Pseudomonas and Burkholderia inhibit growth and asexual development of Phytophthora capsici
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Amena Khatun
, Tarin Farhana , Abdullah As Sabir , Shah Mohammad Naimul Islam , Helen M. West , Mahfuzur Rahman und Tofazzal Islam
Abstract
The objective of this study was to isolate and characterize antagonistic rhizobacteria from chili against a notorious phytopathogen Phytophthora capsici. Among the 48 bacteria isolated, BTLbbc-02, BTLbbc-03, and BTLbbc-05 were selected based on their inhibitory activity against P. capsici. They were tentatively identified as Burkholderia metallica BTLbbc-02, Burkholderia cepacia BTLbbc-03, and Pseudomonas aeruginosa BTLbbc-05, respectively, based on their 16S rRNA gene sequencing. All inhibited the growth of P. capsici at varying levels by inducing characteristic morphological alterations of P. capsici hyphae. The cell-free culture supernatant of all three isolates impaired motility (up to 100%) and caused lysis (up to 50%) of the halted zoospores. Bioassays revealed that Pseudomonas sp. had higher antagonism and zoospore motility-inhibitory effects against P. capsici compared with two other isolates, Burkholderia spp. and B. metallica, which caused vacuolation in mycelium. All three bacteria suppressed sporangium formation and zoosporogenesis of P. capsici, and improved the seed germination and growth of cucumber. Our findings suggest that epiphytic bacteria, B. metallica, B. cepacia, and P. aeruginosa, could be used as potential biocontrol agents against P. capsici. A further study is required to ensure conformity with the existing regulations for soil, plant, and human health.
Acknowledgment
The authors are thankful to the World Bank for funding to CP #2071 (Funder ID: 10.13039/100004421) of Higher Education Quality Enhancement Project of University Grants Commission of Bangladesh. Sincere thanks are also due to W. Yuanchao for generously providing the P. capsici strain.
Competing interests: The authors have declared that there are no conflicts of interests that could be observed as influencing the impartiality of this paper.
Author contributions: A.K. performed experiments, analyzed data, and drafted the manuscript. T.F. and A.A.S performed data collection. T.I., S.M.N.I., M.R., and H.M.W. supervised the design of the study and data analysis, and revised the manuscript. All authors critically reviewed the manuscript for intellectual content and gave final approval for the version to be published.
References
1. Sarma YR. Global scenario of disease and pest management in black pepper. Int Pepper News Bull 2003;69–74.Suche in Google Scholar
2. Judelson HS, Blanco FA. The spores of Phytophthora: weapons of the plant destroyer. Nat Rev Microbiol 2005;3:47–58.10.1038/nrmicro1064Suche in Google Scholar PubMed
3. Qi R, Wang T, Zhao W, Li P, Ding J, Gao Z. Activity of ten fungicides against Phytophthora capsici isolates resistant to metalaxyl. J Phytopathol 2012;160:717–22.10.1111/jph.12009Suche in Google Scholar
4. Deacon JW, Donaldson SP. Molecular recognition in the homing responses of zoosporic fungi, with special reference to Pythium and Phytophthora. Mycol Res 1993;97:1153–71.10.1016/S0953-7562(09)81278-1Suche in Google Scholar
5. Kroon LP, Brouwer H, de Cock AW. The genus Phytophthora anno. Phytopathology 2012;102:348–64.10.1094/PHYTO-01-11-0025Suche in Google Scholar PubMed
6. Islam MT, Hashidoko Y, Deora A, Ito T, Tahara, S. Suppression of damping-off disease in host plants by the rhizoplane bacterium Lysobacter sp. strain SB-K88 is linked to plant colonization and antibiosis against soil borne Peronosporomycetes. Appl Environ Microbiol 2005;71:3786–96.10.1128/AEM.71.7.3786-3796.2005Suche in Google Scholar PubMed PubMed Central
7. Islam MT, Hossain MM. Biological control of peronosporomycete phytopathogen by bacterial antagonist. Bact Agrobiol Dis Manage 2013;167–218.10.1007/978-3-642-33639-3_7Suche in Google Scholar
8. Ahmed SU. The dynamics of agricultural land management system in Bangladesh: the challenges for sustainable development. Am J Rural Dev 2017;5:5–18.Suche in Google Scholar
9. Sang MK, Shrestha A, Kim DY, Park K, Pak CH, Kim KD. Biocontrol of Phytophthora blight and anthracnose in pepper by sequentially selected antagonistic rhizobacteria against Phytophthora capsici. Plant Pathol J 2013;29:154–67.10.5423/PPJ.OA.07.2012.0104Suche in Google Scholar PubMed PubMed Central
10. Ryan RP, Germaine K, Franks A, Ryan DJ, Dowling DN. Bacterial endophytes: recent developments and applications. FEMS Microbiol Lett 2008;278:1–9.10.1111/j.1574-6968.2007.00918.xSuche in Google Scholar PubMed
11. Yanga R, Fana X, Caia X, Hu F. The inhibitory mechanisms by mixtures of two endophytic bacterial strains isolated from Ginkgo biloba against pepper Phytophthora blight. Biol Control 2015;85:59–67.10.1016/j.biocontrol.2014.09.013Suche in Google Scholar
12. Chauhana H, Bagyaraja DJ, Selvakumarb G, Sundaram SP. Novel plant growth promoting rhizobacteria – prospects and potential. Appl Soil Ecol 2015;95:38–53.10.1016/j.apsoil.2015.05.011Suche in Google Scholar
13. Fang X, Zhang M, Tang Q, Wang Y, Zhang X. Inhibitory effect of Xenorhabdus nematophila TB on plant pathogens Phytophthora capsici and Botrytis cinerea in vitro and in planta. Sci Rep 2014;6:4300.10.1038/srep04300Suche in Google Scholar
14. Sopheareth M, Chan S, Naing KW, Lee YS, Hyun HN, Kim YC, et al. Biocontrol of late blight (Phytophthora capsici) disease and growth promotion of pepper by Burkholderia cepacia MPC-7. Plant Pathol J 2013;29:67–76.10.5423/PPJ.OA.07.2012.0114Suche in Google Scholar PubMed
15. Yang MM, Xu LP, Xue QY, Yang JH, Xu Q, Liu HX, et al. Screening potential bacterial biocontrol agents towards Phytophthora capsici in pepper. Eur J Plant Pathol 2012;134:811–20.10.1007/s10658-012-0057-7Suche in Google Scholar
16. Zohara F, Akanda MA, Paul NC, Rahman M, Islam MT. Inhibitory effects of Pseudomonas spp. on plant pathogen Phytophthora capsici in vitro and in planta. Biocatal Agric Biotechnol 2016;5:69–77.10.1016/j.bcab.2015.12.009Suche in Google Scholar
17. Chiarini L, Bevivino A, Dalmastri C, Tabacchioni S, Visca P. Burkholderia cepacia complex species: health hazards and biotechnological potential. Trends Microbiol 2006;14: 277–86.10.1016/j.tim.2006.04.006Suche in Google Scholar PubMed
18. Chiarini L, Bevivino A, Tabacchioni S, Dalmastri C. Inoculation of Burkholderia cepacia, Pseudomonas fluorescens and Enterobacter sp. on Sorghum bicolor: root colonization and plant growth promotion of dual strain inocula. Soil Biol Biochem 1988;30:81–7.10.1016/S0038-0717(97)00096-5Suche in Google Scholar
19. Azadeh BF, Sariah M, Wong MY. Characterization of Burkholderia cepacia genomovar I as a potential biocontrol agent of Ganoderma boninense in oil palm. Afr J Biotechnol 2010;9:3542–8.Suche in Google Scholar
20. Sarker A, Islam, MT. Screening and application of PSB for rice production in acidic soil. Saarbrücken, Germany: LAP Lambert Academic Publishing AG&Co KG, 2012.Suche in Google Scholar
21. Islam MT, Hashidoko Y, Tahara S. Understanding of ecochemical interactions between plants and zoospores: potentials for biorational control of the peronosporomycete soil borne phytopathogens. In: Singh DP, editor. Crop Production in Stress Environments: Genetic and Management Options. Jodhpur, India: Agrobios International, 2007;275–88.Suche in Google Scholar
22. Islam MT, Tahara S. Host-specific plant signal and G protein activator, mastoparan, trigger differentiation of zoospores of the phytopathogenic oomycete Aphanomyces cochlioides. Plant Soil 2003;255:131–42.10.1023/A:1026114731718Suche in Google Scholar
23. Chilpa RR, Vazquez IR, Estrada MJ, Ocana AN, Hernandez JC. Antifungal activity of selected plant secondary metabolites against Coriolus versicolor. J Tropic Forest Prod 1997;3:110–3.Suche in Google Scholar
24. Bergey DH, Holt JG, Noel RK. Bergey’s manual of systematic bacteriology, 9th ed. Baltimore, MD: Williams & Wilkins, 1994;1935–2045.Suche in Google Scholar
25. Park M, Kim C, Yang J, Lee H, Shin W, Kim S, et al. Isolation and characterization of diazotrophic growth promoting bacteria from rhizosphere of agricultural crops of Korea. Microbiol Res 2005;160:127–33.10.1016/j.micres.2004.10.003Suche in Google Scholar PubMed
26. Osborne CA, Galic M, Sangwan P, Janssen PH. PCR-generated artefact from 16S rRNA gene-specific primers. FEMS Microbiol Lett 2005;15:248:183–7.10.1016/j.femsle.2005.05.043Suche in Google Scholar PubMed
27. Altschul SF, Madden TL, Schäffer AA, Zhang J, Zhang Z, Miller W, et al. Gapped BLAST and PSI-BLAST: a new generation of protein database search programs. Nucleic Acids Res 1997;25:3389–402.10.1093/nar/25.17.3389Suche in Google Scholar PubMed PubMed Central
28. Kim OS, Cho YJ, Lee K, Yoon SH, Kim M, Na H, et al. Introducing EzTaxon-e: a praokaryotic 16SrRNA gene sequence database with phylotypes that represent uncultured species. Int J Syst Evol Microbiol 2012;62:716–21.10.1099/ijs.0.038075-0Suche in Google Scholar PubMed
29. Bric JM, Bostock RM, Silverstone SE. Rapid in situ assay for indole acetic acid production by bacteria immobilized on a nitrocellulose membrane. Appl Environ Microbiol 1991;57:535–8.10.1128/aem.57.2.535-538.1991Suche in Google Scholar PubMed
30. Gordon SA, Weber RP. Colorimetric estimation of indole acetic acid. Plant Physiol 1951;26:192–5.10.1104/pp.26.1.192Suche in Google Scholar PubMed
31. Vrbničanin S, Božić D, Sarić M, Pavlović D, Raičević V. Effect of plant growth promoting rhizobacteria on Ambrosia artemisiifolia L. seed germination. Pestic Phytomed 2011;26:141–6.10.2298/PIF1102141VSuche in Google Scholar
32. Ramamoorthy V, Raguchander T, Samiyappan R. Induction of defense-related proteins in tomato roots treated with Pseudomonas fluorescens Pf1 and Fusarium oxysporum f. sp. lycopersici. Plant Soil 2002;239:55–68.10.1023/A:1014904815352Suche in Google Scholar
33. Abdul-Baki AA, Anderson JD. Vigor determination in soybean by multiple criteria. Crop Sci 1973;13:630–3.10.2135/cropsci1973.0011183X001300060013xSuche in Google Scholar
34. Mahenthiralingam E, Bischof J, Byrne SK, Radomski C, Davies JE, Av-Gay Y, et al. DNA-based diagnostic approaches for identification of Burkholderia cepacia complex, Burkholderia vietnamiensis, Burkholderia multivorans, Burkholderia stabilis and Burkholderia cepacia genomovars I and III. J Clin Microbiol 2000;38:3165–73.10.1128/JCM.38.9.3165-3173.2000Suche in Google Scholar PubMed
35. Hazem S, Shafie E, Camele I, Racioppi R, Scrano L, Iacobellis NS, et al. In vitro antifungal activity of Burkholderia gladioli pv. agaricicola against some phytopathogenic fungi. Int J Mol Sci 2012;13:16291–302.10.3390/ijms131216291Suche in Google Scholar PubMed
36. Shehata HR, Lyons EM, Jordan KS, Raizada MN. Relevance of in vitro agar based screens to characterize the anti-fungal activities of bacterial endophyte communities. BMC Microbiol 2016;16:8.10.1186/s12866-016-0623-9Suche in Google Scholar PubMed
37. Lee SY. Bacterial polyhydroxyalkanoates. Biotechnol Bioeng 1996;49:1–14.10.1002/(SICI)1097-0290(19960105)49:1<1::AID-BIT1>3.0.CO;2-PSuche in Google Scholar PubMed
38. Aravind R, Kumar A, Eapen SJ, Ramana KV. Endophytic bacterial flora in root and stem tissues of black pepper (Piper nigrum L.) genotype: isolation, identification and evaluation against Phytophthora capsici. Lett Appl Microbiol 2009;48:58–64.10.1111/j.1472-765X.2008.02486.xSuche in Google Scholar PubMed
39. Dinu A, Kumar A, Aravind R, Eapen SJ. Novel in planta assay for selection of antagonistic bacteria against Phytophthora capsici on black pepper (Piper nigrum L). J Spices Aromatic Crops 2007;16:1–7.Suche in Google Scholar
40. Jung SW, Kim BH, Katano T, Kong DS, Han MS. Pseudomonas fluorescens HYK0210-SK09 offers species-specific biological control of winter algal blooms caused by freshwater diatom Stephanodiscus hantzschii. J Appl Microbiol 2008;105:186–95.10.1111/j.1365-2672.2008.03733.xSuche in Google Scholar PubMed
41. Kim, BS, Lee JY, Hwang BK. In vivo control and in vitro antifungal activity of rhamnolipid B, a glycolipid antibiotic, against Phytophthora capsici and Colletotrichum orbiculare. Pest Manag Sci 2000;56:12.10.1002/1526-4998(200012)56:12<1029::AID-PS238>3.0.CO;2-QSuche in Google Scholar
42. Kim BS. Production of medium chain length polyhydroxyalkanoates by fed-batch culture of Pseudomonas oleovorans. Biotechnol Lett 2002;24:125–30.10.1023/A:1013898504895Suche in Google Scholar
43. Rosales AM, Thomashow L, Cook RJ, Mew TW. Isolation and identification of antifungal metabolites produced by rice-associated antagonistic Pseudomonas spp. Phytopathology 1995;85:1028–32.10.1094/Phyto-85-1028Suche in Google Scholar
44. Mao S, Lee SJ, Hwangbo H, Kim YW, Park KH, Cha GS, et al. Isolation and characterization of antifungal substances from Burkholderia sp. culture broth. Curr Microbiol 2006;53:358–64.10.1007/s00284-005-0333-2Suche in Google Scholar PubMed
45. Veses V, Richards A, Gow NA. Vacuoles and fungal biology. Curr Opin Microbiol 2008;11:503–10.10.1016/j.mib.2008.09.017Suche in Google Scholar PubMed
46. Sid A, Ezziyyani M, Egea-Gilabert C, Candela ME. Selecting bacterial strains for use in the biocontrol of diseases caused by Phytophthora capsici and Alternaria alternata in sweet pepper plants. Biol Plant 2003;47:569–74.10.1023/B:BIOP.0000041063.38176.4aSuche in Google Scholar
47. Vatsa P, Sanchez L, Clement C, Baillieul F, Dorey S. Rhamnolipid biosurfactants as new players in animal and plant defense against microbes. Int J Mol Sci 2010;11:5095–108.10.3390/ijms11125095Suche in Google Scholar PubMed
48. Sang MK, Chun S, Kim KD. Biological control of Phytophthora blight of pepper by antagonistic rhizobacteria selected from a sequential screening procedure. Biol Control 2008;46:424–33.10.1016/j.biocontrol.2008.03.017Suche in Google Scholar
49. Ji X, Lu G, Gai Y, Gao H, Lu B, Kong L, et al. Colonization of Morusalba L. by the plant-growth-promoting and antagonistic bacterium Burkholderia cepacia strain Lu10-1. BMC Microbiol 2010;10:243.10.1186/1471-2180-10-243Suche in Google Scholar
50. Islam S, Akanda MA, Prova A, Islam MT, Hossain MM. Isolation and identification of plant growth promoting rhizobacteria from cucumber rhizosphere and their effect on plant growth promotion and disease suppression. Front Microbiol 2016;6:1360.10.3389/fmicb.2015.01360Suche in Google Scholar PubMed PubMed Central
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Artikel in diesem Heft
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Artikel in diesem Heft
- Frontmatter
- Fast RBC loading by fluorescent antibodies and nuclei staining dye and their potential bioanalytical applications
- Chemical profiling of Di-Wu-Yang-Gan Granules by ultra performance liquid chromatography coupled to quadrupole time-of-flight mass spectrometry with MSE technology
- Design, synthesis, and antibacterial activity of novel 8-methoxyquinoline-2-carboxamide compounds containing 1,3,4-thiadiazole moiety
- Pseudomonas and Burkholderia inhibit growth and asexual development of Phytophthora capsici
- Antiproliferative activity of synthesized some new benzimidazole carboxamidines against MCF-7 breast carcinoma cells
- Overexpression of c-Myc enhances recombinant protein production in High Five cells after baculovirus infection
- Kostchyienones A and B, new antiplasmodial and cytotoxicity of limonoids from the roots of Pseudocedrela kotschyi (Schweinf.) Harms
- Antimicrobial and antioxidant activities of two polyketides from lichen-endophytic fungus Preussia sp.