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Evaluation of Bacillus thuringiensis bioinsecticidal protein effects on soil microorganisms

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Abstract

The effect of B. thuringiensis and its crystal protein on plant growth and on functional groups of microorganisms is not well understood. Soybean (Glycine max) var. Br 322 was grown in non-sterile soil infested with three B. thuringiensis (Bt) inocula: insecticidal crystal protein producer (Cry+), a mutant non-producer (Cry−), or insecticidal crystal protein (ICP), at a rate of 107 cells g−1 dry soil or 1.25 mg of protein g−1 dry soil. Non-inoculated plants were maintained as control. Measurements were carried out on soil samples before sowing (time zero) and after sowing and inoculation (5, 15, 25, 35 and 45 d) on samples of rhizosphere soil. The effect of spore and crystal protein produced by B. thuringiensis on the populations of functional groups of microorganisms (bacteria including actinomycetes and fungi) involved in the biogeochemical cycling of carbon (cellulolytic, amylolytic and proteolytic), phosphorus (arbuscular mycorrhizal fungi), and nitrogen (number of nodules and proteolytic) were evaluated. Population sizes of culturable heterotrophic bacteria and saprophytic fungi were also evaluated. No difference was found in heterotrophic bacterial populations inoculated with B. thuringiensis. Difference was observed in functional groups of C-cycling microorganisms. Nodule formation and plant growth were increased by Cry+ strain and ICP when compared with uninoculated plants. Crystal protein did not show any effect on arbuscular mycorrhiza (AM) colonization. However, a deleterious effect was observed with Cry+ and Cry− strains that inhibited colonization of AM fungi when compared with uninoculated plants.

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References

  • Addison J A 1993. Persistence and nontarget effects of Bacillus thuringiensis in soil: a review. Can J. For. Res. 23, 2329–2342.

    Google Scholar 

  • Andrade G 1999 Interacciones microbianas en la rizosfera. In Soil Fertility, Soil Biology and Plant Nutrition Interrelationships. Eds. J O Siqueira, F M S Moreira, A S Lopes, L R Guilherme, V Faquin, A E Furtinni and J G Carvalho. pp. 551–575. Brazilian Soil Science Society/ Federal University of Lavras/ Soil Science Department (SBCS/UFLA/DCS), Lavras, Brasil.

    Google Scholar 

  • Andrade G, Azcón R and Bethlenfalvay G J 1995 Mycorrhizae in sustainable agriculture 1. An agrosystem affecting rhizobacterium modifies plant soil responses to a mycorrhizal fungus. Appl. Soil Ecol. 2, 195–202.

    Google Scholar 

  • Andrade G, Mihara K L, Linderman R G and Bethlenfalvay G J 1997 Bacteria from rhizosphere and hyphosphere soils of different arbuscular mycorrhizal fungi. Plant Soil 192, 71–79.

    Google Scholar 

  • Bethlenfalvay G J, Andrade G and Azcón-Aguilar C 1997 Mycorrhizae in sustainable agriculture. 2. Plant and soil microorganisms in nodulated and nitrate fertilized peas. Biol. Fert. Soils 24, 164–168.

    Google Scholar 

  • Bradford M M 1976 A rapid and sensitive method for the quantification of microgram quantities of protein utilizing the principle of protein dye binding. Anal. Biochem. 72, 248–254.

    Google Scholar 

  • Cody R M 1989 Distribution of chitinase and chitibiose in Bacillus. Curr. Microbiol. 19, 201–205.

    Google Scholar 

  • Crickmore N, Zeigler D R, Feitelson J, Schnepf E, van Rie J, Lereclus D, Baum J and Dean D H 1998 Revision of the nomenclature for the Bacillus thuringiensis pesticidal crystal proteins. Microbiol. Mol. Biol. Rev. 62, 807–813.

    Google Scholar 

  • Fast P G 1972. The delta-endotoxin of Bacillus thuringiensis III:a rapid method for separating parasporal bodies from spores. J. Invert. Pathol. 20: 139–140.

    Google Scholar 

  • Feitelson J S, Payne J and Kim L 1992 Bacillus thuringiensis insects and beyond. Biotechnology 10: 271–275.

    Google Scholar 

  • Flexner J L, Lighthart B and Croft B A 1986 The effects of microbial pesticides on non-target beneficial arthropods. Agric. Ecosyst. Environ. 16, 203–254.

    Google Scholar 

  • Giovanetti M and Mosse B 1980 An evaluation of techniques for measuring vesicular-arbuscular micorrhizal infections in roots. New Phytol. 84, 489–500.

    Google Scholar 

  • Halverson L J, Clayton M K and J O Handelsman 1993 Population biology of Bacillus cereus UW85 in the rhizosphere of field-grown soybeans. Soil Biol. Biochem. 25, 485–493.

    Google Scholar 

  • Kalmykova G V, Burtseva L I and Yudina T G 1995 Characteristics of mutants of Bacillus thuringiensis subsp. kurstaki. Microbiology 64, 388–394.

    Google Scholar 

  • Kim D S, Cook R J and Weller D M 1997 Bacillus sp. L324-92 for biological control of three root diseases of wheat grown with reduced tillage. Phytopathology 87, 551–558.

    Google Scholar 

  • Lecadet M M, Blondel M O and Ribier J 1980 Generalized transduction in Bacillus thuringiensis var berliner 1715, using bacteriophage CP54 Ber. J. Gen. Microbiol. 121, 203–212.

    Google Scholar 

  • Linderman R G 1992 Vesicular-arbuscular mycorrhizae and soil microbial interantions. In Mycorrhizae in Sustainable Agriculture. Eds. G J Bethlenfalvay and R G Linderman. pp. 45–70. ASA Special Publication, Madison, WI.

  • Olsson S and Person P 1999 The composition of bacterial population in soil fractions differing in their degree of adherence to barley roots. Appl. Soil Ecol. 12, 205–215.

    Google Scholar 

  • Palm C J, Schollee D L, Donegan K K and Seidler R J 1996 Persistance in soil of transgenic plant produced Bacillus thuringiensis var. kurstaki ?-endotoxin. Can. J. Microbiol. 42, 1258–1262.

    Google Scholar 

  • Petras S F and Casida L E Jr 1985 Survival of Bacillus thuringiensis spores in the soil. Appl. Environ. Microbiol. 50, 28–35.

    Google Scholar 

  • Phillips D A and Hayman D S 1970 Improved procedures for clearing roots and staining parasitic and vesicular-arbuscular mycorrhizal fungi for rapid assessment of infection. Trans. Br. Mycol. Soc. 55, 158–161.

    Google Scholar 

  • Reddy M S and Rahe J E 1989 Bacillus subtilis B-2 and selected onion rhizobacteria in onion seedling rhizospheres: effects on seedling growth and indigenous rhizosphere microflora. Soil Biol. Biochem. 21, 379–383.

    Google Scholar 

  • Saxena D and Stotzky G 2001 Bacillus thuringiensis (Bt) toxin released from root exudates and biomass of Bt corn has no apparent effect on earthworms, nematodes, protozoa, bacteria, and fungi in soil. Soil Biol. Biochem. 33, 1225–1230.

    Google Scholar 

  • Sims S R and Ream J E 1997 Soil inactivation of the Bacillus thuringiensis subsp.kurstaki Cry IIA insecticidal protein within transgenic cotton tissue: laboratory microcosm and field studies. J. Agric. Food Chem. 45, 1502–1505.

    Google Scholar 

  • Tapp H and Stotzky G 1995 Insecticidal activity of the toxins from Bacillus thuringiensis subspecieskurstaki and tenebrionis adsorbed and bound on pure and soil clays. Appl. Environ. Microbiol. 61, 1786–1790.

    Google Scholar 

  • Tapp H and Stotzky G 1998 Persistence of the insecticidal toxin from Bacillus thuringiensis subsp. kurstaki in soil. Soil Biol. Biochem. 30, 471–476.

    Google Scholar 

  • Thomas D J I, Morgan A W, Whipps J M and Saunders J R 2000 Plasmid transfer between the Bacillus thuringiensis subspecies kurstaki and tenebrionis in laboratory culture and soil and in lepidopteran and coleopteran larvae. Appl. Environ. Microbiol. 66, 118–124.

    Google Scholar 

  • Toal M E, Yeomans C, Killham K and Meharg A A 2000 A review of rhizosphere carbon flow modeling. Plant Soil 222, 263–281.

    Google Scholar 

  • Venkateswerlu G and Stotzky G 1992 Binding of the protoxin and toxin protein of Bacillus thuringiensis subsp. kurstaki on clay minerals. Curr Microbiol. 25, 1–9.

    Google Scholar 

  • Vilas Bôas L A, Vilas Bôas G F L T, Saridakis H O, Lemos M V F, Lereclus D and Arantes O M N 2000 Survival and conjugation of Bacillus thuringiensis in a soil microcosm. FEMS Microbiol. Ecol. 31, 255–259.

    Google Scholar 

  • West A D, Burges H D, White R J and Wyborn C H 1984 Persistence of Bacillus thuringiensis parasporal crystal insecticidal activity in soil. J. Inver Pathol. 44, 128–133.

    Google Scholar 

  • Whipps J M 1990 Carbon economy. In The Rhizosphere. Ed. J M Lynch. pp. 59–97. John Wiley & Sons, New York.

    Google Scholar 

  • Young C S, Lethbridge G, Shaw L J and Burns R G 1995 Survival of inoculated Bacillus cereus spores and vegetative cells in nonplanted and rhizosphere soil. Soil Biol. Biochem. 27, 1017–1026.

    Google Scholar 

  • Yudina T G and Burtseva L I 1997 Activity of d-endotoxins of four Bacillus thuringiensis subspecies against prokariotes. Microbiology 66, 17–22.

    Google Scholar 

  • Yudina T G, Milko E S and Egorov N S 1996 Sensitivity of Micrococcus luteus dissociation variants to delta-endotoxins of Bacillus thuringiensis. Microbiology 65, 321–325.

    Google Scholar 

  • Zuberer D A 1994 Recovery and enumeration of viable bacteria. In Methods of Soil Analysis, part 2. Microbiological and Biochemical Properties. Eds. R W Weaver, J S Augle and P S Bottomley. pp. 120–157. Books series 5. Soil Science Society of America, Madison, WI.

    Google Scholar 

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Authors and Affiliations

  1. Centro de Ciências Biológicas, Departamento de Biologia Geral, Programa de Mestrado em Genética e Melhoramento, Universidade Estadual de Londrina, Londrina, 86051-990, Brazil

    L.H.P.L. Ferreira

  2. Centro de Ciências Biológicas, Departamento de Microbiologia, Laboratório de Ecologia Microbiana, Universidade Estadual de Londrina, Caixa Postal 6001, Londrina, 86051-990, Brazil

    J.C. Molina, C. Brasil & G. Andrade

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  1. L.H.P.L. Ferreira
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  2. J.C. Molina
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  3. C. Brasil
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  4. G. Andrade
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Correspondence to G. Andrade.

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Ferreira, L., Molina, J., Brasil, C. et al. Evaluation of Bacillus thuringiensis bioinsecticidal protein effects on soil microorganisms. Plant and Soil 256, 161–168 (2003). https://doi.org/10.1023/A:1026256700237

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