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Screening of plant growth promoting traits ofBacillus thuringiensis

  • Ecological and Environmental Microbiology
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Abstract

This study aimed to evaluate the plant growth promoting (PGP) potential ofBacillus thuringiensis. In this context, several genetic determinants of factors implicated in PGP potential were investigated by polymerase chain reaction (PCR) in 16B. thuringiensis strains of different origin and belonging to different subspecies. PCR screening was performed on acid phosphatase, phytase, siderophore biosynthesis protein, 1-aminocyclopropane-1-carboxylate (ACC) deaminase and indolpyruvate decarboxylase (ipdC). Production of indol acetic acid (IAA)-like compounds and of ACC deaminase, and capability of solubilising mineral phosphate were investigated by phenotypic tests. All the strains were PCR positive for the presence of the siderophore biosynthesis protein, ACC deaminase and acid phosphatase genes. Five and seven strains gave an amplicon with the expected length for the phytase andipdC genes respectively. All the strains produced IAA compounds and seven had a high capacity to solubilise inorganic phosphorous. Qualitative phenotypic test for ACC deaminase activity showed that seven strains are able to grow on salt minimal medium containing ACC as sole nitrogen source, indicating the expression of theaccd genes. Our screening results in thirteen strains having more than one PGP trait and showed thatB. thuringiensis harbours and expresses several PGP determinants that could be very interesting in field application to enhance the plant growth. To our knowledge, this is the first report on the multiple plant growth promoting potential ofB. thuringiensis.

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References

  • Arora N., Ahmad T., Rajagopal R., Bhatnagar R.K. (2003). A constitutively expressed 36 kDa exochitinase fromBacillus thuringiensis HD-1. Biochem. Biophys. Res. Commun., 307: 620–625.

    Article  CAS  PubMed  Google Scholar 

  • Belimov A.A., Hontzeas N., Safronova V.I., Demchinskaya S.V., Piluzza G., Bullitta S., Glick B.R. (2005). Cadmium-tolerant plant growth-promoting bacteria associatedwith the roots of Indian mustard (Brassica juncea L. Czern.). Soil Biol. Biochem., 37: 241–250.

    Article  CAS  Google Scholar 

  • Bloemberg G.V., Lugtenberg B.J.J. (2001). Molecular basis of plant growth promotion and biocontrol by rhizobacteria. Curr. Opin. Plant. Biol., 4: 343–350.

    Article  CAS  PubMed  Google Scholar 

  • Brandl M.T., Lindow S.E. (1996). Cloning and characterization of a locus encoding an indolepyruvate decarboxylase involved in indole-3-acetic acid synthesis inErwinia herbicola. Appl. Environ. Microbiol., 62: 4121–4128

    CAS  PubMed  Google Scholar 

  • Cendrowski S., MacArthur W., Hanna P. (2004).Bacillus anthracis requires siderophore biosynthesis for growth in macrophages and mouse virulence. Mol. Microbiol., 51: 407–417.

    Article  CAS  PubMed  Google Scholar 

  • Chattopadhyay A., Bhatnagar N.B., Bhatnagar R. (2004). Bacterial insecticidal toxins. Crit. Rev. Microbiol., 30: 33–54.

    Article  CAS  PubMed  Google Scholar 

  • Cherif A., Chehimi S., Limem F., Rokbani A., Hansen B.M., Hendriksen N.B., Daffonchio D., Boudabous A. (2003). Purification and characterization of the novel bacteriocin entomocine 9, and safety evaluation of its producer,Bacillus thuringiensis subsp.entomocidus HD9. J. Appl. Microbiol., 95: 990–1000.

    Article  CAS  PubMed  Google Scholar 

  • Daffonchio D., Cherif A., Borin S. (2000). Homoduplex and heteroduplex polymorphisms of the amplified ribosomal 16S-23S internal transcribed spacers describe genetic relationships in the ‘Bacillus cereus group’. Appl. Environ. Microbiol. 66: 5460–5468.

    Article  CAS  PubMed  Google Scholar 

  • Dong Y.-H., Xu J.-L., Li X.-Z., Zhang L.-H. (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.

    Article  CAS  PubMed  Google Scholar 

  • Dworkin M., Foster J. (1958). Experiments with some microorganisms which utilize ethane and hydrogen. J. Bacteriol. 75: 592–601.

    CAS  PubMed  Google Scholar 

  • Fujino A., Ose T., Yao M., Tokiwano T., Honma M., Watanabe N., Tanaka I. (2004). Structural and enzymatic properties of 1-aminocyclopropane-1-carboxylate deaminase homologue fromPyrococcus horikoshii. J. Mol. Biol. 341: 999–1013.

    Article  CAS  PubMed  Google Scholar 

  • Glick B.R. (2005). Modulation of plant ethylene levels by the bacterial enzyme ACC deaminase. FEMS Microbiol. Lett. 251: 1–7.

    Article  CAS  PubMed  Google Scholar 

  • Glickmann E., Gardan L., Jacquet S., Hussain S., Elasri M., Petit A., Dessaux Y. (1998). Auxin production is a common feature of most pathovars ofPseudomonas syringae. Molecular Plant-Microbe Interact., 11: 156–162.

    Article  CAS  Google Scholar 

  • Gordon S.A., Weber R.P. (1951). Colorimetric estimation of indole acetic acid. Plant Physiol., 26: 192–195.

    Article  CAS  PubMed  Google Scholar 

  • Grichko V.P., Glick B.R. (2001). Amelioration of flooding stress by ACC deaminase-containing plant growth-promoting bacteria. Plant Physiol. Biochem. 39:11–17.

    Article  CAS  Google Scholar 

  • Hoffmaster A.R., Ravel J., Rasko D.A., Chapman G.D., Chute M.D., Marston C.K., De B.K., Sacchi C.T., Fitzgerald C., Mayer L.W., Maiden M.C.J., Priest F.G., Barker M., Jiang L., Cer R.Z., Rilstone J., Peterson S.N., Weyant R.S., Galloway D.R., Rea, T.D., Popovic T., Fraser C.M. (2004). Identification of anthrax toxin genes in aBacillus cereus associated with an illness resembling inhalation anthrax. Proc. Natl. Acad. Sci. U.S.A., 101: 8449–8454.

    Article  CAS  PubMed  Google Scholar 

  • Hontzeas N., Zoidakis J., Glick B.R., Abu-Omar M.M. (2004). Expression and characterization of 1-aminocyclopropane-1-carboxylate deaminase from the rhizobacteriumPseudomonas putida UW4: a key enzyme in bacterial plant growth promotion. Biochim. Biophys. Acta, 1703: 11–19.

    CAS  PubMed  Google Scholar 

  • Ivanova N., Sorokin A., Anderson I., Galleron N., Candelon B., Kapatral V., Bhattacharyya A., Reznik G., Mikhailova N., Lapidus A., Chu L., Mazur M., Goltsman E., Larsen N., D’Souza M., Walunas T., Grechkin Y., Pusch G., Haselkorn R., Fonstein M., Ehrlich S.D., Overbeek R., Kyrpides N. (2003). Genome sequence ofBacillus cereus and comparative analysis withBacillus anthracis. Nature, 423: 87–91.

    Article  CAS  PubMed  Google Scholar 

  • Masalha J., Kosegarten H., Elmaci Ö., Mengel K. (2000). The central role of microbial activity for iron acquisition in maize and sunflower. Biol. Fertil. Soils, 30: 433–439.

    Article  CAS  Google Scholar 

  • Mayak S., Tirosh T., Glick B.R. (2004a). Plant growth-promoting bacteria confer resistance in tomato plants to salt stress. Plant Physiol. Biochem., 42: 565–572.

    Article  CAS  PubMed  Google Scholar 

  • Mayak S., Tirosh T., Glick B.R. (2004b). Plant growth-promoting bacteria that confer resistance to water stress in tomatoes and peppers. Plant Sci., 166: 525–530.

    Article  CAS  Google Scholar 

  • Mehta S., Nautiyal C.S. (2001). An efficient method for qualitative screening of phosphate-solubilizing bacteria. Curr. Microbiol., 43: 51–56.

    Article  CAS  PubMed  Google Scholar 

  • Nautiyal C.S., Bhadauria S, Kumar P., Lal H., Mondal R., Verma D. (2000). Stress induced phosphate solubilization in bacteria isolated from alkaline soils. FEMS Microbiol. Lett., 182: 291–296.

    Article  CAS  PubMed  Google Scholar 

  • Park R-Y., Choi M.-H., Shin S.-H. (2005). Production of catechol-siderophore and utilization of transferrin-bound iron inBacillus cereus. Biol. Pharm. Bull., 28: 1132–1135.

    Article  CAS  PubMed  Google Scholar 

  • Patten C.L., Glick B.R. (2002). Role ofPseudomonas putida indoleacetic acid in development of the host plant root system. Appl. Environ. Microbiol., 68: 3795–3801.

    Article  CAS  PubMed  Google Scholar 

  • Penrose D.M., Glick B.R. (2003). Methods for isolating and characterizing ACC deaminase-containing plant growth-promoting rhizobacteria. Physiologia Plantarum, 118: 10–15.

    Article  CAS  PubMed  Google Scholar 

  • Penrose D.M., Moffatt B.A., Glick B.R. (2001). Determination of 1-aminocycopropane-1-carboxylic acid (ACC) to assess the effects of ACC deaminase-containing bacteria on roots of canola seedlings. Can. J. Microbiol., 47: 77–80.

    Article  CAS  PubMed  Google Scholar 

  • Raddadi N., Cherif A., Mora D., Brusetti L., Borin S., Boudabous A., Daffonchio D. (2005). The autolytic phenotype of theBacillus cereus group. J. Appl. Microbiol., 99: 1070–1081.

    Article  CAS  PubMed  Google Scholar 

  • Raddadi N., Cherif A., Ouzari H., Marzorati M., Brusetti L., Boudabous A., Daffonchio D. (2007).Bacillus thuringiensis beyond insect biocontrol: plant growth promotion and biosafety of polyvalent strains. Ann. Microbiol., 57: 481–494.

    Article  CAS  Google Scholar 

  • Rasko D.A., Ravel J., Økstad O.A., Helgason E., Cer R.Z., Jiang L., Shores K.A., Fouts D.E., Tourasse N.J., Angiuoli S.V., Kolonay J., Nelson W.C., Kolstø A.B., Fraser C.M., Read, T.D., (2004). The genome sequence ofBacillus cereus ATCC 10987 reveals metabolic adaptations and a large plasmid related toBacillus anthracis pXO1. Nucl. Ac. Res., 32: 977–988.

    Article  CAS  Google Scholar 

  • Read T.D., Peterson S.N., Tourasse N., Les Baillie W., Paulsen I.T., Nelson K.E., Tettelin H., Fouts D.E., Eisen J.A., Gill S.R., Holtzapple E.K., Økstad O.A., Helgason E., Rilstone J., Wu M., Kolonay J.F., Beanan M.J., Dodson R.J., Brinkac L.M., Gwinn M., DeBoy R.T., Madpu R., Daugherty S.C., Durkin A.S., Haft D.H., Nelson W.C., Peterson J.D., Pop M., Khouri H.M., Radune D., Benton J.L., Mahamoud Y., Jiang L., Hance I.R., Weidman J.F., Berry K.J., Plaut R.D., Wolf A.M., Watkins K.L., Nierman W.C., Hazen A., Cline R., Redmond C., Thwaite J.E., White O., White O., Salzberg S.L., Thomason B., Friedlander A.M., Koehler T.M., Hanna P.C., Kolstø A.-B., Fraser C.M. (2003). The genome sequence ofBacillus anthracis Ames and comparison to closely related bacteria. Nature, 423: 81–86.

    Article  CAS  PubMed  Google Scholar 

  • Rodriguez H., Fraga R. (1999). Phosphate solubilizing bacteria and their role in plant growth promotion. Biotechnol. Adv., 17: 319–339.

    Article  CAS  PubMed  Google Scholar 

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

    CAS  PubMed  Google Scholar 

  • Schutz A., Golbik R., Tittman K., Svergun D.I., Koch M.H.J., Hubner G., Konig S. (2003). Studies on structure-function relationships of indolepyruvate decarboxylase fromEnterobacter cloacea, a key enzymeof the indole acetic acid pathway. Eur. J. Biochem., 270: 2322–2331.

    Article  CAS  PubMed  Google Scholar 

  • Schwalm K., Aloni R., Langhans M., Heller W., Stich S., Ullrich C.I. (2003). Flavonoid-related regulation of auxin accumulation inAgrobacterium tumefaciens-induced plant tumors. Planta, 218: 163–178.

    Article  CAS  PubMed  Google Scholar 

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

    CAS  PubMed  Google Scholar 

  • Sharma A., Johri B.N., Sharma A.K., Glick B.R. (2003). Plant growth-promoting bacteriumPseudomonas sp. strain GRP3 influences iron acquisition in mung bean (Vigna radiata L. Wilzeck). Soil Biol. Biochem., 35: 887–894.

    Article  CAS  Google Scholar 

  • Wang C., Knill E., Glick B.R., Defago G. (2000). Effect of transferring 1-aminocyclopropoane-1-carboxylic acid (ACC) deaminase genes intoPseudomonas fluorescens strain CH40 and its gacA derivative CHA96 on their growth-promoting and disease-suppressive capacities. Can. J. Microbiol., 46: 898–907.

    Article  CAS  PubMed  Google Scholar 

  • Wilson M.K., Abergel R.J., Raymond K.N., Arceneaux J.E.L., Byers B.R. (2006). Siderophores ofBacillus anthracis, Bacillus cereus andBacillus thuringiensis. Biochem. Biophys. Res. Comm., 348: 320–325.

    Article  CAS  PubMed  Google Scholar 

  • Yehuda Z., Shenker M., Romheld V., Marschner H., Hador Y., Chen Y. (1996). The role of ligand exchange in the uptake of iron from microbial siderophores by gramineous plant. Plant Physiol., 112: 1273–1280.

    CAS  PubMed  Google Scholar 

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Authors and Affiliations

  1. Dipartimento di Scienze e Tecnologie Alimentari e Microbiologiche (DISTAM), Università degli Studi, via Celoria 2, 20133, Milano, Italy

    Noura Raddadi & Daniele Daffonchio

  2. Laboratoire Microorganismes et Biomolécule Actives (LMBA), Faculté des Sciences de Tunis, 2092, Tunis, Tunisia

    Ameur Cherif & Abdellatif Boudabous

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  1. Noura Raddadi
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  2. Ameur Cherif
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  3. Abdellatif Boudabous
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  4. Daniele Daffonchio
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Correspondence to Daniele Daffonchio.

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Raddadi, N., Cherif, A., Boudabous, A. et al. Screening of plant growth promoting traits ofBacillus thuringiensis . Ann. Microbiol. 58, 47–52 (2008). https://doi.org/10.1007/BF03179444

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  • DOI: https://doi.org/10.1007/BF03179444

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