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Journal of Integrative Agriculture  2021, Vol. 20 Issue (12): 3230-3239    DOI: 10.1016/S2095-3119(20)63467-0
Special Issue: 线虫合辑Nematology
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Effect of Aspergillus niger NBC001 on the soybean rhizosphere microbial community in a soybean cyst nematode-infested field
JIN Na1, 2, LIU Shi-ming2, PENG Huan2, HUANG Wen-kun2, KONG Ling-an2, PENG De-liang2
1 Department of Horticulture, Beijing Vocational College of Agriculture, Beijing 102442, P.R.China
2 State Key Laboratory for Biology of Plant Diseases and Insect Pests, Institute of Plant Protection, Chinese Academy of Agricultural Sciences, Beijing 100193, P.R.China
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大豆孢囊线虫是世界范围内大豆生产的重要病原之一,生物防治目前已成为大豆孢囊线虫病防治的重要手段。黑曲霉NBC001由本实验室从小麦孢囊线虫群体上分离获得,其发酵液拌种在盆栽中不仅可以有效防治大豆孢囊线虫,而且对大豆具有一定的促生作用。本研究将在田间评价NBC001对大豆孢囊线虫的防治效果及对大豆根际土壤产生的微生态效应。研究结果表明在田间应用黑曲霉NBC001发酵浓缩液拌种可以有效防治大豆孢囊线虫病,防效达31.7%。高通量测序结果显示黑曲霉NBC001对大豆根际土壤微生物多样性和群落结构无显著影响,表明NBC001发酵浓缩液拌种对土壤生态环境安全。在大豆定植10天时,黑曲霉 NBC001促进了大豆根际土壤中放线菌门Actinobacteria,酸杆菌门Acidobacteria,叶瘤菌属Phyllobacterium,雷尔氏菌属Ralstonia和H16的丰度;而降低拟杆菌门Bacteroidetes,芽单胞菌门GemmatimonadetesAdhaeribacter,芽单胞菌属Gemmatimonas,鞘氨醇单胞菌属SphingomonasFlavisolibacter的丰度。在定植90 d时,影响程度减小,仅增加气微菌属Aeromicrobium和RB41属的丰度,降低H16的丰度,说明其对大豆根际土壤微生物物种丰度的影响是短暂的。同时结果也表明黑曲霉NBC001可以增加大豆根际土壤中有益微生物放线菌门、酸杆菌门、气微菌属和叶瘤菌属的丰度。综上所述生防菌黑曲霉NBC001对大豆根际土壤微生物无显著影响,因此在田间应用黑曲霉NBC001对土壤生态环境安全。研究结果将为黑曲霉NBC001的安全应用奠定理论基础,为大豆孢囊线虫病生物防治提供高效生防菌株。

Soybean cyst nematode (SCN, Heterodera glycines Ichinohe) is one of the most important pests causing considerable damage to soybean (Glycine max (L.) Merr.) around the world.  Biocontrol provides a strategy for sustainable nematode control.  Previously, Aspergillus niger NBC001 was isolated from the cysts of Heterodera spp. and able to control H. glycines and promote the growth of soybean in a pot experiment.  In this study, the effects of NBC001 on H. glycines density and on the soybean rhizosphere microbial community in a soybean cyst nematode-infested field were studied.  The results showed that NBC001 could suppress H. glycines by 31.7% in the field.  High-throughput sequencing analysis showed that NBC001 had no significant influence on soybean rhizosphere microbial community structure, indicating that seed coat-dressing with the concentrated culture filtrate of NBC001 was safe for the soil ecological environment.  In addition, high-throughput sequencing results demonstrated that at 10 days post transplantation, NBC001 increased the abundances of Actinobacteria and Acidobacteria, but decreased the abundances of Bacteroidetes and Gemmatimonadetes at the phylum level.  Meanwhile, the abundances of Phyllobacterium, Ralstonia and H16 were increased, while the abundances of Adhaeribacter, Gemmatimonas, Sphingomonas, Flavisolibacter were suppressed by application of NBC001.  However, at 90 days post transplantation, NBC001 only increased the abundances of Aeromicrobium and RB41 whereas it decreased the abundance of H16.  The results indicated that application of NBC001 increased the relative abundances of the beneficial microorganisms such as Actinobacteria, Acidobacteria, Aeromicrobium and Phyllobacterium in the soil.  In summary, NBC001 is an eco-friendly biocontrol agent for H. glycines control. 
Received: 20 August 2020   Accepted:
Fund: This study was supported by the Special Fund for Agro-Scientific Research in the Public Interest, China (201503114), the National Natural Science Foundation of China (31672012) and the National Key Research and Development Program of China (2018YFD0201002).
Corresponding Authors:  Correspondence PENG De-liang, Tel/Fax: +86-10-62815611, E-mail:   
About author:  JIN Na, E-mail:;

Cite this article: 

JIN Na, LIU Shi-ming, PENG Huan, HUANG Wen-kun, KONG Ling-an, PENG De-liang. 2021. Effect of Aspergillus niger NBC001 on the soybean rhizosphere microbial community in a soybean cyst nematode-infested field. Journal of Integrative Agriculture, 20(12): 3230-3239.

Anderson L W, Bloom B S. 2001. A Taxonomy for Learning, Teaching, and Assessing: A Revision of Bloom’s Taxonomy of Educational Objectives. Addison-Wesley, London. pp. 323–331.
Berg G, Zachow C, Cardinale M, Müller H. 2011. Ecology and human pathogenicity of plant-associated bacteria. In: Ehlers R U, ed., Regulation of Biological Control Agents. Springer, USA. pp. 175–189.
Bongers T. 1990. The maturity index: An ecological measure of environmental disturbance based on nematode species composition. Oecologia, 83, 14–19.
Clarke K R, Ainsworth M. 1993. A method of linking multivariate community structure to environmental variables. Marine Ecology Progress Series, 92, 205–205.
Cordier C, Alabouvette C. 2009. Effects of the introduction of a biocontrol strain of Trichoderma atroviride on non target soil micro-organisms. European Journal of Soil Biology, 45, 267–274.
Cruz A F, Barka G D, Sylla J, Reineke A. 2018. Biocontrol of strawberry fruit infected by Botrytis cinerea: Effects on the microbial communities on fruit assessed by next-generation sequencing. Journal of Phytopathology, 166, 403–411.
Cycoń M, Wójcik M, Borymski S, Piotrowska S Z. 2013. Short-term effects of the herbicide napropamide on the activity and structure of the soil microbial community assessed by the multi-approach analysis. Applied Soil Ecology, 66, 8–18.
Dawar S, Sattar A, Zaki M J. 2008. Seed dressing with biocontrol agents and nematicides for the control of root knot nematode on sunflower and okra. Pakistan Journal of Botany, 40, 2683–2691.
Dong L L, Xu J, Zhang L J, Yang J, Liao B S, Li X W, Chen S L. 2017. High-throughput sequencing technology reveals that continuous cropping of American ginseng results in changes in the microbial community in arable soil. Chinese Medicine, 12, 18–24.
Du W, Zhou J, Jiang P, Yang T, Bu Y Q, Liu C H, Dai C C. 2013. Effects of Beauveria bassiana and acephate on enzyme activities and microbial diversity in paddy soil. Plant, Soil and Environment, 59, 562–567.
Dyson Z A, Tucci J, Seviour R J, Petrovski S. 2015. Lysis to kill: evaluation of the lytic abilities, and genomics of nine bacteriophages infective for Gordonia spp. and their potential use in activated sludge foam biocontrol. PLoS ONE, 10, e0134512.
Edgar R C. 2013. UPARSE: Highly accurate OTU sequences from microbial amplicon reads. Nature Methods, 10, 996–1005.
Edgar R C, Haas B J, Clemente J C, Quince C, Knight R. 2011. UCHIME improves sensitivity and speed of chimera detection. Bioinformatics, 27, 2194–2200.
Gasoni L, Khan N, Yokoyama K, Chiessa G H, Kobayashi K. 2008. Impact of Trichoderma harzianum biocontrol agent on functional diversity of soil microbial community in Tobacco monoculture in Argentina. World Journal of Agricultural Sciences, 4, 527–532.
Gaur A C. 1990. Phosphate solubilizing micro-organisms as biofertilizer. Agricultural Science, 1, 225–228.
Haas B J, Gevers D, Earl A M, Feldgarden M, Ward D V, Giannoukos G, Ciulla D, Tabbaa D, Highlander S K, Sodergren E. 2011. Chimeric 16S rRNA sequence formation and detection in Sanger and 454-pyrosequenced PCR amplicons. Genome Research, 21, 494–504.
Henderson D R, Riga E, Ramirez R A, Wilson J, Snyder W E. 2009. Mustard biofumigation disrupts biological control by Steinernema spp. nematodes in the soil. Biological Control, 48, 316–322.
Jang J Y, Choi Y H, Shin T S, Kim T H, Shin K S, Park H W, Kim Y H, Kim H, Choi G J, Jang K S. 2016. Biological control of Meloidogyne incognita by Aspergillus niger F22 producing oxalic acid. PLoS ONE, 11, e0156230.
Jin N, Liu S M, Peng H, Huang W K, Kong L A, Wu Y H, Chen Y P, Ge F Y, Jian H, Peng D L. 2019a. Isolation and characterization of Aspergillus niger NBC001 underlying suppression against Heterodera glycines. Scientific Reports, 9, e591.
Jin N, Lu X L, Wang X Y, Liu Q, Peng D L, Jian H. 2019b. The effect of combined application of Streptomyces rubrogriseus HDZ-9-47 with soil biofumigation on soil microbial and nematode communities. Scientific Reports, 9, e16886.
Jin N, Xue H, Li W J, Wang X Y, Liu Q, Liu S S, Liu P, Zhao J L, Jian H. 2017. Field evaluation of Streptomyces rubrogriseus HDZ-9-47 for biocontrol of Meloidogyne incognita on tomato. Journal of Integrative Agriculture, 16, 1347–1357.
Kõljalg U, Nilsson R H, Abarenkov K, Tedersoo L, Taylor A F S, Bahram M, Bates S T, Bruns T D, Bengtsson P J, Callaghan T M, Douglas B, Drenkhan T, Eberhardt U, Duenas M, Grebenc T, Griffith G W, Hartmann M, Kirk P M,  Kohout P, Larsson E, et al. 2013. Towards a unified paradigm for sequence-based identification of fungi. Molecular Ecology, 22, 5271–5277.
Klink V P, Hosseini P, Matsye P, Alkharouf N W, Matthews B F. 2009. A gene expression analysis of syncytia laser microdissected from the roots of the Glycine max (soybean) genotype PI 548402 (Peking) undergoing a resistant reaction after infection by Heterodera glycines (soybean cyst nematode). Plant Molecular Biology, 71, 525–567.
Li X Y, Wang X , Zhang S P, Liu D W , Duan Y X, Dong W. 2011. Comparative profiling of the transcriptional response to soybean cyst nematode infection of soybean roots by deep sequencing. Science Bulletin, 56, 1904–1911.
Liang X, Fu Y M, Liu H. 2015. Isolation and characterization of enzyme-producing bacteria of the silkworm larval gut in bioregenerative life support system. Acta Astronautica, 116, 247–253.
Martin M. 2011. Cutadapt removes adapter sequences from high-throughput sequencing reads. European Molecular Biology Network Journal, 17, 10–12.
Medda S, Hajra A, Dey U, Bose P, Mondal N K. 2015. Biosynthesis of silver nanoparticles from Aloe vera leaf extract and antifungal activity against Rhizopus sp. and Aspergillus sp. Applied Nanoscience, 5, 875–880.
Mielke P W. 1979. On asymptotic non-normality of null distributions of MRPP statistics. Communications in Statistics (Theory and Methods), 8, 1541–1550.
Ou S Q, Peng D L, Liu X M, Li Y, Moens M. 2008. Identification of Heterodera glycines using PCR with sequence characterised amplified region (SCAR) primers. Nematology, 10, 397–403.
Palaniyandi S A, Yang S H, Zhang L X, Su J W. 2013. Effects of actinobacteria on plant disease suppression and growth promotion. Applied Microbiology and Biotechnology, 97, 9621–9636.
Peng D L, Peng H, Wu D Q, Huang W K, Ye W X, Cui J K. 2016. First report of soybean cyst nematode (Heterodera glycines) on soybean from Gansu and Ningxia China. Plant Disease, 100, 229–229.
Rojas A, Holguin G, Glick B R, Bashan Y. 2001. Synergism between Phyllobacterium sp. (N2-fixer) and Bacillus licheniformis (P-solubilizer), both from a semiarid mangrove rhizosphere. FEMS Microbiology Ecology, 35, 181–187.
Vázquez M M, César S, Azcón R, Barea J M. 2000. Interactions between arbuscular mycorrhizal fungi and other microbial inoculants (Azospirillum, Pseudomonas, Trichoderma) and their effects on microbial population and enzyme activities in the rhizosphere of maize plants. Applied Soil Ecology, 15, 261–272.
Vuong T D, Sleper D A, Shannon J G, Nguyen H T. 2010. Novel quantitative trait loci for broad-based resistance to soybean cyst nematode (Heterodera glycines Ichinohe) in soybean PI 567516C. Theoretical and Applied Genetics, 121, 1253–1257.
Walters W, Hyde E R, Donna B L, Ackermann G, Humphrey G, Parada A, Gilbert J A, Jansson J K, Caporaso J G, Fuhrman J A. 2016. Improved bacterial 16S rRNA gene (V4 and V4–5) and fungal internal transcribed spacer marker gene primers for microbial community surveys. Msystems, 1, 9–15.
Xu X L, Zhang C, Huang X L, Zhang X, Liu Y G. 2014. Community diversity of dendrocola mycoflora in spruce needles. Journal of Northeast Forestry University, 42, 122–125.
Yadav A N, Sachan S G, Verma P, Saxena A K. 2015. Prospecting cold deserts of north western Himalayas for microbial diversity and plant growth promoting attributes. Journal of Bioscience and Bioengineering, 119, 683–693.
Yin D H, Wang N, Xia F, Li Q, Wang W. 2013. Impact of biocontrol agents Pseudomonas fluorescens 2P24 and CPF10 on the bacterial community in the cucumber rhizosphere. European Journal of Soil Biology, 59, 36–42.
Zuckerman B M, Matheny M, Acosta N. 1994. Control of plant-parasitic nematodes by a nematicidal strain of Aspergillus niger. Journal of Chemical Ecology, 20, 33–43.
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