该样地土壤微生物受到的磷限制。相反, 氮富集对微生物碳氮不平衡具有显著的负效应, 且微生物NUE与微生物碳氮不平衡呈显著的正相关关系。综上, 氮富集可能不利于亚热带森林土壤氮储存。为改善这一现状, 建议进一步调控土壤生态化学计量平衡。

关键词: 微生物氮利用效率, 氮添加, 生态化学计量, 同位素示踪, 森林

Abstract:

Aims Microbial nitrogen use efficiency (NUE) refers to the ratio of nitrogen used by microorganisms for growth to total organic nitrogen absorbed, which is a key regulator of the soil nitrogen cycle. The ¹⁸O-H₂O method and eco-enzyme stoichiometric model are the most common techniques employed to estimate microbial NUE. However, the impact of nitrogen enrichment on microbial NUE in forest soils remains to be elucidated, which would significantly impede the accurate prediction of soil nitrogen supply.

Methods In this study, we sampled the soils from subtropical Castanopsis faberi forests and used urea to simulate atmospheric nitrogen deposition. In total, three levels of nitrogen additions were set up, including control (CK, 0 kg N·hm^-2·a^-1), low nitrogen (LN, 40 kg N·hm^-2·a^-1), and high nitrogen (HN, 80 kg N·hm^-2·a^-1) treatments. The ¹⁸O-H₂O method and eco-enzyme stoichiometric model were used to compare the differences in soil microbial NUE under different nitrogen enrichment levels. Furthermore, soil physicochemical properties, microbial biomass, extracellular enzyme activity, and stoichiometric imbalance were also measured to explore the factors that influence the response of microbial NUE to nitrogen enrichment.

Important findings The results showed that the microbial NUE, as determined by two different methods, exhibited a decline with the increase of nitrogen enrichment. The vector angle values of different nitrogen treatments were all greater than 55°, indicating that soil microorganisms in this study area were generally phosphorus limited, but nitrogen enrichment did not exacerbate the phosphorus limitation. On the contrary, nitrogen enrichment has a significant negative effect on microbial carbon and nitrogen imbalance, and a positive correlation was observed between microbial NUE and microbial carbon and nitrogen imbalance. In summary, the nitrogen enrichment may have a detrimental effect on soil nitrogen storage in subtropical forests, highlighting the necessity to enhance soil nitrogen storage by means of regulating the soil stoichiometric balance in these forests.

Key words: microbial nitrogen use efficiency, nitrogen addition, ecological stoichiometry, isotope labeling, forest

皮惠之, 张秋芳, 孙浩, 曾泉鑫, 彭园珍, 元晓春, 徐建国, 陈岳民. 微生物碳氮不平衡影响罗浮栲林土壤微生物氮利用效率对氮富集的响应. 植物生态学报, 2026, 50(1): 34-44. DOI: 10.17521/cjpe.2024.0350

PI Hui-Zhi, ZHANG Qiu-Fang, SUN Hao, ZENG Quan-Xin, PENG Yuan-Zhen, YUAN Xiao-Chun, XU Jian-Guo, CHEN Yue-Min. Microbial carbon-nitrogen imbalance affects the response of microbial nitrogen use efficiency to nitrogen enrichment in Castanopsis faberi forest soils. Chinese Journal of Plant Ecology, 2026, 50(1): 34-44. DOI: 10.17521/cjpe.2024.0350

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链接本文: https://www.plant-ecology.com/CN/10.17521/cjpe.2024.0350

https://www.plant-ecology.com/CN/Y2026/V50/I1/34

图/表 4

图1 氮富集对微生物氮利用效率(NUE)的影响。A, 基于18O-H2O方法测定的微生物NUE。B和C, 基于生态酶化学计量模型计算得到的微生物NUE。箱线图中的横线显示中位数, 上下横线表示1/4和3/4分位数。点表示不同处理的重复数(n = 4)。CK, 对照; HN, 高氮富集; LN, 低氮富集。图中p值表示氮富集影响的主效应。不同小写字母表示不同氮富集处理差异显著(p < 0.05)。

Fig. 1 Effect of nitrogen enrichment on microbial nitrogen use efficiency (NUE). A, NUE18O, microbial NUE based on 18O-H2O method. B and C, NUEN:C, NUEN:P, microbial NUE based on ecological enzyme stoichiometric model. The horizontal lines in the boxplot show the median, and the upper and lower horizontal lines indicate the quarters and three-quarters quantiles. The dots represent the number of repetitions for different processes (n = 4). CK, control; HN, high nitrogen enrichment; LN, low nitrogen enrichment. The p value in the figure represents the main effect of nitrogen enrichment. Different lowercase letters indicated significant difference among different nitrogen enrichment treatments (p < 0.05).

图2 使用18O-H2O法和生态酶化学计量模型测定的微生物氮利用效率(NUE)之间的线性回归关系(n = 12)。A, 使用18O-H2O法(NUE18O)和N:C生态酶化学计量模型(NUEN:C)测定的微生物NUE之间的线性回归关系。B, 使用18O-H2O法(NUE18O)和N:P生态酶化学计量模型(NUEN:P)测定的微生物NUE之间的线性回归关系。灰色区域表示95%置信区间。CK, 对照; HN, 高氮富集; LN, 低氮富集。

Fig. 2 Linear regression relationship between microbial nitrogen use efficiency (NUE) measured by 18O-H2O method and ecological enzyme stoichiometric model (n = 12). A, Linear regression relationship between microbial NUE measured using 18O-H2O method (NUE18O) and N:C ecological enzyme stoichiometric model (NUEN:C). B, Linear regression relationship between microbial NUE measured using 18O-H2O method (NUE18O) and N:P ecological enzyme stoichiometric model (NUEN:P). The gray area represents the 95% confidence interval. CK, control; HN, high nitrogen enrichment; LN, low nitrogen enrichment.

表1 氮富集对土壤理化性质、微生物特征、化学计量特征、矢量长度和矢量角度的影响(平均值±标准差, n = 4)

Table 1 Effects of nitrogen enrichment on soil physical and chemical properties, microbial characteristics, stoichiometric characteristics, vector length and vector angle (mean ± SD, n = 4)

指标 Index	对照 CK	低氮 LN	高氮 HN	p
土壤理化性质 Soil physical and chemical property
土壤pH Soil pH	4.37 ± 0.02^a	4.29 ± 0.04^ab	4.27 ± 0.02^b	0.07
土壤总有机碳含量 SOC content (g·kg^-1)	52.64 ± 0.74^b	57.80 ± 0.86^a	57.80 ± 1.35^a	0.01
总氮含量 Total N content (g·kg^-1)	1.97 ± 0.25^c	3.07 ± 0.05^b	4.51 ± 0.45^a	<0.01
总磷含量 Total P content (g·kg^-1)	0.34 ± 0.02^a	0.24 ± 0.01^b	0.19 ± 0.01^c	<0.01
可溶性有机碳含量 DOC content (mg·kg^-1)	148.33 ± 9.92^a	140.79 ± 4.75^a	117.22 ± 2.89^b	0.02
无机氮含量 IN content (mg·kg^-1)	24.20 ± 0.82^b	34.29 ± 2.08^a	35.23 ± 1.03^a	<0.01
有效磷含量 AP content (mg·kg^-1)	3.24 ± 0.38	3.01 ± 0.14	3.24 ± 0.18	0.77
酶活性和微生物生物量 Enzyme activity and microbial biomass
β-葡萄糖苷酶活性 βG activity (nmol·g^-1·h^-1)	7.76 ± 0.09^a	6.70 ± 0.64^a	4.99 ± 0.22^b	<0.01
β-N-乙酰氨基葡萄糖苷酶活性 NAG activity (nmol·g^-1·h^-1)	21.90 ± 1.29	23.37 ± 1.40	20.38 ± 0.77	0.26
亮氨酸氨肽酶活性 LAP activity (nmol·g^-1·h^-1)	2.31 ± 0.40	1.62 ± 0.32	1.61 ± 0.39	0.36
酸性磷酸酶活性 ACP activity (nmol·g^-1·h^-1)	880.39 ± 4.71	684.72 ± 122.17	680.25 ± 98.62	0.26
微生物生物量碳含量 MBC content (mg·kg^-1)	1035.94 ± 59.24	1025.00 ± 58.28	1005.38 ± 48.22	0.93
微生物生物量氮含量 MBN content (mg·kg^-1)	79.87 ± 2.51^b	85.54 ± 3.77^b	96.79 ± 2.60^a	0.01
微生物生物量磷含量 MBP content (mg·kg^-1)	220.06 ± 17.14^a	177.93 ± 5.41^b	144.53 ± 5.81^b	<0.01
化学计量比 Stoichiometric ratio
DOC:IN	6.20 ± 0.64^a	4.14 ± 0.22^b	3.33 ± 0.02^b	<0.01
DOC:AP	46.98 ± 4.35	47.31 ± 3.97	36.38 ± 1.26	0.09
IN:AP	7.84 ± 1.08^b	11.52 ± 1.17^a	10.93 ± 0.37^a	0.05
MBC:MBN	13.01 ± 0.85^a	12.02 ± 0.67^ab	10.40 ± 0.54^b	0.07
MBC:MBP	4.74 ± 0.16^c	5.78 ± 0.41^b	6.95 ± 0.18^a	<0.01
MBN:MBP	0.37 ± 0.03^c	0.48 ± 0.03^b	0.67 ± 0.02^a	<0.01
βG:(NAG + LAP)	0.32 ± 0.02^a	0.28 ± 0.04^ab	0.23 ± 0.00^b	0.10
βG:ACP	0.01 ± 0.01	0.01 ± 0.01	0.01 ± 0.01	0.41
(NAG + LAP):ACP	0.03 ± 0.01	0.04 ± 0.01	0.03 ± 0.01	0.15
化学计量不平衡 Stoichiometric imbalance
碳:氮计量不平衡 Imbalance C:N	0.47 ± 0.03^a	0.35 ± 0.02^b	0.32 ± 0.02^b	<0.01
碳:磷计量不平衡 Imbalance C:P	10.01 ± 1.16^a	8.38 ± 1.16^a	5.24 ± 0.21^b	0.02
氮:磷计量不平衡 Imbalance N:P	21.67 ± 3.59	24.20 ± 2.90	16.36 ± 0.98	0.17
矢量长度 Vector length	0.24 ± 0.02^a	0.21 ± 0.05^ab	0.19 ± 0.01^b	0.07
矢量角度 Vector angle (°)	87.94 ± 0.22	87.18 ± 0.76	87.61 ± 0.63	0.23

表1 氮富集对土壤理化性质、微生物特征、化学计量特征、矢量长度和矢量角度的影响(平均值±标准差, n = 4)

Table 1 Effects of nitrogen enrichment on soil physical and chemical properties, microbial characteristics, stoichiometric characteristics, vector length and vector angle (mean ± SD, n = 4)

指标 Index	对照 CK	低氮 LN	高氮 HN	p
土壤理化性质 Soil physical and chemical property
土壤pH Soil pH	4.37 ± 0.02^a	4.29 ± 0.04^ab	4.27 ± 0.02^b	0.07
土壤总有机碳含量 SOC content (g·kg^-1)	52.64 ± 0.74^b	57.80 ± 0.86^a	57.80 ± 1.35^a	0.01
总氮含量 Total N content (g·kg^-1)	1.97 ± 0.25^c	3.07 ± 0.05^b	4.51 ± 0.45^a	<0.01
总磷含量 Total P content (g·kg^-1)	0.34 ± 0.02^a	0.24 ± 0.01^b	0.19 ± 0.01^c	<0.01
可溶性有机碳含量 DOC content (mg·kg^-1)	148.33 ± 9.92^a	140.79 ± 4.75^a	117.22 ± 2.89^b	0.02
无机氮含量 IN content (mg·kg^-1)	24.20 ± 0.82^b	34.29 ± 2.08^a	35.23 ± 1.03^a	<0.01
有效磷含量 AP content (mg·kg^-1)	3.24 ± 0.38	3.01 ± 0.14	3.24 ± 0.18	0.77
酶活性和微生物生物量 Enzyme activity and microbial biomass
β-葡萄糖苷酶活性 βG activity (nmol·g^-1·h^-1)	7.76 ± 0.09^a	6.70 ± 0.64^a	4.99 ± 0.22^b	<0.01
β-N-乙酰氨基葡萄糖苷酶活性 NAG activity (nmol·g^-1·h^-1)	21.90 ± 1.29	23.37 ± 1.40	20.38 ± 0.77	0.26
亮氨酸氨肽酶活性 LAP activity (nmol·g^-1·h^-1)	2.31 ± 0.40	1.62 ± 0.32	1.61 ± 0.39	0.36
酸性磷酸酶活性 ACP activity (nmol·g^-1·h^-1)	880.39 ± 4.71	684.72 ± 122.17	680.25 ± 98.62	0.26
微生物生物量碳含量 MBC content (mg·kg^-1)	1035.94 ± 59.24	1025.00 ± 58.28	1005.38 ± 48.22	0.93
微生物生物量氮含量 MBN content (mg·kg^-1)	79.87 ± 2.51^b	85.54 ± 3.77^b	96.79 ± 2.60^a	0.01
微生物生物量磷含量 MBP content (mg·kg^-1)	220.06 ± 17.14^a	177.93 ± 5.41^b	144.53 ± 5.81^b	<0.01
化学计量比 Stoichiometric ratio
DOC:IN	6.20 ± 0.64^a	4.14 ± 0.22^b	3.33 ± 0.02^b	<0.01
DOC:AP	46.98 ± 4.35	47.31 ± 3.97	36.38 ± 1.26	0.09
IN:AP	7.84 ± 1.08^b	11.52 ± 1.17^a	10.93 ± 0.37^a	0.05
MBC:MBN	13.01 ± 0.85^a	12.02 ± 0.67^ab	10.40 ± 0.54^b	0.07
MBC:MBP	4.74 ± 0.16^c	5.78 ± 0.41^b	6.95 ± 0.18^a	<0.01
MBN:MBP	0.37 ± 0.03^c	0.48 ± 0.03^b	0.67 ± 0.02^a	<0.01
βG:(NAG + LAP)	0.32 ± 0.02^a	0.28 ± 0.04^ab	0.23 ± 0.00^b	0.10
βG:ACP	0.01 ± 0.01	0.01 ± 0.01	0.01 ± 0.01	0.41
(NAG + LAP):ACP	0.03 ± 0.01	0.04 ± 0.01	0.03 ± 0.01	0.15
化学计量不平衡 Stoichiometric imbalance
碳:氮计量不平衡 Imbalance C:N	0.47 ± 0.03^a	0.35 ± 0.02^b	0.32 ± 0.02^b	<0.01
碳:磷计量不平衡 Imbalance C:P	10.01 ± 1.16^a	8.38 ± 1.16^a	5.24 ± 0.21^b	0.02
氮:磷计量不平衡 Imbalance N:P	21.67 ± 3.59	24.20 ± 2.90	16.36 ± 0.98	0.17
矢量长度 Vector length	0.24 ± 0.02^a	0.21 ± 0.05^ab	0.19 ± 0.01^b	0.07
矢量角度 Vector angle (°)	87.94 ± 0.22	87.18 ± 0.76	87.61 ± 0.63	0.23

图3 18O-H2O法计算的微生物氮利用效率(NUE18O)与土壤性质(包括土壤理化性质、微生物特性、化学计量特征)之间的关系(n = 12)。A, 土壤性质与微生物NUE18O相关关系的主成分(PC)分析。B, 微生物NUE18O与土壤性质之间的相关性热图。*, p < 0.05; **, p < 0.01。C-J, 微生物NUE18O与无机氮含量(IN)、微生物生物量氮含量(MBN)、可溶性有机碳:无机氮(DOC:IN)、微生物生物量碳:氮(MBC:MBN)、可溶性有机碳含量(DOC)、土壤pH、β-1,4-葡萄糖苷酶活性(βG)和碳:氮化学计量不平衡(Imbalance C:N)之间的线性回归关系。灰色区域表示95%置信区间。AP, 有效磷含量; NAG, β-N-乙酰氨基葡萄糖苷酶活性; LAP, 亮氨酸氨肽酶活性; ACP, 酸性磷酸酶活性。CK, 对照; HN, 高氮富集; LN, 低氮富集。

Fig. 3 Relationship between microbial nitrogen use efficiency (NUE18O) measured by the 18O-H2O method and soil properties (including soil physical and chemical characteristics, microbial characteristics, and stoichiometric characteristics) (n = 12). A, Principal component (PC) analysis between soil properties and microbial NUE18O. B, Heatmap of correlation between microbial NUE18O and soil properties. *, p < 0.05; **, p < 0.01. C-J, Microbial NUE18O and inorganic nitrogen content (IN), microbial biomass nitrogen content (MBN), dissolved organic carbon content: inorganic nitrogen content (DOC:IN), microbial biomass carbon content: microbial biomass nitrogen content (MBC:MBN), dissolved organic carbon content (DOC), soil pH, β-1,4-glucosidase activity (βG), and carbon: nitrogen stoichiometric imbalance (Imbalance C:N). The gray area plot represents the 95% confidence interval. ACP, acid phosphatase activity; AP, available phosphate content; LAP, leucine aminopeptidase activity; NAG, β-1,4-N-acetyl-glucosaminidase activity. CK, control; HN, high nitrogen enrichment; LN, low nitrogen enrichment.

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微生物碳氮不平衡影响罗浮栲林土壤微生物氮利用效率对氮富集的响应

Microbial carbon-nitrogen imbalance affects the response of microbial nitrogen use efficiency to nitrogen enrichment in Castanopsis faberi forest soils

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