小叶锦鸡儿灌丛对草地土壤固氮微生物群落的影响

doi:10.11686/cyxb2021403

摘要/Abstract

摘要：

草原灌丛化已成为全球干旱和半干旱地区的普遍现象，关于灌木扩张对草地土壤固氮微生物群落的影响及其机制尚不清楚。小叶锦鸡儿是广泛生长于内蒙古草原的豆科灌木，研究其对土壤固氮微生物群落的影响具有重要意义。本研究采用传统培养法结合分子生物学技术，比较了荒漠草原（干旱地区）和典型草原（半干旱地区）小叶锦鸡儿灌丛内外不同土壤深度固氮微生物群落的差异，并从灌丛对群落物种的选择性、灌丛沃岛效应、灌丛效应和干旱效应的相互关系等方面探讨引起这些差异的机制。结果表明：小叶锦鸡儿灌丛不仅增加了固氮微生物群落的物种丰富度和多度，而且改变了群落组成。群落组成的改变表现在37.50%~58.33%种属的多度发生显著变化、优势属及其优势地位改变、灌丛内外Jaccard相异性指数较大（0.40~0.76）和灌丛内外NMDS（非度量多维度尺度分析）群落组成排序图的分异；ANOSIM检验表明灌丛内外群落组成差异显著。灌丛对固氮微生物群落的效应随着土层深度增加而衰减，随着干旱增加而加强。灌丛对固氮微生物群落的影响大于气候干旱对其的影响。灌木小叶锦鸡儿对固氮微生物群落影响机理是：1）灌丛对固氮微生物物种具有选择性；2）灌丛通过改变土壤理化性质而影响了固氮微生物群落；3）气候干旱增强了灌丛对固氮微生物群落的影响；4）灌丛还通过缓解干旱的作用而影响固氮微生物群落。

关键词: 气候干旱, 固氮微生物, 群落组成, 沃岛效应, 灌丛化

Abstract:

Encroachment of woody species has become a common phenomenon in arid and semi-arid grassland worldwide. However， the effects of shrubs on soil nitrogen-fixing microbial （NFM） communities and the mechanisms underlying them are poorly known. Caragana microphylla （Fabaceae） is widely distributed in the Inner Mongolian Steppe. It is important to explore the effects on NFM communities. In this paper， we compared the differences of soil NFM communities outside and within the canopy areas of shrubs in different soil horizons of desert steppe （arid zone） and typical steppe （semi-arid zone） by traditional culture methods and molecular biology techniques. Furthermore， our study explored the mechanisms underlying the shrub effects in terms of the species selectivity， fertile-island effect， and the interaction of the shrub and aridity effects. It was found that C. microphylla significantly increased the abundance and richness of NFM communities， and also affected their community composition. The change in community composition was manifested as significant variation in abundance of 37.50%-58.33% of genera， as change in the dominant genera and their dominance position， as a large Jaccard dissimilarity index （0.40-0.76） for samples from outside and samples from within shrub canopies， and differences in the ordination of NMDS （non-metric multidimensional scaling） results inside and outside shrub canopies. Based on these data an ‘analysis of similarity’ test showed significant differences in NFM community composition outside and within shrubs. The effect of shrubs on NFM communities decreased with increasing soil depth， and increased with increasing aridity. Shrubs exerted a greater effect on NFM communities than aridity. The mechanisms underlying the C. microphylla effects on NFM communities were： 1） Shrubs had a selective effect on NFM species presence； 2） Shrubs affected NFM communities through soil physical and chemical characteristics； 3） Climate aridity enhanced the impact of shrubs on NFM communities； 4） Shrubs affected NFM communities through mitigating climatic impacts.

Key words: climatic aridity, nitrogen-fixing microbe, microbial community composition, fertile-island effect, woody species encroachment

王春雯, 赵芳, 张晨, 解李娜, 马成仓. 小叶锦鸡儿灌丛对草地土壤固氮微生物群落的影响[J]. 草业学报, 2022, 31(10): 28-40.

Chun-wen WANG, Fang ZHAO, Chen ZHANG, Li-na XIE, Cheng-cang MA. Effects of Caragana microphylla shrubs on the soil nitrogen-fixing microbial communities in steppe land[J]. Acta Prataculturae Sinica, 2022, 31(10): 28-40.

图/表 10

图1 小叶锦鸡儿灌丛对土壤固氮微生物群落物种丰度和多度的影响*表示与0差异显著（P<0.05）。* indicates the significant differences with zero （P<0.05）.

Fig.1 Effects of C. microphylla shrubs on species richness and abundance for soil nitrogen-fixing microbial communities in desert steppe and typical steppe （RII）

图2 荒漠草原和典型草原小叶锦鸡儿灌丛内外土壤固氮微生物群落组成Meth：甲基杆菌属Methylobacterium； Cell：纤维微菌属Cellulosimicrobium； Vari：贪噬菌属Variovorax； Rhiz：根瘤菌属Rhizobium； Baci：芽孢杆菌属Bacillus； Paen：类芽孢杆菌属Paenibacillus； Brev：短芽孢杆菌属Brevibacillus； Acti：马杜拉放线菌属Actinomadura； Sino：中华根瘤菌属Sinorhizobium； Arth：节杆菌属Arthrobacter； Chit：曼噬甲壳菌属Chitinophaga； Microv：微枝形杆菌属Microvirga； Ente：肠杆菌属Enterobacter； Chry：金黄杆菌属Chryseobacterium； Micro：小细菌属Microbacterium； Brevi：短杆菌属Brevibacterium； Brevu：短波单胞菌属Brevundimonas； Pseu：假单胞菌属Pseudomonas； Sphi：鞘氨醇杆菌属Sphingobacterium； Stre：链霉菌属Streptomyces； Achr：无色杆菌属Achromobacter； Cohn：科恩菌属Cohnella； Exig：微小杆菌属Exiguobacterium； Stap：葡萄球菌属Staphylococcus； Mass：马赛菌属Massilia； Curt：短小杆菌属Curtobacterium。*表示灌丛内和灌丛外差异显著（t检验，P<0.05）。气泡图显示属多度（3个土层平均值，空心黑点表示该属在这个地区没出现，实心黑点表示该属的多度在灌丛内或灌丛外为0），堆积图显示属相对多度（数字表示优势属的相对多度）* indicate significant differences between outside and inside shrub canopies （t-test， P<0.05）. Bubble graph shows the abundance of genus （mean across three soil depths； Hollow black spots indicate that the genus is not present in this area， and solid black spots indicate that the abundance of the genus is 0 within or outside the shrub）. Stacked graph shows relative abundance of genus （digit indicate the relative abundance of dominant genera）.下同The same below.

Fig.2 Soil nitrogen-fixing microbial community composition outside and inside C. microphylla shrub canopies in desert steppe and typical steppe

表1 荒漠草原和典型草原小叶锦鸡儿灌丛内外土壤固氮微生物群落优势属和相对多度

Table 1 Dominant genus and relative abundance of soil nitrogen-fixing microbial communities outside and inside C. microphylla shrub canopies in desert steppe and typical steppe （%）

项目

Item

土层

Soil depth

共生

Symbiotic

0~10 cm

链霉菌属Streptomyces 23.84

节杆菌属Arthrobacter 16.25

金黄杆菌属Chryseobacterium 14.15

短小杆菌属Curtobacterium 10.58

芽孢杆菌属Bacillus 46.89

链霉菌属Streptomyces 25.73

链霉菌属Streptomyces 36.88

微杆菌属Microbacterium 21.25

芽孢杆菌属Bacillus 11.80

链霉菌属Streptomyces 47.81

微杆菌属Microbacterium 15.07

芽孢杆菌属Bacillus 14.88

10~20 cm

链霉菌属Streptomyces 33.70

节杆菌属Arthrobacter 16.08

芽孢杆菌属Bacillus 44.59

链霉菌属Streptomyces 30.46

类芽孢杆菌属Paenibacillus 11.17

链霉菌属Streptomyces 34.90

微杆菌属Microbacterium 20.21

芽孢杆菌属Bacillus 15.30

节杆菌属Arthrobacter 14.83

链霉菌属Streptomyces 33.67

芽孢杆菌属Bacillus 23.68

微杆菌属Microbacterium 15.02

节杆菌属Arthrobacter 14.09

30~40 cm

链霉菌属Streptomyces 30.69

假单胞菌属Pseudomonas 13.43

金黄杆菌属Chryseobacterium 12.32

芽孢杆菌属Bacillus 52.48

链霉菌属Streptomyces 28.36

链霉菌属Streptomyces 37.46

节杆菌属Arthrobacter 36.84

芽孢杆菌属Bacillus 19.43

链霉菌属Streptomyces 42.52

芽孢杆菌属Bacillus 21.29

微杆菌属Microbacterium 20.95

自生

Free-living

0~10 cm

芽孢杆菌属Bacillus 49.26

链霉菌属Streptomyces 23.10

中华根瘤菌属Sinorhizobium 15.67

链霉菌属Streptomyces 85.37

链霉菌属Streptomyces 49.87

中华根瘤菌属Sinorhizobium 21.97

链霉菌属Streptomyces 83.02

10~20 cm

芽孢杆菌属Bacillus 49.98

链霉菌属Streptomyces 29.93

链霉菌属Streptomyces 89.78

链霉菌属Streptomyces 54.26

中华根瘤菌属Sinorhizobium 28.67

链霉菌属Streptomyces 80.95

中华根瘤菌属Sinorhizobium 10.44

30~40 cm

链霉菌属Streptomyces 48.36

芽孢杆菌属Bacillus 41.38

链霉菌属Streptomyces 93.81

链霉菌属Streptomyces 41.11

芽孢杆菌属Bacillus 36.40

中华根瘤菌属Sinorhizobium 12.74

链霉菌属Streptomyces 86.31

表1 荒漠草原和典型草原小叶锦鸡儿灌丛内外土壤固氮微生物群落优势属和相对多度

Table 1 Dominant genus and relative abundance of soil nitrogen-fixing microbial communities outside and inside C. microphylla shrub canopies in desert steppe and typical steppe （%）

项目

Item

土层

Soil depth

荒漠草原Desert steppe

典型草原Typical steppe

灌丛内Inside-shrub

灌丛外Outside-shrub

灌丛内Inside-shrub

灌丛外Outside-shrub

共生

Symbiotic

0~10 cm

链霉菌属Streptomyces 23.84

节杆菌属Arthrobacter 16.25

金黄杆菌属Chryseobacterium 14.15

短小杆菌属Curtobacterium 10.58

芽孢杆菌属Bacillus 46.89

链霉菌属Streptomyces 25.73

链霉菌属Streptomyces 36.88

微杆菌属Microbacterium 21.25

芽孢杆菌属Bacillus 11.80

链霉菌属Streptomyces 47.81

微杆菌属Microbacterium 15.07

芽孢杆菌属Bacillus 14.88

10~20 cm

链霉菌属Streptomyces 33.70

节杆菌属Arthrobacter 16.08

芽孢杆菌属Bacillus 44.59

链霉菌属Streptomyces 30.46

类芽孢杆菌属Paenibacillus 11.17

链霉菌属Streptomyces 34.90

微杆菌属Microbacterium 20.21

芽孢杆菌属Bacillus 15.30

节杆菌属Arthrobacter 14.83

链霉菌属Streptomyces 33.67

芽孢杆菌属Bacillus 23.68

微杆菌属Microbacterium 15.02

节杆菌属Arthrobacter 14.09

30~40 cm

链霉菌属Streptomyces 30.69

假单胞菌属Pseudomonas 13.43

金黄杆菌属Chryseobacterium 12.32

芽孢杆菌属Bacillus 52.48

链霉菌属Streptomyces 28.36

链霉菌属Streptomyces 37.46

节杆菌属Arthrobacter 36.84

芽孢杆菌属Bacillus 19.43

链霉菌属Streptomyces 42.52

芽孢杆菌属Bacillus 21.29

微杆菌属Microbacterium 20.95

自生

Free-living

0~10 cm

芽孢杆菌属Bacillus 49.26

链霉菌属Streptomyces 23.10

中华根瘤菌属Sinorhizobium 15.67

链霉菌属Streptomyces 85.37

链霉菌属Streptomyces 49.87

中华根瘤菌属Sinorhizobium 21.97

链霉菌属Streptomyces 83.02

10~20 cm

芽孢杆菌属Bacillus 49.98

链霉菌属Streptomyces 29.93

链霉菌属Streptomyces 89.78

链霉菌属Streptomyces 54.26

中华根瘤菌属Sinorhizobium 28.67

链霉菌属Streptomyces 80.95

中华根瘤菌属Sinorhizobium 10.44

30~40 cm

链霉菌属Streptomyces 48.36

芽孢杆菌属Bacillus 41.38

链霉菌属Streptomyces 93.81

链霉菌属Streptomyces 41.11

芽孢杆菌属Bacillus 36.40

中华根瘤菌属Sinorhizobium 12.74

链霉菌属Streptomyces 86.31

图3 荒漠草原和典型草原小叶锦鸡儿灌丛内外土壤固氮微生物群落组成的非度量多维度尺度分析（NMDS）和ANOSIM检验

Fig.3 Non-metric multi-dimensional scale analysis （NMDS） and ANOSIM test of the soil nitrogen-fixing microbial community composition outside and inside C. microphylla shrub canopies in desert steppe and typical steppe

图4 荒漠草原和典型草原小叶锦鸡儿灌丛内和灌丛外土壤固氮微生物群落的Jaccard相异性指数

Fig.4 The Jaccard dissimilarity index of soil nitrogen-fixing microbial communities between outside and inside C. microphylla shrub canopies in desert steppe and typical steppe

图5 小叶锦鸡儿灌丛内或灌丛外土壤固氮微生物群落在荒漠草原和典型草原之间的Jaccard相异性指数

Fig.5 The Jaccard dissimilarity index of nitrogen-fixing microbial communities between desert steppe and typical steppe outside or inside C. microphylla shrub canopies

表2 荒漠草原和典型草原小叶锦鸡儿灌丛对土壤固氮微生物的选择性物种比例

Table 2 The percentage of selective species of C. microphylla shrub canopies on soil nitrogen-fixing microbial communities in desert steppe and typical steppe （%）

项目 Item	土层 Soil depth	荒漠草原Desert steppe			典型草原Typical steppe
项目 Item	土层 Soil depth	正选择 Positive-selective	负选择 Negative-selective	总选择 Total selective	正选择 Positive-selective	负选择 Negative-selective	总选择 Total selective
共生Symbiotic	0~10 cm	52.94	17.65	70.59	25.00	12.50	37.50
	10~20 cm	27.78	16.67	44.45	6.67	20.00	26.67
	30~40 cm	20.00	20.00	40.00	14.29	28.57	42.86
自生Free-living	0~10 cm	54.55	0.00	54.55	55.56	0.00	55.56
	10~20 cm	44.44	0.00	44.44	37.50	12.50	50.00
	30~40 cm	33.33	16.67	50.00	60.00	20.00	80.00

图6 小叶锦鸡儿灌丛的沃岛效应

Fig.6 Fertile island effect of C. microphylla shrub canopies

图7 土壤固氮微生物和环境因子的冗余分析AP：速效磷Available phosphorous； AK：速效钾Available potassium； OM：有机质Organic matter； WC：含水量Water content； NO3- -N：硝态氮Nitrate nitrogen； NH4+-N：铵态氮Ammonium nitrogen； AI：干旱指数Aridity index.

Fig.7 Relationships between soil nitrogen-fixing microbial community composition and environmental factors by redundancy analysis （RDA）

表3 灌丛和气候干旱对土壤固氮微生物影响的相对重要性

Table 3 The relative effects of shrub canopies and climatic aridity on soil nitrogen-fixing microbial communities （%）

项目 Item	土层 Soil depth	灌丛 Shrub canopies	气候干旱 Climate aridity
共生 Symbiotic	0~10 cm	45.27	16.67
	10~20 cm	53.61	26.47
	30~40 cm	69.03	0.00
自生 Free-living	0~10 cm	74.47	28.69
	10~20 cm	33.61	7.00
	30~40 cm	49.39	0.00

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