Abstract
The application of nematicidal microorganisms and their virulence factors provides more opportunities to control root-knot nematodes. Bacillus altitudinis AMCC 1040, previously isolated from suppressive soils, showed significant nematicidal activity, and in this study, nematicidal substances produced by Bacillus altitudinis AMCC 1040 were investigated. The results of the basic properties of active substances showed that these compounds have good thermal stability and passage, are resistant to acidic environment and sensitive to alkaline conditions. Further analysis showed that it is a volatile component. Using HS-SPME-GC/MS, the volatile compounds produced by Bacillus altitudinis AMCC 1040 were identified and grouped into four major categories: ethers, alcohols, ketone, and organic acids, comprising a total of eight molecules. Six of them possess nematicidal activities, including 2,3-butanedione, acetic acid, 2-isopropoxy ethylamine, 3-methylbutyric acid, 2-methylbutyric acid and octanoic acid. Our results further our understanding of the effects of Bacillus altitudinis and its nematicidal metabolites on the management of Meloidogyne incognita and may help in finding less toxic nematicides to control root knot nematodes.
Similar content being viewed by others
References
Ali T, Mubeen M, Jamil Y, Ahmad U, Khan HA, Aiman IS, Baber Y, Hassan F, Usman HM, Sohail MA, Abbas A (2021) An overview of root-knot nematodes and their management. J Entomol Zool Stud 9(1):35–40
Barros AF, Campos VP, Da Silva JCP, Pedroso MP, Medeiros FHV, Pozza EA, Reale AL (2014) Nematicidal activity of volatile organic compounds emitted by Brassica juncea, Azadirachta indica, Canavalia ensiformis, Mucuna pruriens and Cajanus cajan against Meloidogyne incognita. Appl Soil Ecol 80:34–43. https://doi.org/10.1016/j.apsoil.2014.02.011
Bi Y, Gao C, Yu Z (2018) Rhabdopeptides from Xenorhabdus budapestensis SN84 and their nematicidal activities against Meloidogyne incognita. J Agr Food Chem 66:3833–3839. https://doi.org/10.1021/acs.jafc.8b00253
Castaneda-Alvarez C, Aballay E (2016) Rhizobacteria with nematicide aptitude: enzymes and compounds associated. World J Microb Biot 32:137. https://doi.org/10.1007/s11274-016-2165-6
Chen X, Jia H, Li Z, Xu X (2019) Synthesis and nematicidal evaluation of 1,2,3-benzotriazin-4-one derivatives containing piperazine as linker against Meloidogyne incognita Chinese. Chem Lett 30:1207–1213. https://doi.org/10.1016/j.cclet.2019.02.033
Cheng W, Yang J, Nie Q, Huang D, Yu C, Zheng L, Cai M, Thomashow LS, Weller DM, Yu Z, Zhang J (2017) Volatile organic compounds from Paenibacillus polymyxa KM2501–1 control Meloidogyne incognita by multiple strategies. Sci Rep. https://doi.org/10.1038/s41598-017-16631-8
Collange B, Navarrete M, Peyre G, Mateille T, Tchamitchian M (2011) Root-knot nematode (Meloidogyne) management in vegetable crop production: the challenge of an agronomic system analysis. Crop Prot 30:1251–1262. https://doi.org/10.1016/j.cropro.2011.04.016
Eloh K, Demurtas M, Deplano A, Ngoutane MA, Murgia A, Maxia A, Onnis V, Caboni P (2015) In vitro nematicidal activity of aryl hydrazones and comparative GC-MS metabolomics analysis. J Agr Food Chem 63:9970–9976. https://doi.org/10.1021/acs.jafc.5b04815
Estupiñan-López L, Campos VP, Da Silva Júnior JC, Pedroso MP, Terra WC, Da Silva JCP, de Paula LL (2018) Volatile compounds produced by Fusarium spp. isolated from Meloidogyne paranaensis egg masses and corticous root tissues from coffee crops are toxic to Meloidogyne incognita. Trop Plant Patholog 43:183–193. https://doi.org/10.1007/s40858-017-0202-0
Freire ES, Campos VP, Pinho RSC, Oliveira DF, Faria MR, Pohlit AM, Noberto NP, Rezende EL, Pfenning LH, Silva JRC (2012) Volatile substances produced by Fusarium oxysporum from coffee rhizosphere and other microbes affect Meloidogyne incognita and Arthrobotrys conoides. J Nematol 44:321–328. https://doi.org/10.1186/1742-9994-9-34
Gu Y, Mo M, Zhou J, Zou C, Zhang K (2007) Evaluation and identification of potential organic nematicidal volatiles from soil bacteria. Soil Biol and Biochem 39:2567–2575. https://doi.org/10.1016/j.soilbio.2007.05.011
Hwang C, Chen Y, Luo C, Chiang W (2016) Antioxidant and antibacterial activities of peptide fractions from flaxseed protein hydrolysed by protease from Bacillus altitudinis HK02. Int J Food Sci Tech 51:681–689. https://doi.org/10.1111/ijfs.13030
Jones JT, Haegeman A, Danchin EG, Gaur HS, Helder J (2013) Top 10 plant-parasitic nematodes in molecular plant pathology. Mol Plant Pathol 14:946–961. https://doi.org/10.1111/mpp.12057
Kanchiswamy CN, Malnoy M, Maffei ME (2015) Chemical diversity of microbial volatiles and their potential for plant growth and productivity. Front Plant Sci. https://doi.org/10.3389/fpls.2015.00151
Kaur T, Jasrotia S, Ohri P, Manhas RK (2016a) Evaluation of in vitro and in vivo nematicidal potential of a multifunctional streptomycete, Streptomyces hydrogenans strain DH16 against Meloidogyne incognita. Microbio Res 192:247–252. https://doi.org/10.1016/j.micres.2016a.07.009
Kaur T, Kaur A, Sharma V, Manhas RK (2016b) Purification and characterization of a new antifungal compound 10-(2,2-dimethyl-cyclohexyl)-6,9-dihydroxy-4,9-dimethyl-dec-2-enoic acid methyl ester from Streptomyces hydrogenans strain DH16. Front Microbiol. https://doi.org/10.3389/fmicb.2016b.01004
Li M, Wen F, Ying H, He MM, Qin XJ, Qing DY, Huang FD, Hui YS (2012) A strategy to discover potential nematicidal fumigants based on toxic volatiles from nematicidal bacteria. Africa J of Microbio Res 6:6106–6113. https://doi.org/10.5897/AJMR12.1328
Li J, Zou C, Xu J, Ji X, Niu X, Yang J, Huang X, Zhang K (2015) Molecular mechanisms of nematode-nematophagous microbe interactions: basis for biological control of plant-parasitic nematodes. Annu Rev Phytopathol 53:67–95. https://doi.org/10.1146/annurev-phyto-080614-120336
Li B, Wang B, Pan P, Li P, Qi Z, Zhang Q, Shi C, Hao W, Zhou B, Lin R (2019) Bacillus altitudinis strain AMCC 101304: a novel potential biocontrol agent for potato common scab. Biocontrol Sci Techn 29:1009–1022. https://doi.org/10.1080/09583157.2019.1641791
Liarzi O, Bucki P, Braun MS, Ezra D (2016) Bioactive volatiles from an endophytic Daldinia cf. concentrica isolate affect the viability of the plant parasitic nematode Meloidogyne javanica. PLoS ONE 11:e0168437. https://doi.org/10.1371/journal.pone.0168437
Marin-Bruzos M, Susan JG (2019) Biological control of nematodes by plant growth promoting rhizobacteria. Second Metab Involv Potent Appl. https://doi.org/10.1007/978-981-13-5862-3_13
Masahiko K, Chikako K, Shingo U, Eiichi O, Taeko T, Takayuki M (2009) Nematicidal activity of volatile fatty acids generated from wheat bran in reductive soil disinfestation. Nematological Res 39:53–62. https://doi.org/10.3725/jjn.39.53
Murungi LK, Kirwa H, Coyne D, Teal PEA, Beck JJ, Torto B (2018) Identification of key root volatiles signaling preference of tomato over spinach by the root knot nematode Meloidogyne incognita. J Agric Food Chem 66:7328–7336. https://doi.org/10.1021/acs.jafc.8b03257
Ni X, Kathy SL, Joseph WK, Patricia AD, John AM (2017) Biological control of Meloidogyne incognita by spore-forming plant growth-promoting rhizobacteria on cotton. Plant Dis 101:774–784. https://doi.org/10.1094/PDIS-09-16-1369-RE
Rajer FU, Wu H, Xie Y, Xie S, Raza W, Tahir HAS, Gao X (2017) Volatile organic compounds produced by a soil-isolate, Bacillus subtilis FA26 induce adverse ultra-structural changes to the cells of Clavibacter michiganensis ssp. sepedonicus, the causal agent of bacterial ring rot of potato. Microbiology 163:523–530. https://doi.org/10.1099/mic.0.000451
Seo S, Kim J, Koh S, Ahn Y, Park I (2014) Nematicidal activity of natural ester compounds and their analogues against pine wood nematode, Bursaphelenchus xylophilus. J Agric Food Chem 62:9103–9108. https://doi.org/10.1021/jf503631e
Sharma A, Sharma S, Dalela M (2014) Nematicidal activity of Paecilomyces lilacinus 6029 cultured on Karanja cake medium. Microb Pathogenes 75:16–20. https://doi.org/10.1016/j.micpath.2014.08.007
Shivaji S, Chaturvedi P, Suresh K, Reddy GSN, Dutt CBS, Wainwright M, Narlikar JV, Bhargava PM (2006) Bacillus aerius sp. nov., Bacillus aerophilus sp. nov., Bacillus stratosphericus sp. nov. and Bacillus altitudinis sp. nov., isolated from cryogenic tubes used for collecting air samples from high altitudes. Int J Syst Evol Micr 56:1465–1473. https://doi.org/10.1099/ijs.0.64029-0
Song GC, Ryu CM (2013) Two volatile organic compounds trigger plant self-defense against a bacterial pathogen and a sucking insect in cucumber under open field conditions. Int J of Mol Sci 14:9803–9819. https://doi.org/10.3390/ijms14059803
Terra WC, Campos VP, Pedroso MP, Da Costa AL, Freire ES, de Pinto IP, Da Silva JCP, Lopez LE, Santos TCN (2017) Volatile molecules of Fusarium oxysporum strain 21 are retained in water and control Meloidogyne incognita. Biol Control 112:34–40. https://doi.org/10.1016/j.biocontrol.2017.06.004
Tian B, Yang J, Zhang KQ (2007) Bacteria used in the biological control of plant-parasitic nematodes: populations, mechanisms of action, and future prospects. FEMS Microbiol Ecol 61:197–213. https://doi.org/10.1111/j.1574-6941.2007.00349.x
Wang L, Boussetta N, Lebovka N, Vorobiev E (2019) Ultrasound assisted purification of polyphenols of apple skins by adsorption/desorption procedure. Ultrason Sonochem 55:18–24. https://doi.org/10.1016/j.ultsonch.2019.03.002
Wang JY, Guo C, Zhao P, Yu FY, Su Y, Qu JP, Wang JL, Lin RS, Wang B, Gao Z, Yang ZY, Zhou B (2021a) Biocontrol potential of Bacillus altitudinis AMCC1040 against root-knot nematode disease of ginger and its impact on rhizosphere microbial community. Biol Control 158:104598. https://doi.org/10.1016/j.biocontrol.2021a.104598
Wang JY, Zhang XC, Guo C, Li PG, Yu FY, Zhao P, Li G, Lin RS, Zhang XY, Wang B, Gao Z, Zhou B (2021b) Diversity and nematocidal activity of culturable bacteria from suppressive soils in Shandong province, China. Biocontrol Sci Tech 31:387–399. https://doi.org/10.1080/09583157.2020.1854176
Yu J, Du G, Li R, Li L, Li Z, Zhou C, Chen C, Guo D (2015) Nematicidal activities of bacterial volatiles and components from two marine bacteria, Pseudoalteromonas marina strain H-42 and Vibrio atlanticus strain S-16, against the pine wood nematode, Bursaphelenchus xylophilus. Nematology 17:1011–1025. https://doi.org/10.1163/15685411-00002920
Zhai Y, Shao Z, Cai M, Zheng L, Li G, Huang D, Cheng W, Thomashow LS, Weller DM, Yu Z, Zhang J (2018) Multiple modes of nematode control by volatiles of Pseudomonas putida 1A00316 from antarctic soil against Meloidogyne incognita. Front Microbiol. https://doi.org/10.3389/fmicb.2018.00253
Zhang W, Ruan W, Deng Y, Gao Y (2012) Potential antagonistic effects of nine natural fatty acids against Meloidogyne incognita. J Agr Food Chem 60:11631–11637. https://doi.org/10.1021/jf3036885
Funding
This work was supported by the Key R&D project of Shandong Province (2020CXGC010803), Major Applied Agricultural Technology Innovation Projects of Shandong Province (SD2019ZZ009), Key R&D project of Ningxia Hui Autonomous Region (2021BBF02006) and Quancheng Scholars Program of Jinan, China (No.00262019026), Shandong Provincial Natural Science Foundation, China (ZR2021MC183) and Modern Agricultural Industry Technology System of Shandong Province, China (SDAIT-06–13).
Author information
Authors and Affiliations
Contributions
All authors contributed to the study conception and design. Material preparation and data collection and analysis were performed by all authors. The first draft of the manuscript was written by YL and J-YW, all authors commented on previous versions of the manuscript. All authors read and approved the final manuscript.
Corresponding authors
Ethics declarations
Conflict of interest
The authors declare that they have no conflict of interest.
Additional information
Communicated by Erko Stackebrandt.
Publisher's Note
Springer Nature remains neutral with regard to jurisdictional claims in published maps and institutional affiliations.
Rights and permissions
About this article
Cite this article
Ye, L., Wang, JY., Liu, XF. et al. Nematicidal activity of volatile organic compounds produced by Bacillus altitudinis AMCC 1040 against Meloidogyne incognita. Arch Microbiol 204, 521 (2022). https://doi.org/10.1007/s00203-022-03024-3
Received:
Accepted:
Published:
DOI: https://doi.org/10.1007/s00203-022-03024-3