The common garden environment and genetic differentiation jointly influence the diversity and community structure of nitrogen-fixing bacteria in the rhizosphere soil of three Caragana species

doi:10.17520/biods.2022477

Abstract

Abstract:

Aim: Environmental and genetic factors are believed to be the main drivers of variation of plant function traits, which may further influence rhizosphere soil bacteria through root exudates. However, it still remains unclear whether the genetic differentiation would affect the diversity and community structure of nitrogen-fixing bacteria in the rhizosphere soil of plant species.

Method: A common garden experiment was established to examine the diversity and community structure of nitrogen-fixing bacteria in the rhizosphere soil of three Caragana from different provenances by using high-throughput sequencing techniques, which was subsequently correlated with the provenance climates and common garden soil properties to investigate how the environmental factor and genetic differentiation affect the rhizosphere nitrogen-fixing bacterial diversity and community structure.

Result: The present results demonstrated that the rhizosphere nitrogen-fixing bacteria of three Caragana species belonged to 6 phyla, 9 classes, 18 orders, 21 families, 33 genera and 72 species. Proteobacteria, Verrucomicrobia and Cyanobacteria were the main dominant phyla of the three Caragana species of nitrogen-fixing bacteria in the rhizosphere soil, and Mesorhizobium, Azohydromonas and Bradyrhizobium were the dominant genera. There were no significant differences in the diversity and community structure of rhizosphere nitrogen-fixing bacteria among the three Caragana species, but significant differences in the α diversity index between provenances were observed in C. liouana and C. roborovskyi (P < 0.05). The community structure between provenances of C. microphylla and C. roborovskyiwas also significant (P < 0.05). Furthermore, redundancy analysis showed that soil pH of the common garden and mean annual temperature (MAT) of provenance were the dominant factors respectively affecting the diversity and community of rhizosphere nitrogen-fixing bacteria of the three Caragana species.

Conclusion: In summary, our results indicate that the common garden environment and genetic differentiation jointly shape the diversity and community structure of nitrogen-fixing bacteria in the rhizosphere soil of Caragana species. This research can provide important theoretical basis and data support for the ecological adaptation mechanism and introduction and cultivation of Caragana.

Key words: Caragana, common garden, nitrogen-fixing bacteria, diversity and community structure, provenance climate

Lulu Wei, Tingting Xu, Yuanyuan Li, Zhe Ai, Fei Ma. The common garden environment and genetic differentiation jointly influence the diversity and community structure of nitrogen-fixing bacteria in the rhizosphere soil of three Caragana species[J]. Biodiv Sci, 2023, 31(4): 22477.

Add to citation manager EndNote|Ris|BibTeX

URL: https://www.biodiversity-science.net/EN/10.17520/biods.2022477

https://www.biodiversity-science.net/EN/Y2023/V31/I4/22477

Figures/Tables 9

References 46

[1]	Abdelfattah A, Wisniewski M, Schena L, Tack A (2021) Experimental evidence of microbial inheritance in plants and transmission routes from seed to phyllosphere and root. Environmental Microbiology, 23, 2199-2214. DOI PMID
[2]	Albaugh TJ, Fox TR, Maier CA, Campoe OC, Rubilar RA, Cook RL, Raymond JE, Alvares CA, Stape JL (2018) A common garden experiment examining light use efficiency and heat sum to explain growth differences in native and exotic Pinus taeda. Forest Ecology and Management, 425, 35-44. DOI URL
[3]	Baker KL, Langenheder S, Nicol GW, Ricketts D, Killham K, Campbell CD, Prosser JI (2009) Environmental and spatial characterisation of bacterial community composition in soil to inform sampling strategies. Soil Biology and Biochemistry, 41, 2292-2298. DOI URL
[4]	Bao SD (2000) Soil Agrochemical Analysis. China Agriculture Press, Beijing. (in Chinese)
	[ 鲍士旦 (2000) 土壤农化分析. 中国农业出版社, 北京.]
[5]	Berendsen RL, Pieterse CMJ, Bakker PAHM (2012) The rhizosphere microbiome and plant health. Trends in Plant Science, 17, 478-486. DOI PMID
[6]	Bowen JL, Kearns PJ, Byrnes JEK, Wigginton S, Allen WJ, Greenwood M, Tran K, Yu J, Cronin JT, Meyerson LA (2017) Lineage overwhelms environmental conditions in determining rhizosphere bacterial community structure in a cosmopolitan invasive plant. Nature Communications, 8, 433. DOI PMID
[7]	Che RX, Deng YC, Wang F, Wang WJ, Xu ZH, Hao YB, Xue K, Zhang B, Tang L, Zhou HK, Cui XY (2018) Autotrophic and symbiotic diazotrophs dominate nitrogen-fixing communities in Tibetan grassland soils. Science of the Total Environment, 639, 997-1006. DOI URL
[8]	Delgado-Baquerizo M, Fry EL, Eldridge DJ, de Vries FT, Manning P, Hamonts K, Kattge J, Boenisch G, Singh BK, Bardgett RD (2018) Plant attributes explain the distribution of soil microbial communities in two contrasting regions of the globe. New Phytologist, 219, 574-587. DOI PMID
[9]	Geng LL, Shao GX, Ben R, Wang ML, Sun XX, Shu CL, Zhang J (2018) Subterranean infestation by Holotrichia parallela larvae is associated with changes in the peanut (Arachis hypogaea L.) rhizosphere microbiome. Microbiological Research, 211, 13-20. DOI URL
[10]	Guo HY, Gao YB, Ma CC, Ren AZ, Wu JB, Wang YH (2008) Genetic diversity and genetic relationship of Caragana microphylla, Caragana davazamcii and Caragana korshinskii in Inner Mongolia Plateau. Acta Ecologica Sinica, 28, 3729-3736. (in Chinese with English abstract) DOI URL
	[ 郭宏宇, 高玉葆, 马成仓, 任安芝, 吴建波, 王银华 (2008) 内蒙古高原小叶锦鸡儿(Caragana microphylla)、中间锦鸡儿(C. davazamcii)和柠条锦鸡儿(C. korshinskii)的遗传多样性及遗传关系. 生态学报, 28, 3729-3736.]
[11]	Haas BJ, Gevers D, Earl AM, Feldgarden M, Ward DV, Giannoukos G, Ciulla D, Tabbaa D, Highlander SK, Sodergren E, Methé B, DeSantis TZ, Consortium HM, Petrosino JF, Knight R, Birren BW (2011) Chimeric 16S rRNA sequence formation and detection in Sanger and 454-pyrosequenced PCR amplicons. Genome Research, 21, 494-504. DOI PMID
[12]	Hu XJ, Liu JJ, Zhu P, Wei D, Jin J, Liu XB, Wang GH (2018) Long-term manure addition reduces diversity and changes community structure of diazotrophs in a neutral black soil of northeast China. Journal of Soils and Sediments, 18, 2053-2062. DOI
[13]	Jason R, Siefert JL, Staples CR, Blankenship RE (2004) The Natural History of Nitrogen Fixation. Molecular Biology and Evolution, 21, 541-554. PMID
[14]	Ji RX, Yu X, Chang Y, Shen C, Bai XQ, Xia XL, Yin WL, Liu C (2020) Geographical provenance variation of leaf anatomical structure of Caryopteris mongholica and its significance in response to environmental changes. Chinese Journal of Plant Ecology, 44, 277-286. (in Chinese with English abstract) DOI URL
	[ 纪若璇, 于笑, 常远, 沈超, 白雪卡, 夏新莉, 尹伟伦, 刘超 (2020) 蒙古莸叶片解剖结构的地理种源变异及其对环境变化响应的意义. 植物生态学报, 44, 277-286.] DOI
[15]	Li YY, Xu TT, Ai Z, Ma F (2021) Fungal community diversity and driving factors in rhizosphere soil of Caragana species across semi-arid regions, China. Chinese Journal of Applied Ecology, 32, 4289-4297. (in Chinese with English abstract)
	[ 李媛媛, 徐婷婷, 艾喆, 马飞 (2021) 半干旱区锦鸡儿属植物根际土壤真菌群落多样性及驱动因素. 应用生态学报, 32, 4289-4297.] DOI
[16]	Li YY, Xu TT, Ai Z, Wei LL, Ma F (2022) Differences in bacterial community structure in rhizosphere soil of three Caragana species and its driving factors in a common garden experiment, China. Environmental Science, 43, 3854-3864. (in Chinese with English abstract)
	[ 李媛媛, 徐婷婷, 艾喆, 魏庐潞, 马飞 (2022) 同质环境下不同锦鸡儿属植物根际土壤细菌群落结构差异及其影响因素. 环境科学, 43, 3854-3864.]
[17]	Lin YX, Ye GP, Liu DY, Ledgard S, Luo JF, Fan JB, Yuan JJ, Chen ZM, Ding WX (2018) Long-term application of lime or pig manure rather than plant residues suppressed diazotroph abundance and diversity and altered community structure in an acidic Ultisol. Soil Biology and Biochemistry, 123, 218-228. DOI URL
[18]	Liu S, Wang JG, Ci ZL, Bai SL, Shao DH (2012) AMF diversity in Caragana in different habitats of Oerhtossu Plateau, China. Journal of Inner Mongolia Agricultural University (Natural Science Edition), 33(4), 74-80. (in Chinese with English abstract)
	[ 刘声, 王琚钢, 慈忠玲, 白淑兰, 邵东华 (2012) 鄂尔多斯高原不同生境锦鸡儿属植物AMF多样性. 内蒙古农业大学学报, 33(4), 74-80.]
[19]	Lladó S, Jiménez N, Viñas M, Solanas AM (2009) Microbial populations related to PAH biodegradation in an aged biostimulated creosote-contaminated soil. Biodegradation, 20, 593-601. DOI PMID
[20]	Ma F, Xu TT, Li M, Liu JL, Wang J, Zhao LX, Wang HJ, Na XF (2017) Effect of plantation of Caragana species on soil properties and bacterial community dynamics in saline-alkali soil. Acta Botanica Boreali-Occidentalia Sinica, 37, 1872-1880. (in Chinese with English abstract)
	[ 马飞, 徐婷婷, 李明, 刘吉利, 王静, 赵聆希, 王贺瑾, 纳小凡 (2017) 锦鸡儿植物对盐碱地土壤理化性质和细菌群落的影响. 西北植物学报, 37, 1872-1880.]
[21]	Ma RP, Dai XL, Liu GY, Xie YC, Gao XL, Gao X (2021) Effects of fertilizer patterns on the potential nitrogen fixation rate and community structure of asymbiotic diazotroph in highland barley fields on the Tibetan Plateau. Chinese Journal of Eco-Agriculture, 29, 1692-1703. (in Chinese with English abstract)
	[ 马瑞萍, 戴相林, 刘国一, 谢永春, 高小丽, 高雪 (2021) 施肥模式对青稞田土壤潜在固氮速率和自生固氮微生物群落结构的影响. 中国生态农业学报, 29, 1692-1703.]
[22]	Ma XY, Liu LL, Yin MQ, Song HJ, Zhu PC, Yu XN, Du N, Wang RQ, Guo WH (2021) Variation in plant functional traits of Phragmites australis based on field investigation and common garden experiment. Acta Ecologica Sinica, 41, 3755-3764. (in Chinese with English abstract)
	[ 马香艳, 刘乐乐, 尹美淇, 宋慧佳, 朱鹏程, 于晓娜, 杜宁, 王仁卿, 郭卫华 (2021) 基于野外调查和同质种植园实验的芦苇植物功能性状变异研究. 生态学报, 41, 3755-3764.]
[23]	Na XF, Xu TT, Li M, Zhou ZN, Ma SL, Wang J, He J, Jiao BZ, Ma F (2018) Variations of bacterial community diversity within the rhizosphere of three phylogenetically related perennial shrub plant species across environmental gradients. Frontiers in Microbiology, 9, 709. DOI PMID
[24]	Nie G, Chen WM, Wei GH (2014) Genetic diversity of rhizobia isolated from shrubby and herbaceous legumes in Shenmu arid area, China. Chinese Journal of Applied Ecology, 25, 1674-1680. (in Chinese with English abstract)
	[ 聂刚, 陈卫民, 韦革宏 (2014) 神木地区耐旱灌木和草本豆科植物根瘤菌遗传多样性. 应用生态学报, 25, 1674-1680.]
[25]	Peiffer JA, Spor A, Koren O, Jin Z, Tringe SG, Dangl JL, Buckler ES, Ley RE (2013) Diversity and heritability of the maize rhizosphere microbiome under field conditions. Proceedings of the National Academy of Sciences of the USA, 110, 6548-6553.
[26]	Quast C, Pruesse E, Yilmaz P, Gerken J, Schweer T, Yarza P, Peplies J, Glöckner FO (2013) The SILVA ribosomal RNA gene database project: Improved data processing and web-based tools. Nucleic Acids Research, 41, D590-D596.
[27]	Rösch C, Mergel A, Bothe H (2002) Biodiversity of denitrifying and dinitrogen-fixing bacteria in an acid forest soil. Applied and Environmental Microbiology, 68, 3818-3829. DOI PMID
[28]	Vitousek P, Cassman K, Cleveland C, Crews T, Field C, Grimm N, Howarth R, Marino R, Martinelli L, Rastetter E, Sprent J (2002) Towards an ecological understanding of biological nitrogen fixation. Biogeochemistry, 57/58, 1-45.
[29]	Wang CC, Zhong QL, Cheng DL, Yu H, Xu CB (2019) Relationship between the leaf functional traits of Zenia insignis and the provenance environments in common gardens during the introduction period. Acta Ecologica Sinica, 39, 4892-4899. (in Chinese with English abstract)
	[ 王楚楚, 钟全林, 程栋梁, 余华, 徐朝斌 (2019) 引种期同质园翅荚木主要叶功能性状与种源地环境关系. 生态学报, 39, 4892-4899.]
[30]	Wang J, Bao JT, Li XR, Liu YB (2016) Molecular ecology of nifH genes and transcripts along a chronosequence in revegetated areas of the Tengger Desert. Microbial Ecology, 71, 150-163. DOI PMID
[31]	Wang JM, Wang Y, He NP, Ye ZQ, Chen C, Zang RG, Feng YM, Lu Q, Li JW (2020) Plant functional traits regulate soil bacterial diversity across temperate deserts. Science of the Total Environment, 715, 136976. DOI URL
[32]	Wang L, Wang J, Zhang AJ, Zhang H, Zhang YC (2020) Effects of long-term organic fertilization on soil diazotrophic community structure and diversity under wheat-sweet potato rotation system. Acta Ecologica Sinica, 40, 5771-5782. (in Chinese with English abstract)
	[ 王磊, 王静, 张爱君, 张辉, 张永春 (2020) 小麦-甘薯轮作长期增施有机肥对碱性土壤固氮菌群落结构及多样性的影响. 生态学报, 40, 5771-5782.]
[33]	Wang Q, Garrity GM, Tiedje JM, Cole JR (2007) Naive Bayesian classifier for rapid assignment of rRNA sequences into the new bacterial taxonomy. Applied and Environmental Microbiology, 73, 5261-5267. DOI PMID
[34]	Wang YS, Li CN, Kou YP, Wang JJ, Tu B, Li H, Li XZ, Wang CT, Yao MJ (2017) Soil pH is a major driver of soil diazotrophic community assembly in Qinghai-Tibet alpine meadows. Soil Biology and Biochemistry, 115, 547-555.
[35]	Wang YS, Li CN, Shen ZH, Rui JP, Jin DC, Li JB, Li XZ (2019) Community assemblage of free-living diazotrophs along the elevational gradient of Mount Gongga. Soil Ecology Letters, 1, 136-146.
[36]	Wang ZM, Li CH, Ma QL, Li QX, Wei YR, Zhao J, Yu JL, Xi NNG (2021) Moisture, salinity and pH co-driving spatial heterogeneity of Verrucomicrobial populations in Xilin River landscape, China. Acta Microbiologica Sinica, 61, 1728-1742. (in Chinese with English abstract)
	[ 王泽铭, 李传虹, 马巧丽, 李千雪, 魏亚茹, 赵吉, 于景丽, 希尼尼根 (2021) 湿度盐度pH协同驱动锡林河景观疣微菌群空间异质性. 微生物学报, 61, 1728-1742.]
[37]	Xu B, Sun GL, Wang XM, Lu JW, Wang IJ, Wang Z (2017) Population genetic structure is shaped by historical, geographic, and environmental factors in the leguminous shrub Caragana microphylla on the Inner Mongolia Plateau of China. BMC Plant Biology, 17, 200. DOI URL
[38]	Xu YD, Zhang W, Zhong ZK, Guo SJ, Han XH, Yang GH, Ren CJ, Chen ZX, Dai YY, Qiao WJ (2019) Vegetation restoration alters the diversity and community composition of soil nitrogen-fixing microorganisms in the loess hilly region of China. Soil Science Society of America Journal, 83, 1378-1386. DOI URL
[39]	Yang YD, Feng XM, Hu YG, Ren CZ, Zeng ZH (2017) Effects of legume-oat intercropping on abundance and community structure of soil N₂-fixing bacteria. Chinese Journal of Applied Ecology, 28, 957-965. (in Chinese with English abstract)
	[ 杨亚东, 冯晓敏, 胡跃高, 任长忠, 曾昭海 (2017) 豆科作物间作燕麦对土壤固氮微生物丰度和群落结构的影响. 应用生态学报, 28, 957-965.] DOI
[40]	Zhang C, Liu GB, Xue S, Wang GL (2016) Soil bacterial community dynamics reflect changes in plant community and soil properties during the secondary succession of abandoned farmland in the Loess Plateau. Soil Biology and Biochemistry, 97, 40-49.
[41]	Zhang P, Li XR, Zhang ZS, Pan YX, Liu YM, Su JQ (2012) Nitrogen fixation potential of biological soil crusts in southeast edge of Tengger Desert, Northwest China. Chinese Journal of Applied Ecology, 23, 2157-2164. (in Chinese with English abstract) PMID
	[ 张鹏, 李新荣, 张志山, 潘艳霞, 刘艳梅, 苏洁琼 (2012) 腾格里沙漠东南缘生物土壤结皮的固氮潜力. 应用生态学报, 23, 2157-2164.] PMID
[42]	Zhang TH, Su YZ, Cui JY, Zhang ZH, Chang XX (2006) A leguminous shrub (Caragana microphylla) in semiarid sandy soils of North China. Pedosphere, 16, 319-325. DOI URL
[43]	Zhang YT, Jiang D, Tang J, Luo YF, Liang YM, Shah MMR, Jin P, Daroch M (2019) Isolation and characterization of two thermophilic Leptolyngbyaceae strains isolated from Huizhou area, China. Microbiology China, 46, 481-493. (in Chinese with English abstract)
	[ 张艳婷, 江东, 唐杰, 雒义凡, 梁园梅, Shah MMR, 金鹏, Daroch M (2019) 两株采自惠州的细鞘丝藻亚科(Leptolyngbyaceae)嗜热蓝细菌的分离鉴定及细胞组分分析. 微生物学通报, 46, 481-493.]
[44]	Zhang YX, Liu F, Duan N, Xu J, Chen HL, Zhang G (2014) Study on drought resistance of 4 species of Caragana, China. Chinese Agricultural Science Bulletin, 30, 25-29. (in Chinese with English abstract)
	[ 章尧想, 刘芳, 段娜, 徐军, 陈海玲, 张格 (2014) 4种锦鸡儿属(Caragana)植物抗旱性研究. 中国农学通报, 30, 25-29.]
[45]	Zhao H, Zhou YC (2020) Characteristics of structure and abundance of the nitrogen-fixing bacterial community in Pinus massoniana soil developed from different parent rocks. Acta Ecologica Sinica, 40, 6189-6201. (in Chinese with English abstract)
	[ 赵辉, 周运超 (2020) 不同母岩发育马尾松土壤固氮菌群落结构和丰度特征. 生态学报, 40, 6189-6201.]
[46]	Zhou ZY, Yu MH, Ding GD, Gao GL, He YY (2020) Diversity of bacterial communities in the rhizocompartments of Caragana in the Mu Us Desert. Journal of Desert Research, 40, 128-137. (in Chinese with English abstract)
	[ 周子渊, 于明含, 丁国栋, 高广磊, 何莹莹 (2020) 毛乌素沙地锦鸡儿(Caragana)根系微域细菌群落多样性特征. 中国沙漠, 40, 128-137.] DOI

样点 Site	东经 Longitude (E)	北纬 Latitude (N)	海拔 ALT (m)	年均温 MAT (℃)	年均降水量 MAP (mm)
CM1	119.15°	42.98°	626	6.23	326.76
CM2	121.88°	44.03°	1,178	6.68	331.43
CM3	114.33°	42.07°	1,419	2.51	325.42
CL1	110.28°	39.33°	1,285	7.34	382.46
CL2	110.15°	39.21°	1,257	7.19	379.92
CL3	107.67°	38.85°	1,344	7.42	225.23
CR1	100.69°	38.48°	2,295	1.71	190.10
CR2	103.15°	36.88°	2,314	5.38	303.75
CR3	101.36°	38.58°	2,032	3.92	158.89

样点 Site	东经 Longitude (E)	北纬 Latitude (N)	海拔 ALT (m)	年均温 MAT (℃)	年均降水量 MAP (mm)
CM1	119.15°	42.98°	626	6.23	326.76
CM2	121.88°	44.03°	1,178	6.68	331.43
CM3	114.33°	42.07°	1,419	2.51	325.42
CL1	110.28°	39.33°	1,285	7.34	382.46
CL2	110.15°	39.21°	1,257	7.19	379.92
CL3	107.67°	38.85°	1,344	7.42	225.23
CR1	100.69°	38.48°	2,295	1.71	190.10
CR2	103.15°	36.88°	2,314	5.38	303.75
CR3	101.36°	38.58°	2,032	3.92	158.89

优势类群 Dominant group	pH	有机碳 SOC	全氮 TN	全磷 TP	电导率 EC	海拔 ALT	年均降水量 MAP	年均温 MAT
门水平 Phylum level
变形菌门 Proteobacteria	?0.316	0.197	0.118	0.228	?0.041	?0.053	?0.113	0.279
疣微菌门 Verrucomicrobia	?0.458^*	0.129	?0.01	0.601^**	0.197	0.234	?0.24	0.047
蓝细菌门 Cyanobacteria	0.192	?0.384^*	?0.317	?0.188	?0.19	0.134	?0.102	0.098
纲水平 Class level
α-变形菌纲 Alphaproteobacteria	?0.345	0.325	0.214	0.14	?0.009	?0.086	?0.063	0.253
丰佑菌纲 Opitutae	?0.458^*	0.129	?0.01	0.601^**	0.197	0.234	?0.24	0.047
β-变形菌纲 Betaproteobacteria	0.055	?0.356	?0.271	0.286	?0.09	0.097	?0.165	0.101
γ-变形菌纲 Gammaproteobacteria	0.169	?0.336	?0.222	?0.036	?0.417^*	?0.047	0.140	0.147
属水平 Genus level
中慢生根瘤菌属 Mesorhizobium	?0.374	0.351	0.237	0.154	0.030	?0.074	?0.084	0.216
固氮氢自养单胞菌属Azohydromonas	0.050	?0.359	?0.261	0.287	?0.089	0.086	?0.149	0.105
慢生根瘤菌属 Bradyrhizobium	0.303	?0.365	?0.299	?0.232	?0.487^**	?0.250	0.416^*	0.406^*
斯科曼氏球菌属 Skermanella	0.317	?0.127	?0.158	0.031	?0.236	0.146	?0.139	0.279
念珠藻属 Nostoc	0.217	?0.486^*	?0.391^*	?0.337	?0.208	?0.037	0.087	0.127

优势类群 Dominant group	pH	有机碳 SOC	全氮 TN	全磷 TP	电导率 EC	海拔 ALT	年均降水量 MAP	年均温 MAT
门水平 Phylum level
变形菌门 Proteobacteria	?0.316	0.197	0.118	0.228	?0.041	?0.053	?0.113	0.279
疣微菌门 Verrucomicrobia	?0.458^*	0.129	?0.01	0.601^**	0.197	0.234	?0.24	0.047
蓝细菌门 Cyanobacteria	0.192	?0.384^*	?0.317	?0.188	?0.19	0.134	?0.102	0.098
纲水平 Class level
α-变形菌纲 Alphaproteobacteria	?0.345	0.325	0.214	0.14	?0.009	?0.086	?0.063	0.253
丰佑菌纲 Opitutae	?0.458^*	0.129	?0.01	0.601^**	0.197	0.234	?0.24	0.047
β-变形菌纲 Betaproteobacteria	0.055	?0.356	?0.271	0.286	?0.09	0.097	?0.165	0.101
γ-变形菌纲 Gammaproteobacteria	0.169	?0.336	?0.222	?0.036	?0.417^*	?0.047	0.140	0.147
属水平 Genus level
中慢生根瘤菌属 Mesorhizobium	?0.374	0.351	0.237	0.154	0.030	?0.074	?0.084	0.216
固氮氢自养单胞菌属Azohydromonas	0.050	?0.359	?0.261	0.287	?0.089	0.086	?0.149	0.105
慢生根瘤菌属 Bradyrhizobium	0.303	?0.365	?0.299	?0.232	?0.487^**	?0.250	0.416^*	0.406^*
斯科曼氏球菌属 Skermanella	0.317	?0.127	?0.158	0.031	?0.236	0.146	?0.139	0.279
念珠藻属 Nostoc	0.217	?0.486^*	?0.391^*	?0.337	?0.208	?0.037	0.087	0.127

α多样性 α diversity			群落结构 Community structure
环境因子 Environmental factor	解释度 Explains (%)	P	环境因子 Environmental factor	解释度 Explains (%)	P
pH	14.5	0.048	年均温 MAT	14.2	0.036
全氮 TN	5.9	0.182	全磷 TP	8.3	0.072
海拔 ALT	6.1	0.196	年均降水量 MAP	7.8	0.108
年均降水量 MAP	5.4	0.238	有机碳 SOC	5.6	0.158
全磷 TP	2.2	0.438	电导率 EC	2.2	0.490
电导率 EC	2	0.454	海拔 ALT	2	0.498
年均温 MAT	0.2	0.848	pH	1.8	0.544
有机碳 SOC	< 0.1	0.902	全氮 TN	0.7	0.838