Skip to main content
Log in

Temporal dynamics of microbial communities in the rhizosphere of two genetically modified (GM) maize hybrids in tropical agrosystems

  • Original Paper
  • Published:
Antonie van Leeuwenhoek Aims and scope Submit manuscript

Abstract

The use of genetically modified (GM) plants still raises concerns about their environmental impact. The present study aimed to evaluate the possible effects of GM maize, in comparison to the parental line, on the structure and abundance of microbial communities in the rhizosphere. Moreover, the effect of soil type was addressed. For this purpose, the bacterial and fungal communities associated with the rhizosphere of GM plants were compared by culture-independent methodologies to the near-isogenic parental line. Two different soils and three stages of plant development in two different periods of the year were included. As evidenced by principal components analysis (PCA) of the PCR-DGGE profiles of evaluated community, clear differences occurred in these rhizosphere communities between soils and the periods of the year that maize was cultivated. However, there were no discernible effects of the GM lines as compared to the parental line. For all microbial communities evaluated, soil type and the period of the year that the maize was cultivated were the main factors that influenced their structures. No differences were observed in the abundances of total bacteria between the rhizospheres of GM and parental plant lines.

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

Similar content being viewed by others

References

  • Anderson IC, Campbell CD, Prosser JI (2003a) Diversity of fungi in organic soils under a moorland-Scots pine (Pinus sylvestris L.) gradient. Environ Microbiol 11:1121–1132

    Article  Google Scholar 

  • Anderson IC, Campbell CD, Prosser JI (2003b) Potential bias of fungal 18S rRNA and internal transcribed spacer polymerase chain reaction primers for estimating fungal biodiversity in soil. Environ Microbiol 1:36–47

    Article  Google Scholar 

  • Andreote FD, Mendes R, Dini-Andreote F, Rossetto PB, Labate CA, Pizzirani-Kleiner AA, van Elsas JD, Azevedo JL, Araújo WL (2008) Transgenic tobacco revealing altered bacterial diversity in the rhizosphere during early plant development. Antonie Van Leeuwenhoek 93:415–424

    Article  PubMed  CAS  Google Scholar 

  • Andreote FD, Carneiro RT, Salles JF, Marcon J, Labate CA, Azevedo JL, Araújo WL (2009) Culture-independent assessment of Alphaproteobacteria related to order Rhizobiales and the diversity of cultivated Methylobacterium in the rhizosphere and rhizoplane of transgenic eucalyptus. Microb Ecol 57:82–93

    Article  PubMed  Google Scholar 

  • Bach HJ, Tomanova J, Schloter JC, Munch JC (2002) Enumeration of total bacteria with genes for proteolytic activity in pure cultures and in environmental samples by quantitative PCR mediated amplification. J Microbiol Methods 49:235–245

    Article  PubMed  CAS  Google Scholar 

  • Badea EM, Chelu F, Lacatusu A (2010) Results regarding the levels of Cry1Ab protein in transgenic corn tissue (MON810) and the fate of Bt protein in three soil types. Rom Biotechnol Lett 15:55–62

    CAS  Google Scholar 

  • Barriuso J, Valverde JR, Mellado RP (2012) Effect of Cry1Ab protein on rhizobacterial communities of Bt-maize over a four-year cultivation period. PLoS ONE 7:e35481

    Article  PubMed  CAS  Google Scholar 

  • Baumgarten S, Tebbe CC (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  Google Scholar 

  • Blackwood CB, Buyer JS (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 

  • Bruinsma M, Kowalchuk GA, van Veen JA (2003) Effects of genetically modified plants on microbial communities and processes in soil. Biol Fertil Soils 37:329–337

    Google Scholar 

  • Carpenter JE (2011) Impacts of GM crops on biodiversity. GM Crops 1:1–17

    Google Scholar 

  • Castaldini M, Turrini A, Sbrana C, Beneditti A, Marchionni M, Mocali S, Fabiani A, Landi S, Santomassimo F, Pietrangeli B, Nuti MP, Miclaus N, Giovannetti M (2005) Impact of Bt corn in rhizospheric and soil eubacterial communities and on beneficial mycorrhizal symbiosis in experimental microcosms. Appl Environ Microbiol 71:6719–6729

    Article  PubMed  CAS  Google Scholar 

  • Chauhan PS, Chaudhry V, Mishra S, Nautiyal CS (2011) Uncultured bacterial diversity in tropical maize (Zea mays L.) rhizosphere. J Basic Microbiol 51:15–32

    Article  PubMed  CAS  Google Scholar 

  • Chiarini L, Bevivino A, Dalmastri C, Nacamulli C, Tabacchioni S (1998) Influence of plants development, cultivar and soil type on microbial colonization of maize root. Appl Soil Ecol 8:11–18

    Article  Google Scholar 

  • Chun YJ, Kim DY, Kim HJ, Park KW, Jeong S-C, Park S, Lee B, Ham CH, Kim HM, Kim C-G (2011) Do transgenic chili pepper plants producing viral coat protein affect the structure of a soil microbial community? Appl Soil Ecol 51:130–138

    Article  Google Scholar 

  • da Silva KRA, Salles JF, Seldin L, van Elsas JD (2003) Application of a novel Paenibacillus-specific PCR-DGGE method and sequence analysis to assess the diversity of Paenibacillus spp. in the maize rhizosphere. J Microbiol Methods 54:213–231

    Article  PubMed  Google Scholar 

  • di Giovanni GD, Watrud LS, Seidler RJ, Widmer F (1999) Comparison of parental and transgenic alfalfa rhizosphere bacterial communities using BIOLOG GN metabolic fingerprinting and Enterobacterial Intergenic Consensus Sequence-PCR (ERIC-PCR). Microbiol Ecol 37:129–139

    Article  Google Scholar 

  • Dively GP, Rose R, Sears MK, Hellmich RL, Stanley-Horn DE, Calvin DD, Russo JM, Anderson PL (2004) Effects on monarch butterfly larvae (Lepidoptera: Danaidae) after continuous exposure to Cry1Ab-expressing corn during anthesis. Ann Entomol Soc Am 33:1116–1125

    CAS  Google Scholar 

  • Donegan KK, Seidler RJ, Porteous LA, Digiovanni G, Widmer F, Watrud LS (1999) A field study with genetically engineered alfafa inoculated with recombinant Sinorhizobium meliloti: effects on the soil ecosystem. J Appl Ecol 6:920–936

    Article  Google Scholar 

  • Dunfield KE, Germida JJ (2004) Impact of genetically modified crops on soil-and plant-associated microbial communities. J Environ Qual 33:806–815

    Article  PubMed  CAS  Google Scholar 

  • Eichner CA, Erb RW, Timmis KN, Wagner-Dobler I (1999) Thermal gradient gel electrophoresis analysis of bioprotection from pollutant shocks in the activated sludge microbial community. Appl Environ Microbiol 65:102–109

    PubMed  CAS  Google Scholar 

  • Feng Y, Ling L, Fan H, Liu Y, Tan F, Shu Y, Wang J (2011) Effects of temperature, water content and pH on degradation of Cry1Ab protein released from Bt corn straw in soil. Soil Biol Biochem 43:1600–1606

    Article  CAS  Google Scholar 

  • Garbeva P, van Veen JA, van Elsas JD (2004) Microbial diversity in soil: selection of microbial populations by plant and soil type and applications for disease suppressiveness. Annu Rev Phytopathol 42:243–270

    Article  PubMed  CAS  Google Scholar 

  • Gelsomino A, Keijzer-Wolters AC, Cacco G, van Elsas JD (1999) Assessment of bacterial community structure in soil by polymerase chain reaction and denaturing gradient gel electrophoresis. J Microbiol Methods 38:1–15

    Article  PubMed  CAS  Google Scholar 

  • Gruber H, Paul V, Meyer HHD, Müller 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 21:77–88

    Article  PubMed  CAS  Google Scholar 

  • Hanulla SE, Boschker HTS, de Boer W, van Veen JA (2012) 13C pulse-labeling assessment of the community structure of active fungi in the rhizosphere of a genetically starch-modified potato (Solanum tuberosum) cultivar and its parental isoline. New Phytol 194:784–799

    Article  Google Scholar 

  • Helassa N, Charek AM, Quiquampoix H, Noinville S, Déjardin P, Frutos R, Staunton S (2011) Effects of physicochemical interactions and microbial activity on the persistence of Cry1Ab Bt (Bacillus thuringiensis) toxin in soil. Soil Biol Biochem 5:1089–1097

    Article  Google Scholar 

  • Heuer H, Krsek M, Baker P, Smalla K, Wellington EMH (1997) Analysis of actinomycete communities by specific amplification of genes encoding 16S rRNA and gel electrophoretic separation in denaturing gels. Appl Environ Microbiol 8:3233–3241

    Google Scholar 

  • Icoz I, Stotzky G (2007) Cry3Bb1 protein from Bacillus thuringiensis in root exudates and biomass of transgenic corn does not persist in soil. Transgenic Res 4:609–620

    Google Scholar 

  • Icoz I, Stotzky G (2008) Fate and effects of insect-resistant Bt crops in soil ecosystems. Soil Biol Biochem 40:559–586

    Article  CAS  Google Scholar 

  • James C (2010) Global status of commercialized biotech/GM Crops: ISAAA Brief No. 42. ISAAA: Ithaca, NY

  • Jurelevicius D, Korenblum E, Casella R, Vital RL, Seldin L (2010) Polyphasic analysis of bacterial community in the rhizosphere and roots of Cyperus rotundus L. grown in a petroleum-contaminated soil. J Microbiol Biotechnol 5:862–870

    Article  Google Scholar 

  • Lamarche J, Hamelin RC (2007) No evidence of an impact on the rhizosphere diazotroph community by the expression of Bacillus thuringiensis Cry1Ab toxin by Bt white spruce. Applied Environ Microbiol 73:6577–6583

    Article  CAS  Google Scholar 

  • Lee S-H, Kim C-G, Kang H (2011) Temporal dynamics of bacterial and fungal communities in a genetically modified (GM) rice ecosystem. Microbiol Ecol 61:646–659

    Article  Google Scholar 

  • Leps J, Smilauer P (2003) Multivariate analysis of ecological data using CANOCO. University Press, Cambridge

    Book  Google Scholar 

  • Lynch JM, Benedetti A, Insam H, Nuti MP, Smalla K, Torsvik V, Nannipieri P (2004) Microbial diversity in soil: ecological theories, the contribution of molecular techniques and the impact of transgenic plants and transgenic microorganism. Biol Fertil Soils 40:363–385

    Article  CAS  Google Scholar 

  • McLaren J, Copping L (2011) Transgenic maize—the registration status of lines that have been commercialised: the first in a series that examines the GM crop market. Outlooks Pest Manag 2:66–73

    Article  Google Scholar 

  • Motavalli PP, Kremer RJ, Fang M, Means NE (2004) Impact of genetically modified crops and their management on soil microbial mediated plant nutrient transformations. J Environ Qual 33:816–824

    Article  PubMed  CAS  Google Scholar 

  • Muyzer G, de Wall EC, Uitterlinden AG (1993) Profiling of complex microbial population by denaturing gradient gel electrophoresis analysis of polymerase chain reaction—amplified genes coding for 16S rRNA. Appl Environ Microbiol 59:695–700

    PubMed  CAS  Google Scholar 

  • Nübel U, Engelen B, Felske A, Snaidr J, Wieshuber A, Amann RI, Ludwig W, Backhaus H (1996) Sequence heterogeneities of genes encoding 16S rRNAs in Paenibacillus polymyxa detected by temperature gradient gel electrophoresis. J Bacteriol 19:5636–5643

    Google Scholar 

  • Raybould A, Higgins LS, Horak MJ, Layton RJ, Storer NP, de la Fuente JM, Herman RA (2011) Assessing the ecological risks from the persistence and spread of feral populations of insect-resistant transgenic maize. Transgenic Res 3:55–64

    Google Scholar 

  • Rui YK, Yi GX, Zhao J, Wang BM, Li ZH, Zhai ZX, He ZP, Li QX (2005) Changes of Bt toxin in the rhizosphere of transgenic Bt cotton and its influence on soil functional bacteria. World J Microbiol Biotechnol 21:1279–1284

    Article  CAS  Google Scholar 

  • Salles JF, van Veen JA, van Elsas JD (2004) Multivariate analyses of Burkholderia species in soil: effect of crop and land use history. Appl Environ Microbiol 70:4012–4020

    Article  PubMed  CAS  Google Scholar 

  • Sambrook J, Fritsch EF, Manniatis T (1989) Molecular cloning: a laboratory manual, 2nd edn. Cold Spring Harbor Laboratory Press, Cold Spring Harbor

    Google Scholar 

  • Saxena D, 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

    Article  CAS  Google Scholar 

  • Saxena D, Flores S, Stotzky G (2002) Bt toxin is released in root exudates from 12 transgenic corn hybrids representing three transformation events. Soil Biol Biochem 34:133–137

    Article  CAS  Google Scholar 

  • Seldin L, Rosado AS, da Cruz DW, Nobrega A, van Elsas JD (1998) Comparison of Paenibacillus azotofixans isolated from rhizoplane, rhizosphere, and non-root associated soil from maize planted in two different Brazilian soils. Appl Environ Microbiol 64:3860–3868

    PubMed  CAS  Google Scholar 

  • Semenov AV, Pereira e Silva MC, Szuturc-Koestsier AE, Schmitt H, Salles JF, van Elsas JD (2012) Impact of incorporated fresh 13C potato tissues on the bacterial and fungal community composition of soil. Soil Biol Biochem 49:88–95

    Google Scholar 

  • Tan F, Wang J, Feng Y, Chi G, Kong H, Qiu H, Wei S (2010) Bt corn plants and their straw have no apparent impact on soil microbial communities. Plant Soil 329:349–364

    Article  CAS  Google Scholar 

  • Tan F, Wang J, Chen Z, Feng Y, Chi G, Rehman SU (2011) Assessment of the arbuscular mycorrhizal fungal community in roots and rhizosphere soils of Bt corn and their non-Bt isolines. Soil Biol Biochem 43:2473–2479

    Article  CAS  Google Scholar 

  • Van Veen JA, van Overbeek LS, van Elsas JD (1997) Fate and activity of microorganisms introduced into soil. Microbiol Mol Biol Rev 61:121–135

    PubMed  Google Scholar 

  • Yu HL, Li YH, Wu KM (2011) Risk assessment and ecological effects of transgenic Bacillus thuringiensis crops on non-target organisms. J Integrative Plant Biol 7:520–538

    Article  Google Scholar 

Download references

Acknowledgments

This study was supported by the Coordenação de Aperfeiçoamento de Pessoal de Nível Superior (CAPES) and Fundação de Amparo à Pesquisa do Estado do Rio de Janeiro (FAPERJ). Thanks are also due to the Conselho Nacional de Pesquisa (CNPq) for providing a fellowship to Simone Cotta to come over to the Groningen Microbial Ecology laboratory. The Soil Biotechnology Foundation is acknowledged for providing financial support to Armando C F Dias and received a graduate fellowship from FAPESP (no. 2008/54013-8).

Author information

Authors and Affiliations

Authors

Corresponding author

Correspondence to Lucy Seldin.

Electronic supplementary material

Below is the link to the electronic supplementary material.

Supplementary material 1 (DOCX 14 kb)

Rights and permissions

Reprints and permissions

About this article

Cite this article

Cotta, S.R., Dias, A.C.F., Marriel, I.E. et al. Temporal dynamics of microbial communities in the rhizosphere of two genetically modified (GM) maize hybrids in tropical agrosystems. Antonie van Leeuwenhoek 103, 589–601 (2013). https://doi.org/10.1007/s10482-012-9843-7

Download citation

  • Received:

  • Accepted:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1007/s10482-012-9843-7

Keywords

Navigation