Skip to main content
Log in

Novel roles of Bacillus thuringiensis to control plant diseases

  • Mini-Review
  • Published:
Applied Microbiology and Biotechnology Aims and scope Submit manuscript

Abstract

Bacillus thuringiensis is well known as an effective bio-insecticidal bacterium. However, the roles of B. thuringiensis to control plant diseases are not paid great attention to. In recent years, many new functions in protecting plants from pathogen infection have been discovered. For example, acyl homoserine lactone lactonase produced by B. thuringiensis can open the lactone ring of N-acyl homoserine lactone, a signal molecule in the bacterial quorum-sensing system. This in turn, significantly silences bacterial virulence. This finding resulted in the development of a new strategy against plant bacterial diseases by quenching bacterial quorum sensing. Another new discovery about B. thuringiensis function is zwittermicin A, a linear aminopolyol antibiotic with high activity against the Oomycetes and their relatives, as well as some gram-negative bacteria. This paper summarized the relative progresses of B. thuringiensis in plant disease control and its favorable application prospects.

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

  • Barnard AM, Salmond GP (2007) Quorum sensing in Erwinia species. Anal Bioanal Chem 387:415–423

    CAS  PubMed  Google Scholar 

  • Broderick NA, Goodman RM, Raffa KF, Handelsman J (2000) Synergy between zwittermicin A and Bacillus thuringiensis subsp. Kurstaki against gypsy moth (Lepidoptera: Lymantriidae). Environ Entomol 29:101–107

    CAS  Google Scholar 

  • Broderick NA, Goodman RM, Handelsman J, Raffa KF (2003) Effect of host diet and insect source on synergy of gypsy moth (Lepidoptera: Lymantriidae) mortality to Bacillus thuringiensis subsp. kurstaki by zwittermicin A. Environ Entomol 32:387–391

    Google Scholar 

  • Chan YA, Boyne MT, Podevels AM, Klimowicz AK, Handelsman J, Kelleher NL, Thomas MG (2006) Hydroxymalonyl-acyl carrier protein (ACP) and aminomalonyl-ACP are two additional type I polyketide synthase extender units. Proc Natl Acad Sci USA 103:14349–14354

    CAS  PubMed  PubMed Central  Google Scholar 

  • Cho HS, Park SY, Ryu CM, Kim JF, Kim JG, Park SH (2007) Interference of quorum sensing and virulence of the rice pathogen Burkholderia glumae by an engineered endophytic bacterium. FEMS Microbiol Ecol 60:14–23

    CAS  PubMed  Google Scholar 

  • Crickmore N (2006) Beyond the spore—past and future developments of Bacillus thuringiensis as a biopesticide. J Appl Microbiol 101:616–619

    CAS  PubMed  Google Scholar 

  • Cundliffe E (1989) How antibiotic-producing organisms avoid suicide. Annu Rev Microbiol 43:207–233

    CAS  PubMed  Google Scholar 

  • Dong YH, Xu JL, Li XZ, Zhang LH (2000) AiiA, an enzyme that inactivates the acylhomoserine lactone quorum-sensing signal and attenuates the virulence of Erwinia carotovora. Proc Natl Acad Sci USA 97:3526–3531

    CAS  PubMed  PubMed Central  Google Scholar 

  • Dong YH, Wang LH, Xu JL, Zhang HB, Zhang XF, Zhang LH (2001) Quenching quorum-sensing-dependent bacterial infection by an N-acyl homoserine lactonase. Nature 411:813–817

    CAS  PubMed  Google Scholar 

  • Dong YH, Gusti AR, Zhang Q, Xu JL, Zhang LH (2002) Identification of quorum-quenching N-acyl homoserine lactonases from Bacillus species. Appl Environ Microbiol 68:1754–1759

    CAS  PubMed  PubMed Central  Google Scholar 

  • Dong YH, Zhang XF, Xu JL, Zhang LH (2004) Insecticidal Bacillus thuringiensis silences Erwinia carotovora virulence by a new form of microbial antagonism, signal interference. Appl Environ Microbiol 70:954–960

    CAS  PubMed  PubMed Central  Google Scholar 

  • Eberl L (2006) Quorum sensing in the genus Burkholderia. Int J Med Microbiol 296:103–112

    CAS  PubMed  Google Scholar 

  • Emmert EA, Klimowicz AK, Thomas MG, Handelsman J (2004) Genetics of zwittermicin a production by Bacillus cereus. Appl Environ Microbiol 70:104–113

    CAS  PubMed  PubMed Central  Google Scholar 

  • Girard G, Bloemberg GV (2008) Central role of quorum sensing in regulating the production of pathogenicity factors in Pseudomonas aeruginosa. Future Microbiol 3:97–106

    CAS  PubMed  Google Scholar 

  • Handelsman J, Raffel S, Mester EH, Wunderlich L, Grau CR (1990) Biological control of damping-off of alfalfa seedlings with Bacillus cereus UW85. Appl Environ Microbiol 56:713–718

    CAS  PubMed  PubMed Central  Google Scholar 

  • He H, Silo-Suh LA, Handelsman J, Clardy J (1994) Zwittermicin A, an antifungal and plant protection agent from Bacillus cereus. Tetrahedron Lett 35:2499–2502

    CAS  Google Scholar 

  • Jensen GB, Hansen BM, Eilenberg J, Mahillon J (2003) The hidden lifestyles of Bacillus cereus and relatives. Environ Microbiol 5:631–640

    CAS  PubMed  Google Scholar 

  • Khyami-Horani H, Hajaij M, Charles JF (2003) Characterization of Bacillus thuringiensis ser. jordanica (serotype H71), a novel serovariety isolated in Jordan. Curr Microbiol 47:26–31

    CAS  PubMed  Google Scholar 

  • Kim MH, Choi WC, Kang HO, Lee JS, Kang BS, Kim KJ, Derewenda ZS, Oh TK, Lee CH, Lee JK (2005a) The molecular structure and catalytic mechanism of a quorum-quenching N-acyl-l-homoserine lactone hydrolase. Proc Natl Acad Sci USA 102:17606–17611

    CAS  PubMed  PubMed Central  Google Scholar 

  • Kim MH, Kang HO, Kang BS, Kim KJ, Choi WC, Oh TK, Lee CH, Lee JK (2005b) Crystallization and preliminary crystallographic analysis of Bacillus thuringiensis AHL-lactonase. Biochim Biophys Acta 1750:5–8

    CAS  PubMed  Google Scholar 

  • Lee SJ, Park SY, Lee JJ, Yum DY, Koo BT, Lee JK (2002) Genes encoding the N-acyl homoserine lactone-degrading enzyme are widespread in many subspecies of Bacillus thuringiensis. Appl Environ Microbiol 68:3919–3924

    CAS  PubMed  PubMed Central  Google Scholar 

  • Liu D, Lepore BW, Petsko GA, Thomas PW, Stone EM, Fast W, Ringe D (2005) Three-dimensional structure of the quorum-quenching N-acyl homoserine lactone hydrolase from Bacillus thuringiensis. Proc Natl Acad Sci USA 102:11882–11887

    CAS  PubMed  PubMed Central  Google Scholar 

  • Lu X, Yuan Y, Xue XL, Zhang GP, Zhou SN (2006) Identification of the critical role of Tyr-194 in the catalytic activity of a novel N-acyl-homoserine lactonase from marine Bacillus cereus strain Y2. Curr Microbiol 53:346–350

    CAS  PubMed  Google Scholar 

  • Milner JL, Stohl EA, Handelsman J (1996) Zwittermicin A resistance gene from Bacillus cereus. J Bacteriol 178:4266–4272

    CAS  PubMed  PubMed Central  Google Scholar 

  • Molnar I, Aparicio JF, Haydock SF, Khaw LE, Schwecke T, Konig A, Staunton J, Leadlay PF (1996) Organisation of the biosynthetic gene cluster for rapamycin in Streptomyces hygroscopicus: analysis of genes flanking the polyketide synthase. Gene 169:1–7

    CAS  PubMed  Google Scholar 

  • Momb J, Thomas PW, Breece RM, Tierney DL, Fast W (2006) The quorum-quenching metallo-gamma-lactonase from Bacillus thuringiensis exhibits a leaving group thio effect. Biochemistry 45:13385–13393

    CAS  PubMed  Google Scholar 

  • Nair JR, Narasimman G, Sekar V (2004) Cloning and partial characterization of zwittermicin A resistance gene cluster from Bacillus thuringiensis subsp. kurstaki strain HD1. J Appl Microbiol 97:495–503

    CAS  PubMed  Google Scholar 

  • Raffel SJ, Stabb EV, Milner JL, Handelsman J (1996) Genotypic and phenotypic analysis of zwittermicin A-producing strains of Bacillus cereus. Microbiology 142:3425–3436

    CAS  PubMed  Google Scholar 

  • Recktenwald J, Shawky R, Puk O, Pfennig F, Keller U, Wohlleben W, Pelzer S (2002) Nonribosomal biosynthesis of vancomycin-type antibiotics: a heptapeptide backbone and eight peptide synthetase modules. Microbiology 148:1105–1118

    CAS  PubMed  Google Scholar 

  • Roh JY, Choi JY, Li MS, Jin BR, Je YH (2007) Bacillus thuringiensis as a specific, safe, and effective tool for insect pest control. J Microbiol Biotechnol 17:547–559

    CAS  PubMed  Google Scholar 

  • Schnepf E, Crickmore N, Van Rie J, Lereclus D, Baum J, Feitelson J, Zeigler DR, Dean DH (1998) Bacillus thuringiensis and its pesticidal crystal proteins. Microbiol Mol Biol Rev 62(3):775–806

    CAS  PubMed  PubMed Central  Google Scholar 

  • Shang H, Chen J, Handelsman J, Goodman RM (1999) Behavior of Pythium torulosum zoospores during their interaction with tobacco roots and Bacillus cereus. Curr Microbiol 38:199–204

    CAS  PubMed  Google Scholar 

  • Shao T, Bai L, Zhang J, Wang G, Liu D, Li Z, Liu J, Song F, Huang D (2008) A nonribosomal peptide synthetase gene tzw1 is involved in zwittermicin A biosynthesis in Bacillus thuringiensis G03. Curr Microbiol 57(1):61–65

    CAS  PubMed  Google Scholar 

  • Silo-Suh LA, Lethbridge BJ, Raffel SJ, He H, Clardy J, Handelsman J (1994) Biological activities of two fungistatic antibiotics produced by Bacillus cereus UW85. Appl Environ Microbiol 60:2023–2030

    CAS  PubMed  PubMed Central  Google Scholar 

  • Silo-Suh LA, Stabb EV, Raffel SJ, Handelsman J (1998) Target range of zwittermicin A, an aminopolyol antibiotic from Bacillus cereus. Curr Microbiol 37:6–11

    CAS  PubMed  Google Scholar 

  • Stabb EV, Handelsman J (1998) Genetic analysis of zwittermicin A resistance in Escherichia coli: effects on membrane potential and RNA polymerase. Mol Microbiol 27:311–322

    CAS  PubMed  Google Scholar 

  • Stabb EV, Jacobson LM, Handelsman J (1994) Zwittermicin A-producing strains of Bacillus cereus from diverse soils. Appl Environ Microbiol 60:4404–4412

    CAS  PubMed  PubMed Central  Google Scholar 

  • Stohl EA, Brady SF, Clardy J, Handelsman J (1999) ZmaR, a novel and widespread antibiotic resistance determinant that acetylates zwittermicin A. J Bacteriol 181:5455–5460

    CAS  PubMed  PubMed Central  Google Scholar 

  • Thomas PW, Stone EM, Costello AL, Tierney DL, Fast W (2005) The quorum-quenching lactonase from Bacillus thuringiensis is a metalloprotein. Biochem 44:7559–7569

    CAS  Google Scholar 

  • Von Bodman SB, Bauer WD, Coplin DL (2003) Quorum sensing in plant-pathogenic bacteria. Annu Rev Phytopathol 41:455–483

    Google Scholar 

  • Wang LH, Weng LX, Dong YH, Zhang LH (2004) Specificity and enzyme kinetics of the quorum-quenching N-acyl homoserine lactone lactonase (AHL-lactonase). J Biol Chem 279:13645–13651

    CAS  PubMed  Google Scholar 

  • White CE, Winans SC (2007) Cell–cell communication in the plant pathogen Agrobacterium tumefaciens. Philos Trans R Soc Lond B Biol Sci 7362:1135–1148

    Google Scholar 

  • Zhang HB, Wang LH, Zhang LH (2002) Genetic control of quorum-sensing signal turnover in Agrobacterium tumefaciens. Proc Natl Acad Sci USA 99:4638–4643

    CAS  PubMed  PubMed Central  Google Scholar 

  • Zhang HB, Wang C, Zhang LH (2004) The quormone degradation system of Agrobacterium tumefaciens is regulated by starvation signal and stress alarmone (p)ppGpp. Mol Microbiol 52:1389–1401

    CAS  PubMed  Google Scholar 

  • Zhang Y, Fernando WG, de Kievit TR, Berry C, Daayf F, Paulitz TC (2006) Detection of antibiotic-related genes from bacterial biocontrol agents with polymerase chain reaction. Can J Microbiol 52(5):476–481

    CAS  PubMed  Google Scholar 

  • Zhang L, Ruan L, Hu C, Wu H, Chen S, Yu Z, Sun M (2007) Fusion of the genes for AHL-lactonase and S-layer protein in Bacillus thuringiensis increases its ability to inhibit soft rot caused by Erwinia carotovora. Appl Microbiol Biotechnol 74:667–675

    CAS  PubMed  Google Scholar 

  • Zhao C, Luo Y, Song C, Liu Z, Chen S, Yu Z, Sun M (2007) Identification of three Zwittermicin A biosynthesis-related genes from Bacillus thuringiensis subsp. kurstaki strain YBT-1520. Arch Microbiol 187:313–319

    CAS  PubMed  Google Scholar 

  • Zhao C, Zeng H, Yu Z, Sun M (2008) N-acyl homoserine lactonase promotes prevention of Erwinia virulence with zwittermicin A-producing strain Bacillus cereus. Biotechnol Bioeng 100(3):599–603

    CAS  PubMed  Google Scholar 

  • Zhou Y, Ye WX, Zhou Y, Zhu CG, Sun M, Yu Z (2006) Ethanol tolerance, yield of melanin, swarming motility and growth are correlated with the expression levels of aiiA gene in Bacillus thuringiensis. Enzyme Microb Technol 38:967–974

    CAS  Google Scholar 

  • Zhu C, Yu Z, Sun M (2006) Restraining Erwinia virulence by expression of N-acyl homoserine lactonase gene pro3A-aiiA in Bacillus thuringiensis subsp leesis. Biotechnol Bioeng 95:526–532

    CAS  PubMed  Google Scholar 

Download references

Acknowledgments

This paper was partially supported by the Dong-A University Research Fund.

Author information

Authors and Affiliations

Authors

Corresponding authors

Correspondence to Yong-Lark Choi or Ziniu Yu.

Rights and permissions

Reprints and permissions

About this article

Cite this article

Zhou, Y., Choi, YL., Sun, M. et al. Novel roles of Bacillus thuringiensis to control plant diseases. Appl Microbiol Biotechnol 80, 563–572 (2008). https://doi.org/10.1007/s00253-008-1610-3

Download citation

  • Received:

  • Revised:

  • Accepted:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1007/s00253-008-1610-3

Keywords

Navigation