荒漠草原土壤氨氧化细菌群落结构对氮添加和枯落物输入的响应

doi:10.17521/cjpe.2022.0220

植物生态学报 ›› 2023, Vol. 47 ›› Issue (5): 699-712.DOI: 10.17521/cjpe.2022.0220

荒漠草原土壤氨氧化细菌群落结构对氮添加和枯落物输入的响应

张雅琪¹^,², 庞丹波¹^,², 陈林¹^,², 曹萌豪¹^,², 何文强¹^,², 李学斌¹^,^*()

1.宁夏大学西北退化生态系统恢复与重建教育部重点实验室, 宁夏大学西北土地退化与生态恢复国家重点实验室培育基地, 银川 750021
2.宁夏大学生态环境学院, 银川 750021

收稿日期:2022-05-26 接受日期:2022-09-28 出版日期:2023-05-20 发布日期:2022-09-28
通讯作者: * (lixuebin@nux.edu.cn)
基金资助:
国家自然科学基金(31960359);宁夏重点研发计划(2021BEG02005);第三批宁夏青年科技人才托举工程(TJGC2018068)

Response of ammonia oxidizing bacteria to nitrogen fertilization and plant litter input on desert steppe

ZHANG Ya-Qi¹^,², PANG Dan-Bo¹^,², CHEN Lin¹^,², CAO Meng-Hao¹^,², HE Wen-Qiang¹^,², LI Xue-Bin¹^,^*()

1. Key Laboratory of Restoration and Reconstruction of Degraded Ecosystems in Northwestern China of Ministry of Education, Breeding Base for State Key Laboratory of Land Degradation and Ecological Restoration in Northwestern China, Ningxia University, Yinchuan 750021, China
2. School of Ecology and Environment, Ningxia University, Yinchuan 750021, China

Received:2022-05-26 Accepted:2022-09-28 Online:2023-05-20 Published:2022-09-28
Supported by:
National Natural Science Foundation of China(31960359);Ningxia Huizu Autonomous Region Key Research and Development Project(2021BEG02005);Third Batch of Ningxia Young Scientific and Technological Talent Support Project(TJGC2018068)

摘要/Abstract

摘要：

为了解荒漠草原表层土壤氨氧化细菌(AOB)对枯落物输入及氮添加的响应, 该研究以宁夏回族自治区盐池县荒漠草原为实验平台, 选择4种常见植物——苦豆子(Sophora alopecuroides)、猪毛蒿(Artemisia scoparia)、短花针茅(Stipa breviflora)和沙芦草(Agropyron mongolicum)的枯落物设置枯落物输入处理, 设置对照(0 g·m^-2·a^-1)、氮添加(9.2 g·m^-2·a^-1) 2个处理, 运用荧光定量PCR、高通量测序等分子生物学技术, 探究了荒漠草原0-5 cm表层土壤AOB对氮添加和不同枯落物输入的响应。研究结果显示, 在氮添加和枯落物输入条件下, 荒漠草原土壤表层AOB共有3门4纲6目7科8属17种。实验所测AOB群落物种主要来源于β-变形菌纲(beta-Proteobacteria)中的亚硝基单胞菌属(Nitrosomonas)和亚硝基螺旋菌属(Nitrosospira), 且以亚硝基单胞菌属为优势种群。与对照相比, 氮添加显著降低了AOB-氨单加氧酶(amoA)基因拷贝数, 表明施氮会抑制荒漠草原表层土壤中的硝化作用。在不同种类的枯落物输入下, AOB-amoA基因丰度的响应具有差异性, 枯落物输入能够在一定程度上缓解氮添加对土壤AOB-amoA基因丰度的抑制, 但总体上不会改变其变化趋势。冗余分析结果表明土壤有机碳、全磷、硝态氮和铵态氮含量是影响AOB-amoA基因丰度的主要土壤理化因子。研究结果表明, 氮添加能够显著降低荒漠草原土壤表层AOB-amoA的基因丰度, 该结果有助于丰富和拓展未来干旱半干旱荒漠草原地区氮沉降变化对土壤表层氮循环功能基因丰度的影响和机制的认识。

关键词: 氨氧化细菌, 荒漠草原, 多样性, 氮添加, 枯落物输入, 微生物生态学

Abstract:

Aims This study aimed to explore the response of ammonia oxidizing bacteria (AOB) to litter decomposition and nitrogen application in the topsoil of desert steppe, and the main environmental factors influencing the AOB were also analyzed. Thus, this study will contribute to better understanding of the mechanism of nitrogen cycle function gene abundance in response to nitrogen deposition in arid and semi-arid desert steppe regions.
Methods We conducted the nitrogen fertilization experiment in the desert steppe in Yanchi, Ningxia. The four plant litters, including Sophora alopecuroides, Artemisia scoparia, Stipa breviflora and Agropyron mongolicum were selected as plant litter input treatments. The nitrogen fertilization treatments, including control (0 g·m^-2·a^-1) and nitrogen application (9.2 g·m^-2·a^-1), were applied to explore the response of AOB to nitrogen deposition and different litter inputs in top soil (0-5 cm) of desert steppe by fluorescent quantitative PCR and high-throughput sequencing.
Important findings Our results showed that there were 3 phyla, 4 classes, 6 orders, 7 families, 8 genera and 17 species of AOB in the topsoil of desert steppe under nitrogen application and litter decomposition. The AOB communities were mainly derived from Nitrosomonas and Nitrosospira, which were from beta-Proteobacteria, and Nitrosospira was the dominant species. Compared with the control, the gene copy number of AOB was significantly decreased under nitrogen application, indicating that nitrogen application inhibited nitrification in the topsoil of the desert steppe. Whereas, the response of AOB-ammonia monooxy genase subsuit A (amoA) gene abundance varied under different plant litter decomposition. Litter input could alleviate the inhibition of nitrogen enrichment on soil AOB-amoA gene abundance to a certain extent, but did not change the trend of soil AOB-amoA gene abundance. A redundancy analysis confirmed that soil organic carbon, total phosphorus, ammonium nitrogen and nitrate nitrogen contents were the key environmental factors affecting niche separation of AOB-amoA gene abundance in desert steppe soil. The results showed that nitrogen addition could significantly reduce the gene abundance of AOB-amoA, thereby affecting the nitrification and the direction of soil nitrogen transformation in the topsoil of desert steppe.

Key words: ammonia oxidizing bacteria, desert steppe, diversity, nitrogen deposition, litter addition, microbial ecology

张雅琪, 庞丹波, 陈林, 曹萌豪, 何文强, 李学斌. 荒漠草原土壤氨氧化细菌群落结构对氮添加和枯落物输入的响应. 植物生态学报, 2023, 47(5): 699-712. DOI: 10.17521/cjpe.2022.0220

ZHANG Ya-Qi, PANG Dan-Bo, CHEN Lin, CAO Meng-Hao, HE Wen-Qiang, LI Xue-Bin. Response of ammonia oxidizing bacteria to nitrogen fertilization and plant litter input on desert steppe. Chinese Journal of Plant Ecology, 2023, 47(5): 699-712. DOI: 10.17521/cjpe.2022.0220

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链接本文: https://www.plant-ecology.com/CN/10.17521/cjpe.2022.0220

https://www.plant-ecology.com/CN/Y2023/V47/I5/699

图/表 9

表1 荒漠草原氮添加和枯落物输入下的土壤化学性质(平均值±标准差)

Table 1 Chemical properties of soil under effects of nitrogen application and different litter addition in a desert steppe (mean ± SD)

土壤因子 Soil factor	氮处理 Nitrogen treatment	枯落物处理 Litter input treatment				N	L	L × N
土壤因子 Soil factor	氮处理 Nitrogen treatment	短花针茅 ZM	沙芦草 BC	猪毛蒿 H	苦豆子 K	N	L	L × N
pH	CK	8.96 ± 0.08^Aa	8.95 ± 0.06^Aa	8.83 ± 0.05^Aa	8.43 ± 0.11^Ab	0.091	0.127	0.607
pH	N	8.91 ± 0.08^Aa	8.46 ± 0.80^Ac	8.72 ± 0.05^Ab	8.43 ± 0.11^Ac	0.091	0.127	0.607
SOC (mg·kg^-1)	CK	36.12 ± 3.04^Aa	33.00 ± 4.44^Ab	28.99 ± 0.50^Ac	23.79 ± 0.41^Bd	0.000^**	0.000^**	0.000^**
SOC (mg·kg^-1)	N	34.78 ± 3.76^Ab	35.00 ± 5.93^Ab	28.00 ± 4.32^Ac	66.08 ± 0.49^Aa	0.000^**	0.000^**	0.000^**
TN (mg·kg^-1)	CK	4.03 ± 1.12^Ad	3.86 ± 0.10^Bc	5.52 ± 2.88^Aa	4.32 ± 0.02^Ab	0.004^**	0.191	0.077
TN (mg·kg^-1)	N	4.71 ± 0.24^Ac	6.76 ± 0.83^Aa	5.47 ± 1.24^Ab	4.60 ± 0.29^Ac	0.004^**	0.191	0.077
TP (mg·kg^-1)	CK	3.32 ± 0.47^Ac	3.84 ± 0.37^Ab	3.95 ± 0.64^Ab	4.48 ± 0.03^Aa	0.000^**	0.617	0.095
TP (mg·kg^-1)	N	4.33 ± 0.19^Bb	4.39 ± 0.48^Ab	3.97 ± 0.15^Ac	4.48 ± 0.03^Aa	0.000^**	0.617	0.095
NO₃^--N (mg·kg^-1)	CK	28.47 ± 2.36^Bb	23.86 ± 3.84^Bc	18.73 ± 0.52^Bc	80.29 ± 13.29^Ba	0.001^**	0.011^*	0.000^**
NO₃^--N (mg·kg^-1)	N	42.56 ± 6.51^Ac	30.18 ± 2.61^Ac	56.18 ± 6.09^Ab	107.76 ± 20.23^Aa	0.001^**	0.011^*	0.000^**
NH⁺₄-N (mg·kg^-1)	CK	20.73 ± 2.55^Bd	26.86 ± 4.63^Ac	26.86 ± 4.63^Ac	30.20 ± 0.63^Bb	0.001^**	0.016^*	0.005^**
NH⁺₄-N (mg·kg^-1)	N	42.56 ± 6.51^Ab	32.18 ± 9.33^Ac	33.19 ± 6.70^Ac	54.84 ± 0.98^Aa	0.001^**	0.016^*	0.005^**
TS (mg·kg^-1)	CK	0.29 ± 0.05^Ab	0.25 ± 0.04^Ab	0.27 ± 0.06^Bb	0.37 ± 0.03^Aa	0.020^*	0.312	0.321
TS (mg·kg^-1)	N	0.30 ± 0.04^Ad	0.33 ± 0.06^Ab	0.37 ± 0.01^Aa	0.37 ± 0.03^Aa

图1 荒漠草原氮添加(A)和枯落物输入(B)对土壤氨氧化细菌氨单加氧酶(AOB-amoA)基因丰度的影响(平均值±标准差)。CK, 对照; N, 氮添加。BC, 沙芦草; H, 猪毛蒿; K, 苦豆子; ZM, 短花针茅。不同大写字母代表同一枯落物处理不同氮处理下有显著差异(p < 0.05); 不同小写字母表示同一施氮处理下不同枯落物间差异显著(p < 0.05)。

Fig. 1 Effects of nitrogen application (A) and litter addition (B) on gene abundance of ammonia oxidizing bacteria ammonia monooxy genase subsuit A (AOB-amoA) in a desert steppe (mean ± SD). CK, control group; N, nitrogen addition treatment. BC, Agropyron mongolicum; H, Artemisia scoparia; K, Sophora alopecuroides; ZM, Stipa breviflora. different uppercase letters indicate significant differences between different nitrogen additions in the same litter treatment (p < 0.05); Different lowercase letters indicate statistically significant difference between different litter treatments in the same nitrogen application treatment (p < 0.05).

图2 荒漠草原对照和施氮处理下土壤氨氧化细菌(AOB)多样性差异。CK, 对照; N, 氮添加。

Fig. 2 Difference of soil ammonia oxidizing bacteria (AOB) diversity under control and nitrogen application treatment in a desert steppe. CK, control group; N, nitrogen addition treatment.

图3 荒漠草原施氮和枯落物输入下土壤氨氧化细菌(AOB)多样性差异。CKBC, 对照组+沙芦草; CKH, 对照组+猪毛蒿; CKK, 对照组+苦豆子; CKZM, 对照组+短花针茅; NBC, 施氮+沙芦草; NH, 施氮+猪毛蒿; NK, 施氮+苦豆子; NZM, 施氮+短花针茅。不同小写字母表示同一物种不同施氮处理下差异显著(p < 0.05);

Fig. 3 Difference of soil ammonia oxidizing bacteria (AOB) diversity under nitrogen application and litter input in a desert steppe. CKBC, control group + Agropyron mongolicum; CKH, control group + Artemisia scoparia; CKK, control group + Sophora alopecuroides; CKZM, control group + Stipa breviflora; NBC, nitrogen addition treatment + Agropyron mongolicum; NH, nitrogen addition treatment + Artemisia scoparia; NK, nitrogen addition treatment + Sophora alopecuroides; NZM, nitrogen addition treatment + Stipa breviflora. Different lowercase letters indicate significant differences between different nitrogen addition treatments of the same species (p < 0.05)

表2 荒漠草原氮添加和枯落物输入对土壤氨氧化细菌(AOB)群落多样性的双因素方差分析

Table 2 Two-way variance analysis of soil ammonia oxidizing bacteria (AOB) community diversity by nitrogen addition and litter type in a desert steppe

指标 Index	氮添加 Nitrogen addition (N)		枯落物种类 Litter type (L)		L × N
指标 Index	F	p	F	p	F	p
Shannon-Wiener	7.243	0.016^*	3.208	0.049^*	6.217	0.005^*
Simpson	0.887	0.360	3.371	0.045^*	6.957	0.003^*
Ace	0.641	0.435	4.880	0.013^*	2.630	0.086
Chao1	0.658	0.429	4.852	0.014^*	2.115	0.139
Sobs	1.720	0.208	0.476	0.009^**	2.896	0.067

图4 荒漠草原氮添加(A)和不同枯落物输入下(B)分类操作单元(OTU)水平上土壤氨氧化细菌主成分分析(PCA)。CK, 对照; N, 氮添加。CKBC, 对照组+沙芦草; CKH, 对照组+猪毛蒿; CKK, 对照组+苦豆子; CKZM, 对照组+短花针茅; NBC, 施氮+沙芦草; NH, 施氮+猪毛蒿; NK, 施氮+苦豆子; NZM, 施氮+短花针茅。

Fig. 4 Principal component analysis (PCA) of soil ammonia oxidizing bacterial operational taxonomic unit (OTU) level under nitrogen application (A) and litter input (B) in a desert steppe. CK, control group; N, nitrogen addition treatment. CKBC, control group + Agropyron mongolicum; CKH, control group + Artemisia scoparia; CKK, control group + Sophora alopecuroides; CKZM, control group + Stipa breviflora; NBC, nitrogen addition treatment + Agropyron mongolicum; NH, nitrogen addition treatment + Artemisia scoparia; NK, nitrogen addition treatment + Sophora alopecuroides; NZM, nitrogen addition treatment + Stipa breviflora.

图5 荒漠草原施氮(A)和枯落物输入(B)下土壤氨氧化细菌(AOB)群落组成。OTU, 分类操作单元。CK, 对照; N, 氮添加。CKBC, 对照组+沙芦草; CKH, 对照组+猪毛蒿; CKK, 对照组+苦豆子; CKZM, 对照组+短花针茅; NBC, 施氮+沙芦草; NH, 施氮+猪毛蒿; NK, 施氮+苦豆子; NZM, 施氮+短花针茅。图B中不同小写字母表示同一物种不同施氮处理下差异显著(p < 0.05)。

Fig. 5 Community composition of soil ammonia oxidizing bacteria (AOB) under nitrogen application (A) and litter input (B) in a desert steppe. OTU, operational taxonomic unit. CK, control group; N, nitrogen addition treatment. CKBC, control group + Agropyron mongolicum; CKH, control group + Artemisia scoparia; CKK, control group + Sophora alopecuroides; CKZM, control group + Stipa breviflora; NBC, nitrogen addition treatment + Agropyron mongolicum; NH, nitrogen addition treatment + Artemisia scoparia; NK, nitrogen addition treatment + Sophora alopecuroides; NZM, nitrogen addition treatment + Stipa breviflora; Different lowercase letters in Figure B indicate significant differences in the percentage relative abundance of OTU in soil AOB under different N application treatments for the same species (p < 0.05).

图6 荒漠草原氮添加和枯落物输入下土壤氨氧化细菌(AOB)基因系统发育树。各支上的数字是1 000次重抽样分析的支持百分比, 小于50的省略, AY627780-KY474829为基因序列在Genbank数据库中的登录号。OUT, 97%相似度下的分类操作单元。

Fig. 6 Phylogenetic tree of soil ammonia oxidizing bacteria (AOB) gene under nitrogen application and litter addition in a desert steppe. Values indicate the percentage of 1 000 replicate trees supporting the branching order; values below 50 are omitted. AY627780-KY474829 are the Genbank accession numbers. OTU, operational taxonomic units under 97% similarity.

图7 荒漠草原施氮和枯落物输入下土壤氨氧化细菌氨单加氧酶基因丰度与土壤理化性质间的冗余分析(RDA)。NH+4-N, 铵态氮含量; NO3--N, 硝态氮含量; SOC, 有机碳含量; TN, 全氮含量; TP, 全磷含量; TS, 全盐含量。CKBC, 对照组+沙芦草; CKH, 对照组+猪毛蒿; CKK, 对照组+苦豆子; CKZM, 对照组+短花针茅; NBC, 施氮+沙芦草; NH, 施氮+猪毛蒿; NK, 施氮+苦豆子; NZM, 施氮+短花针茅。

Fig. 7 Redundancy analysis (RDA) between ammonia monooxy genase subsuit A gene abundance of soil ammonia oxidizing bacteria and soil physical and chemical properties under nitrogen application and litter addition in a desert steppe. NH+4-N, ammonium nitrogen content; NO3--N, nitrate nitrogen content; SOC, soil organic carbon content; TN, total nitrogen content; TP, total phosphorus content; TS, total salt content. CKBC, control group + Agropyron mongolicum; CKH, control group + Artemisia scoparia; CKK, control group + Sophora alopecuroides; CKZM, control group + Stipa breviflora; NBC, nitrogen addition treatment + Agropyron mongolicum; NH, nitrogen addition treatment + Artemisia scoparia; NK, nitrogen addition treatment + Sophora alopecuroides; NZM, nitrogen addition treatment + Stipa breviflora.

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荒漠草原土壤氨氧化细菌群落结构对氮添加和枯落物输入的响应

Response of ammonia oxidizing bacteria to nitrogen fertilization and plant litter input on desert steppe

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