Skip to main content
Log in

Mode of antagonism of a biocontrol bacterium Lysobacter sp. SB-K88 toward a damping-off pathogen Aphanomyces cochlioides

  • Original Paper
  • Published:
World Journal of Microbiology and Biotechnology Aims and scope Submit manuscript

Abstract

The biocontrol bacterium Lysobacter sp. SB-K88 suppresses damping-off disease in sugar beet and spinach caused by Aphanomyces cochlioides and Pythium sp. through characteristic plant colonization and antibiosis against the pathogens. This study aimed to unravel further details on mode of antagonism of SB-K88 against a damping-off pathogen A. cochlioides AC-5. The SB-K88 substantially inhibited growth and decomposed AC-5 mycelia and suppressed the release of zoospores from the hyphae. The excised root tips of sugar beet seedlings from seeds previously inoculated with SB-K88 were less attractive to AC-5 zoospores. Although aerial growth was not affected, however, root hairs of SB-K88 inoculated sugar beet seedlings were remarkably shorter and thicker than those of uninoculated control. When exposed to zoospores, the SB-K88 inhibited motility of zoospores and/or caused lysis, and then aggregated around the dead cystospores or lysed residues within 3–6 h likely to be micro-predatory behavior to a eukaryotic organism. Confocal laser scanning microscopic analysis revealed that number of lipid bodies and activities of mitochondria were markedly increased in the affected hyphae compared with control hyphae as visualized by established vital stains. Taken together, these results suggest that Lysobacter sp. SB-K88 suppresses damping-off diseases through exerting multifaceted antagonistic effects against the peronosporomycetes.

This is a preview of subscription content, log in via an institution to check access.

Access this article

Price excludes VAT (USA)
Tax calculation will be finalised during checkout.

Instant access to the full article PDF.

Fig. 1
Fig. 2
Fig. 3
Fig. 4
Fig. 5

Similar content being viewed by others

References

  • Ahmed K, Chohnan S, Ohashi H, Hirata T, Masaki T, Sakiyama F (2003) Purification, bacteriolytic activity, and specificity of β-lytic protease from Lysobacter sp. IB-9374. J Biosci Bioeng 95:27–34

    Google Scholar 

  • Bais HP, Fall R, Vivanco JM (2004) Biocontrol of Bacillus subtilis against infection of Arabidopsis root by Pseudomonas syringae is facilitated by biofilm formation and surfactin production. Plant Physiol 134:307–319

    Article  CAS  Google Scholar 

  • Burnham JC, Collart SA, Highison BW (1981) Entrapment and lysis of the cyanobacterium Phormidium luridum by aqueous colonies of Myxococcus xanthus PCO2. Arch Microbiol 129:285–294

    Article  Google Scholar 

  • Christensen P, Cook FD (1978) Lysobacter, a new genus of nonfruiting, gliding bacteria with high base ratio. Int J Syst Bacteriol 28:367–393

    Article  Google Scholar 

  • Deora A, Hashidoko Y, Islam MT, Aoyama Y, Ito T, Tahara S (2006) An antagonistic rhizoplane bacterium Pseudomonas sp. strain EC-S101 physiologically stresses a spinach root rot pathogen Aphanomyces cochlioides. J Gen Plant Pathol 72:57–74

    Article  CAS  Google Scholar 

  • Fallon RD, Brock TD (1979) Lytic organisms and photooxidative effects: influence on blue-green algae (cyanobacteria in Lake Mendota, Wisconsin). Appl Environ Microbiol 38:499–505

    CAS  Google Scholar 

  • Folman LB, Postma J, van Veen JA (2003) Characterization of Lysobacter enzymogenes (Christensen and Cook, 1978) strain 3.1T8, a powerful antagonist of fungal disease of cucumber. Microbiol Res 158:107–115

    Article  CAS  Google Scholar 

  • Hashidoko Y, Nakayama T, Homma Y, Tahara S (1999) Structure elucidation of xanthobaccin A, a new antibiotic produced from Stenotrophomonas sp. strain SB-K88. Tetrahedron Lett 40:2957–2960

    Article  CAS  Google Scholar 

  • Heungens K, Parke JL (2000) Zoospore homing and infection events: effects of the biocontrol bacterium Burkholderia cepacia AMMDR1 on two oomycete pathogens of pea (Pisum sativum L.). Appl Environ Microbiol 66:5192–5200

    Article  CAS  Google Scholar 

  • Hogan DA, Kolter R (2002) Pseudomonas-Candida interactions: an ecological role for virulence factors. Science 296:2229–2232

    Article  CAS  Google Scholar 

  • Homma Y, Uchino H, Kanzawa K, Nakayama T, Sayama M (1993) Suppression of sugar beet damping-off and production of antagonistic substances by strains of rhizobacteria. Ann Phytopathol Soc Jpn 59:282

    Google Scholar 

  • Islam MT (2008) Disruption of ultrastructure and cytoskeleton network is involved with biocontrol of damping-off pathogen Aphanomyces cochlioides by Lysobacter sp. SB-K88. Biol Control 46:312–321

    Article  Google Scholar 

  • Islam MT, Tahara S (2001) Chemotaxis of fungal zoospores, with special reference to Aphanomyces cochlioides. Biosci Biotechnol Biochem 65:1933–1948

    Article  CAS  Google Scholar 

  • Islam MT, Ito T, Tahara S (2001) Morphological studies on zoospores of Aphanomyces cochlioides and changes during the interaction with host materials. J Gen Plant Pathol 67:255–261

    Article  Google Scholar 

  • Islam MT, Ito T, Tahara S (2002) Microscopic studies on attachment and differentiation of zoospores of the phytopathogenic fungus Aphanomyces cochlioides. J Gen Plant Pathol 68:111–117

    Article  CAS  Google Scholar 

  • Islam MT, Ito T, Tahara S (2003) Host-specific plant signal and G-protein activator, mastoparan, trigger differentiation of zoospores of the phytopathogenic oomycete Aphanomyces cochlioides. Plant Soil 255:131–142

    Article  CAS  Google Scholar 

  • Islam MT, Hashidoko Y, Deora A, Ito T, Tahara S (2004a) Interactions between rhizoplane bacteria and a phytopathogenic Peronosporomycete Aphanomyces cochlioides in relation to the suppression of damping-off disease in sugar beet and spinach. IOBC/WPRS Bull 27:255–260

    Google Scholar 

  • Islam MT, Ito T, Tahara S (2004b) Interruption of the homing events of phytopathogenic Aphanomyces cochlioides zoospores by secondary metabolites from nonhost Amaranthus gangeticus. J Pestic Sci 29:6–14

    Article  CAS  Google Scholar 

  • Islam MT, Hashidoko Y, Deora A, Ito T, Tahara S (2005a) Lysobacter-Aphanomyces interactions: an ecological role for biocontrol of damping-off disease. Nippon Nogei Kagakkai Taikai Koen Yoshishu 2005:221

    Google Scholar 

  • Islam MT, Hashidoko Y, Deora A, Ito T, Tahara S (2005b) 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 soilborne peronosporomycetes. Appl Environ Microbiol 71:3786–3796

    Article  CAS  Google Scholar 

  • Islam MT, Sakasai M, Hashidoko Y, Deora A, Sakihama Y, Tahara S (2007) Composition of culture medium influences zoosporogenesis and differentiation of Aphanomyces cochlioides. J Gen Plant Pathol 73:324–329

    Article  CAS  Google Scholar 

  • Ji GH, Wei LF, He YQ, Wu YP, Bai XH (2008) Biological control of rice bacterial blight by Lysobacter antibioticus strain 13–1. Biol Control 45:288–296

    Article  Google Scholar 

  • Kilic-Ekici O, Yuen GY (2003) Induced resistance as a mechanism of biological control by Lysobacter enzymogenes strain C3. Phytopathology 93:1103–1110

    Article  Google Scholar 

  • Kobayashi DY, Reedy RM, Palumbo JD, Zhou JM, Yuen GY (2005) A clp gene homologue belonging to the Crp gene family globally regulates lytic enzyme production, antimicrobial activity, and biological control activity expressed by Lysobacter enzymogenes strain C3. Appl Environ Microbiol 71:261–269

    Article  CAS  Google Scholar 

  • Lin D, McBride MJ (1996) Development of techniques for the genetic manipulation of the gliding bacteria Lysobacter enzymogenes and Lysobacter brunescens. Can J Microbiol 42:896–902

    Article  CAS  Google Scholar 

  • Martin MO (2002) Predatory prokaryotes: an emerging research opportunity. J Mol Microbiol Biotechnol 4:467–477

    CAS  Google Scholar 

  • Nakayama T, Homma Y, Hashidoko Y, Mizutani J, Tahara S (1999) Possible role of xanthobaccins produced by Stenotrophomonas sp. strain SB-K88 in suppression of sugar beet damping-off disease. Appl Environ Microbiol 65:4334–4339

    CAS  Google Scholar 

  • Park JH, Kim R, Aslam Z, Joen CO, Chung YR (2008) Lysobacter capsici sp. nov., with antimicrobial activity, isolated from the rhizosphere of pepper, and emended description of the genus Lysobacter. Int J Syst Evol Microbiol 58:387–392

    Article  CAS  Google Scholar 

  • Postma J, Schilder MT, Bloem J, van Leeuwen-Haagsma WK (2008) Soil suppressiveness and functional diversity of the soil microflora in organic farming systems. Soil Biol Biochem 40:2394–2406

    Article  CAS  Google Scholar 

  • Postma J, Stevens LH, Wiegers GL, Davelaar E, Nijhuis EH (2009) Biological control of Pythium aphanidermarum in cucumber with a combined application of Lysobacter enzymogenes strain 3.1T8 and chitosan. Biol Control 48:301–309

    Article  Google Scholar 

  • Thomashow LS, Weller DM (1988) Role of phenazine antibiotic from Pseudomonas fluorescens in biological control of Gaeumannomyces graminis var. tritici. J Bacteriol 170:3499–3508

    CAS  Google Scholar 

  • Walker R, Rossal S, Asher MJC (2002) Colonization of the developing rhizosphere of sugar beet seedlings by potential biocontrol agents applied as seed treatments. J Appl Microbiol 92:228–237

    Article  Google Scholar 

  • West PV, Appiah AA, Gow NAR (2003) Advances in research on oomycete root pathogens. Physiol Mol Plant Pathol 62:99–113

    Article  Google Scholar 

  • Whipps JM (2001) Microbial interactions and biocontrol in the rhizosphere. J Exp Bot 52:487–511

    CAS  Google Scholar 

  • Yu F, Zaleta-Rivera K, Zhu X, Huffman J, Millet JC, Harris SD, Yuen G, Li XC, Du L (2007) Structure and biosynthesis of heat-stable antifungal factor (HSAF), a broad-spectrum antimycotic with a novel mode of action. Antimicrob Agents Chemother 51:64–72

    Article  CAS  Google Scholar 

  • Yuen GY, Zhang Z (2001) Control of brown patch disease using the bacterium Stenotrophomonas maltophilia strain C3 and culture fluid. Int Turfgrass Soc Res J 9:742–747

    Google Scholar 

  • Zhang Z, Yuen GY (1999) Biological control of Bipolaris sorokiniana on tall fescue by Stenotrophomonas maltophilia C3. Phytopathology 89:817–822

    Article  CAS  Google Scholar 

  • Zhang Z, Yuen GY (2000) The role of chitinase production by Stenotrophomonas maltophilia C3 in biological control of Bipolaris sorokiniana. Phytopathology 90:384–389

    Article  CAS  Google Scholar 

  • Zhang Z, Yuen GY, Sarath G, Penheiter A (2001) Chitinases from the plant disease biocontrol agent, Stenotrophomonas maltophilia C3. Phytopathology 91:204–211

    Article  CAS  Google Scholar 

Download references

Acknowledgments

I’m very thankful to Prof. Dr. Satoshi Tahara and Prof. Yasuyuki Hashidoko for their kind supports and encouragements during this work at Laboratory of Ecological Chemistry of Hokkaido University, Japan. My sincere thanks are also due to Prof. R. Yokosawa (Health Science University of Hokkaido, Japan) and Dr. Y. Homma and Dr. T. Nakayama (National Agricultural Research Center for Hokkaido Region, Sapporo, Japan) for their kind gifts of A. cochlioides AC-5 and Lysobacter sp. SB-K88, respectively. Dr. A. Deora, T. Ito, and Y. Aoyama, Graduate School of Agriculture of Hokkaido University, Japan deserve thanks for their assistance during SEM and CLSM studies. deserve special The financial support and a Postdoctoral Fellowship from the Japan Society for the Promotion of Science (JSPS) are also very much appreciated.

Author information

Authors and Affiliations

Authors

Corresponding author

Correspondence to Md. Tofazzal Islam.

Rights and permissions

Reprints and permissions

About this article

Cite this article

Tofazzal Islam, M. Mode of antagonism of a biocontrol bacterium Lysobacter sp. SB-K88 toward a damping-off pathogen Aphanomyces cochlioides . World J Microbiol Biotechnol 26, 629–637 (2010). https://doi.org/10.1007/s11274-009-0216-y

Download citation

  • Received:

  • Accepted:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1007/s11274-009-0216-y

Keywords

Navigation