Skip to main content
Log in

The influence of Bt-transgenic maize pollen on the bacterial diversity in the midgut of Apis mellifera ligustica

  • Original article
  • Published:
Apidologie Aims and scope Submit manuscript

Abstract

Honeybees are subjected to direct contact with transgenic maize pollen due to their feeding activities on pollen. The potential side effects of transgenic cry1Ah-maize pollen on the midgut bacteria of the larvae and worker bees of Apis mellifera ligustica were investigated through denaturing gradient gel electrophoresis under both laboratory and field conditions. Newly emerged bees were fed transgenic cry1Ah-maize pollen, normal maize pollen, linear cry1Ah gene DNA, supercoiled plasmid DNA, and sugar syrup under the laboratory conditions. The results showed that there were no significant differences in the midgut bacterial community composition among the five treatments. No significant effects were observed in the midgut communities between larvae and adult honeybees fed transgenic cry1Ah-maize pollen and non-transgenic maize pollen in the field trials.

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.

Institutional subscriptions

Figure 1.
Figure 2.
Figure 3.
Figure 4.
Figure 5.
Figure 6.
Figure 7.

Similar content being viewed by others

References

  • Al-Deeb, M.A., Wilde, G.E., Blair, J.M., Todd, T.C. (2003) Effect of Bt corn for corn rootworm control on nontarget soil microarthropods and nematodes. Environ. Entomol. 32, 859–865

    Article  Google Scholar 

  • Babendreier, D., Joller, D., Romeis, J., Bigler, F., Widmer, F. (2007) Bacterial community structures in honeybee intestines and their response to two insecticidal proteins. FEMS Microbiol. Ecol. 59, 600–610

    Article  PubMed  CAS  Google Scholar 

  • Baumgarte, S., Tebbe, C.C. (2005) Field studies on the environmental fate of the Cry1Ab Bt-toxin produced by transgenic maize (MON810) and its effect on bacterial communities in the maize rhizosphere. Mol. Ecol. 14, 2539–2551

    Article  PubMed  CAS  Google Scholar 

  • Blackwood, C.B., Buyer, J.S. (2004) Soil microbial communities associated with Bt and non-Bt corn in three soils. J. Environ. Qual. 33, 832–836

    Article  PubMed  CAS  Google Scholar 

  • Clive J. (2012) Global Status of Commercialized Biotech/GM Crops: 2011. ISAAA Brief No. 43-2011

  • Cox-Foster, D.L., Conlan, S., Holmes, E.C., Palacios, G., Evans, J.D., Moran, N.A., Quan, P.L., Briese, T., Hornig, M., Geiser, D.M. (2007) A metagenomic survey of microbes in honey bee colony collapse disorder. Science 318, 283–287

    Article  PubMed  CAS  Google Scholar 

  • Dai, P.L., Zhou, W., Zhang, J., Jiang, W.Y., Wang, Q., Cui, H.J., Sun, J.H., Wu, Y.Y., Zhou, T. (2012a) The effects of Bt Cry1Ah toxin on worker honeybees (Apis mellifera ligustica and Apis cerana cerana). Apidologie 43, 384–391

    Article  CAS  Google Scholar 

  • Dai, P.L., Zhou, W., Zhang, J., Cui, H.J., Wang, Q., Jiang, W.Y., Sun, J.H., Wu, Y.Y., Zhou, T. (2012b) Field assessment of Bt cry1Ah corn pollen on the survival, development and behavior of Apis mellifera ligustica. Ecotoxicol. Environ. Saf. 79, 232–237

    Article  PubMed  CAS  Google Scholar 

  • Daudu, C.K., Muchaonyerwa, P., Mnkeni, P.N.S. (2009) Litterbag decomposition of genetically modified maize residues and their constituent Bacillus thuringiensis protein (Cry1Ab) under field conditions in the central region of the Eastern Cape, South Africa. Agric. Ecosyst. Environ. 134, 153–158

    Article  CAS  Google Scholar 

  • Duan, J.J., Marvier, M., Huesing, J., Dively, G., Huang, Z.Y. (2008) A meta-analysis of effects of Bt crops on honey bees (Hymenoptera: Apidae). PLoS One 3, e1415

    Article  PubMed  Google Scholar 

  • Gathmann, A., Wirooks, L., Hothorn, L.A., Bartsch, D., Schuphan, I. (2006) Impact of Bt maize pollen (MON810) on lepidopteran larvae living on accompanying weeds. Mol. Ecol. 15, 2677–2685

    Article  PubMed  CAS  Google Scholar 

  • Gruber, H., Paul, V., Meyer, H.H.D., Müller, M.M. (2012) Determination of insecticidal Cry1Ab protein in soil collected in the final growing seasons of a nine-year field trial of Bt-maize MON810. Transgenic Res. 21, 77–78

    Article  PubMed  CAS  Google Scholar 

  • Hendriksma, H.P., Härtel, S., Steffan-Dewenter, I. (2011) Testing pollen of single and stacked insect-resistant Bt-maize on in vitro reared honey bee larvae. PLoS One 6, e28174

    Article  PubMed  CAS  Google Scholar 

  • Higgins, L.S., Babcock, J., Neese, P., Layton, R.J., Moellenbeck, D.J., Storer, N. (2009) Three-year field monitoring of Cry1F, event DAS-Ø15Ø7-1, maize hybrids for nontarget arthropod effects. Environ. Entomol. 38, 281–292

    Article  PubMed  Google Scholar 

  • Lima, M.A.P., Pires, C.S.S., Guedes, R.N.C., Nakasu, E.Y.T., Lara, M.S., Fontes, E.M.G., Sujii, E.R., Dias, S.C., Campos, L.A.O. (2011) Does Cry1Ac Bt-toxin impair development of worker larvae of Africanized honey bee? J. Appl. Entomol. 135, 415–422

    Article  CAS  Google Scholar 

  • Malone, L.A., Todd, J.H., Burgess, E.P.J., Christeller, J.T. (2004) Development of hypopharyngeal glands in adult honey bees fed with a Bt toxin, a biotin-binding protein and a protease inhibitor. Apidologie 35, 655–664

    Article  CAS  Google Scholar 

  • Martinson, V.G., Danforth, B.N., Minckley, R.L., Rueppell, O., Tingek, S., Moran, N.A. (2011) A simple and distinctive microbiota associated with honey bees and bumble bees. Mol. Ecol. 20, 619–628

    Article  PubMed  Google Scholar 

  • Mohr, K.I., Tebbe, C.C. (2006) Diversity and phylotype consistency of bacteria in the guts of three bee species (Apoidea) at an oilseed rape field. Environ. Microbiol. 8, 258–272

    Article  PubMed  CAS  Google Scholar 

  • Mohr, K., Tebbe, C. (2007) Field study results on the probability and risk of a horizontal gene transfer from transgenic herbicide-resistant oilseed rape pollen to gut bacteria of bees. Appl. Microbiol. Biot. 75, 573–582

    Article  CAS  Google Scholar 

  • Nakatsu, C.H., Torsvik, V., Ovreas, L. (2000) Soil community analysis using DGGE of 16 s rDNA polymerase chain reaction products. Soil Sci. Soc. Am. J. 64, 1382–1388

    Article  CAS  Google Scholar 

  • Prischl, M., Hackl, E., Pastar, M., Pfeiffer, S., Sessitsch, A. (2012) Genetically modified Bt maize lines containing cry3Bb1, cry1A105 or cry1Ab2 do not affect the structure and functioning of root-associated endophyte communities. Appl. Soil Ecol. 54, 39–48

    Article  Google Scholar 

  • Ramirez-Romero, R., Chaufaux, J., Pham-Delegue, M. (2005) Effects of Cry1Ab protoxin, deltamethrin and imidacloprid on the foraging activity and the learning performances of the honeybee Apis mellifera, a comparative approach. Apidologie 36, 601–611

    Article  CAS  Google Scholar 

  • Romeis, J., Bartsch, D., Bigler, F., Candolfi, M.P., Gielkens, M.M.C., et al. (2008) Assessment of risk of insect-resistant transgenic crops to nontarget arthropods. Nat. Biotechnol. 26, 203–208

    Article  PubMed  CAS  Google Scholar 

  • Rose, R., Dively, G.P., Pettis, J. (2007) Effects of Bt corn pollen on honey bees: emphasis on protocol development. Apidologie 38, 368–377

    Article  Google Scholar 

  • Shan, G., Embrey, S.K., Herman, R.A., McCormick, R. (2008) Cry1F protein not detected in soil after three years of transgenic Bt corn (1507 corn) use. Environ. Entomol. 37, 255–262

    Article  PubMed  CAS  Google Scholar 

  • Wang Y.F. (2010) Field trails and genetic stability analysis of insect resistant transgenic Bt maize. Ph.D. dissertation, Northeast Agricultural University, Heilongjiang

  • Wang, Y.B., Lang, Z., Zhang, J., He, K.L., Song, F.P., Huang, D.F. (2008) Ubi1 intron-mediated enhancement of the expression of Bt cry1Ah gene in transgenic maize (Zea mays L.). Chin. Sci. Bull. 53, 3185–3190

    Article  CAS  Google Scholar 

  • Xue, J., Liang, G., Crickmore, N., Li, H., He, K., Song, F., Feng, X., Huang, D., Zhang, J. (2008) Cloning and characterization of a novel Cry1A toxin from Bacillus thuringiensis with high toxicity to the Asian corn borer and other lepidopteran insects. FEMS Microbiol. Lett. 280, 95–101

    Article  PubMed  CAS  Google Scholar 

  • Yoshiyama, M., Kimura, K. (2009) Bacteria in the gut of Japanese honeybee, Apis cerana japonica, and their antagonistic effect against Paenibacillus larvae, the causal agent of American foulbrood. J. Invertebr. Pathol. 102, 91–96

    Article  PubMed  Google Scholar 

  • Zwahlen, C., Hilbeck, A., Nentwig, W. (2007) Field decomposition of transgenic Bt maize residue and the impact on non-target soil invertebrates. Plant Soil 300, 245–257

    Article  CAS  Google Scholar 

Download references

Acknowledgments

This work was supported by grants from the Major State Basic Research Development Program of China (973 Program; No. 2009CB118902) and the National Transgenic Major Program of China (No. 2009ZX08011-016B).

Author information

Authors and Affiliations

Authors

Corresponding author

Correspondence to Jie Zhang.

Additional information

Manuscript editor: Monique Gauthier

L’influence du pollen de maïs-Bt transgénique sur la diversité bactérienne de l’intestin moyen d’ Apis mellifera ligustica

Maïs transgénique / Apis mellifera / flore intestinale / électrophorèse sur gel à gradient dénaturant

Der Einfluss von Bt-transgenem Maispollen auf die bakterielle Diversität im Mitteldarm von Apis mellifera ligustica

transgener Mais / Apis mellifera / Darmflora / denaturierende Gradientengelelektrophorese

Li-Li Geng and Hong-Juan Cui contributed equally to this work.

Rights and permissions

Reprints and permissions

About this article

Cite this article

Geng, LL., Cui, HJ., Dai, PL. et al. The influence of Bt-transgenic maize pollen on the bacterial diversity in the midgut of Apis mellifera ligustica . Apidologie 44, 198–208 (2013). https://doi.org/10.1007/s13592-012-0171-8

Download citation

  • Received:

  • Revised:

  • Accepted:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1007/s13592-012-0171-8

Keywords

Navigation