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Deciphering the rhizobacterial assemblages under the influence of genetically engineered maize carrying mcry genes

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Abstract

Genetically engineered (GE) maize has been thoroughly studied regarding its agro-environmental impact; however, its concerns for the soil environment remain. This work was aimed to decode rhizosphere microbe interactions and potential ecological hazards associated with GE maize. Rhizobacterial communities of field grown transgenic insect-resistant 2A5 maize carrying mcry1Ab and mcry2Ab genes were compared with control Z58 using PacBio sequencing platform. Also full-length 16S rDNA gene sequencing was used to verify the partial (V3–V4) sequencing results obtained in 2017. Measures of α-diversity displayed transgenic 2A5 to be significantly lower in species richness at the flowering stage; however, diversity remained undisturbed. β-diversity was least affected by genetic modifications where similar community profiles were shared by transgenic 2A5 and control Z58. In addition, root exudation patterns were found to drive variations in bacterial assemblages based on developmental stages. For example, genus Massilia successfully colonized the rhizosphere at jointing stage, while Mucilaginobacter showed higher relative abundance in flowering stages of both 2A5 and Z58. These members are known to possess attributes related to plant growth. The impact of dual-transgene insertion on nifH gene abundance was also analyzed where no apparent significant difference in nifH gene copy number was observed. Our results confirmed that full-length 16S rDNA sequencing was sufficient to provide higher taxonomic resolution. Also, results of our 2-year field trials confirmed that there is no significant impact of mcry gene integration on belowground biomasses. Therefore, GE insect-resistant 2A5 maize carrying mcry1Ab and mcry2Ab genes can continue to benefit human populations by increasing crop productivity. In future, further research needs to be catalyzed to analyze the impact of Bt-insertion on microbial community structure across the years for ecosystem sustainability.

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Data availability

Raw sequence data file is available in FASTQ format in NCBI Sequence Read Archive with SRA Bio Project ID: PRJNA686837.

References

  • Ahmad N, Mukhtar Z (2017) Genetic manipulations in crops: Challenges and opportunities. Genomics 109:494–505

    Article  CAS  Google Scholar 

  • Alok D, Annapragada H, Singh S, Murugesan S, Singh NP (2020) Symbiotic nitrogen fixation and endophytic bacterial community structure in Bt-transgenic chickpea (Cicer arietinum L). Sci Rep-Uk 10

  • Araus JL, Serret MD, Lopes MS (2019) Transgenic solutions to increase yield and stability in wheat: shining hope or flash in the pan? J Exp Bot 70:1419–1424

    Article  CAS  Google Scholar 

  • Azzouz H, Cherqui A, Campan EDM, Rahbe Y, Duport G, Jouanin L, Kaiser L, Giordanengo P (2005) Effects of plant protease inhibitors, oryzacystatin I and soybean Bowman-Birk inhibitor, on the aphid Macrosiphum euphorbiae (Homoptera, Aphididae) and its parasitoid Aphelinus abdominalis (Hymenoptera, Aphelinidae). J Insect Physiol 51:75–86

    Article  CAS  Google Scholar 

  • Bais HP, Weir TL, Perry LG, Gilroy S, Vivanco JM (2006) The role of root exudates in rhizosphere interactions with plants and other organisms. Annu Rev Plant Biol 57:233–266

    Article  CAS  Google Scholar 

  • Bawa AS, Anilakumar KR (2013) Genetically modified foods: safety, risks and public concerns-a review. J Food Sci Tech Mys 50:1035–1046

    Article  CAS  Google Scholar 

  • Beckers B, De Beeck MO, Thijs S, Truyens S, Weyens N, Boerjan W, Vangronsveld J (2016) Performance of 16 s rDNA Primer Pairs in the Study of Rhizosphere and Endosphere Bacterial Microbiomes in Metabarcoding Studies. Front Microbiol 7

  • Chen SM, Waghmode TR, Sun RB, Kuramae EE, Hu CS, Liu BB (2019) Root-associated microbiomes of wheat under the combined effect of plant development and nitrogen fertilization. Microbiome:7

  • Coz I, Saxena D, Andow DA, Zwahlen C, Stotzky G (2008) Microbial populations and enzyme activities in soil in situ under transgenic corn expressing Cry proteins from Bacillus thuringiensis. J Environ Qual 37:647–662

    Article  Google Scholar 

  • De Meyer SE, Cnockaert M, Moulin L, Howieson JG, Vandamme P (2018) Symbiotic and non-symbiotic Paraburkholderia isolated from South African Lebeckia ambigua root nodules and the description of Paraburkholderia fynbosensis sp nov. Int J Syst Evol Microbiol 68:2607–2614

    Article  Google Scholar 

  • DeSantis TZ, Hugenholtz P, Larsen N, Rojas M, Brodie EL, Keller K, Huber T, Dalevi D, Hu P, Andersen GL (2006) Greengenes, a chimera-checked 16S rRNA gene database and workbench compatible with ARB. Appl Environ Microbiol 72:5069–5072

    Article  CAS  Google Scholar 

  • Ferber D (1999) Risks and benefits - GM crops in the cross hairs. Science 286:1662–1666

    Article  CAS  Google Scholar 

  • Fikri-Benbrahim K, Chraibi M, Lebrazi S, Moumni M, Ismaili M (2017) Phenotypic and genotypic diversity and symbiotic effectivenessof rhizobia isolated from Acacia sp grown in Morocco. J Agr Sci Tech-Iran 19:201–216

    Google Scholar 

  • Hartmann A, Schmid M, van Tuinen D, Berg G (2009) Plant-driven selection of microbes. Plant Soil 321:235–257

    Article  CAS  Google Scholar 

  • Holzinger A, Becker B (2015) Desiccation tolerance in the streptophyte green alga Klebsormidium: The role of phytohormones. Commun Integr Biol 8:e1059978

    Article  CAS  Google Scholar 

  • Hothorn T, Bretz F, Westfall P (2008) Simultaneous inference in general parametric models. Biom J 50:346–363

    Article  Google Scholar 

  • Hu LF, Robert CAM, Cadot S, Zhang X, Ye M, Li BB, Manzo D, Chervet N, Steinger T, van der Heijden MGA, Schlaeppi K, Erb M (2018) Root exudate metabolites drive plant-soil feedbacks on growth and defense by shaping the rhizosphere microbiota. Nat Commun 9:2738

    Article  Google Scholar 

  • Jacoby R, Peukert M, Succurro A, Koprivova A, Kopriva S (2017) The role of soil microorganisms in plant mineral nutrition-current knowledge and future directions. Front Plant Sci 8

  • Klimova AY, Stepanov AL, Manucharova NA (2019) Specific features of nitrogen and carbon transformation in an oligotrophic peat soil. Eurasian Soil Sci 52:1223–1226

    Article  CAS  Google Scholar 

  • Kuffner M, De Maria S, Puschenreiter M, Fallmann K, Wieshammer G, Gorfer M, Strauss J, Rivelli AR, Sessitsch A (2010) Culturable bacteria from Zn- and Cd-accumulating Salix caprea with differential effects on plant growth and heavy metal availability. J Appl Microbiol 108:1471–1484

    Article  CAS  Google Scholar 

  • Kumar K, Gambhir G, Dass A, Tripathi AK, Singh A, Jha AK, Yadava P, Choudhary M, Rakshit S (2020) Genetically modified crops: current status and future prospects. Planta:251

  • Lee HR, Han SI, Rhee KH, Whang KS (2013) Mucilaginibacter herbaticus sp nov., isolated from the rhizosphere of the medicinal plant Angelica sinensis. Int J Syst Evol Microbiol 63:2787–2793

    Article  CAS  Google Scholar 

  • Li XG, Liu BA, Cui JJ, Liu DD, Ding SA, Gilna B, Luo JY, Fang ZX, Cao W, Han ZM (2011) No evidence of persistent effects of continuously planted transgenic insect-resistant cotton on soil microorganisms. Plant Soil 339:247–257

    Article  CAS  Google Scholar 

  • Liang J, Meng F, Sun S, Wu CX, Wu HY, Zhang MR, Zhang HF, Zheng XB, Song XY, Zhang ZG (2015) Community structure of arbuscular mycorrhizal fungi in rhizospheric soil of a transgenic high-methionine soybean and a near isogenic variety. PLoS One 10:e0145001

    Article  Google Scholar 

  • Liu B, Zeng Q, Yan FM, Xu HG, Xu CR (2005) Effects of transgenic plants on soil microorganisms. Plant Soil 271:1–13

    Article  CAS  Google Scholar 

  • Lu GH, Tang CY, Hua XM, Cheng J, Wang GH, Zhu YL, Zhang LY, Shou HX, Qi JL, Yang YH (2018) Effects of an EPSPS-transgenic soybean line ZUTS31 on root-associated bacterial communities during field growth. PLoS One 13

  • Marvier M, McCreedy C, Regetz J, Kareiva P (2007) A meta-analysis of effects of Bt cotton and maize on nontarget invertebrates. Science 316:1475–1477

    Article  CAS  Google Scholar 

  • Mougel C, Offre P, Ranjard L, Corberand T, Gamalero E, Robin C, Lemanceau P (2006) Dynamic of the genetic structure of bacterial and fungal communities at different developmental stages of Medicago truncatula Gaertn. cv. Jemalong line J5. New Phytol 170:165–175

    Article  CAS  Google Scholar 

  • Mus F, Crook MB, Garcia K, Costas AG, Geddes BA, Kouri ED, Paramasivan P, Ryu MH, Oldroyd GED, Poole PS, Udvardi MK, Voigt CA, Ane JM, Peters JW (2016) Symbiotic Nitrogen Fixation and the Challenges to Its Extension to Nonlegumes. Appl Environ Microbiol 82:3698–3710

    Article  CAS  Google Scholar 

  • Na XF, Xu TT, Li M, Ma F, Kardol P (2017) Bacterial diversity in the rhizosphere of two phylogenetically closely related plant species across environmental gradients. J Soils Sediments 17:122–132

    Article  CAS  Google Scholar 

  • Ofek M, Hadar Y, Minz D (2012) Ecology of Root Colonizing Massilia (Oxalobacteraceae). PLoS One 7:e40117

    Article  CAS  Google Scholar 

  • Philippot L, Raaijmakers JM, Lemanceau P, van der Putten WH (2013) Going back to the roots: the microbial ecology of the rhizosphere. Nat Rev Microbiol 11:789–799

    Article  CAS  Google Scholar 

  • Poly F, Monrozier LJ, Bally R (2001) Improvement in the RFLP procedure for studying the diversity of nifH genes in communities of nitrogen fixers in soil. Res Microbiol 152:95–103

    Article  CAS  Google Scholar 

  • Pootakham W, Mhuantong W, Yoocha T, Putchim L, Sonthirod C, Naktang C, Thongtham N, Tangphatsornruang S (2017) High resolution profiling of coral-associated bacterial communities using full-length 16S rRNA sequence data from PacBio SMRT sequencing system. Sci Rep-Uk:7

  • Rilling JI, Acuna JJ, Sadowsky MJ, Jorquera MA (2018) Putative Nitrogen-Fixing Bacteria Associated With the Rhizosphere and Root Endosphere of Wheat Plants Grown in an Andisol From Southern Chile. Front Microbiol:9

  • Roley SS, Duncan DS, Liang D, Garoutte A, Jackson RD, Tiedje JM, Robertson GP (2018) Associative nitrogen fixation (ANF) in switchgrass (Panicum virgatum) across a nitrogen input gradient. PLoS One 13:e0197320

    Article  Google Scholar 

  • Schloss PD, Westcott SL, Ryabin T, Hall JR, Hartmann M, Hollister EB, Lesniewski RA, Oakley BB, Parks DH, Robinson CJ, Sahl JW, Stres B, Thallinger GG, Van Horn DJ, Weber CF (2009) Introducing mothur: Open-Source, Platform-Independent, Community-Supported Software for Describing and Comparing Microbial Communities. Appl Environ Microbiol 75:7537–7541

    Article  CAS  Google Scholar 

  • Shabayev VP, Bocharnikova EA, Ostroumov VE (2019) Plant and Soil Mechanisms of Plant Resistance to Cd Toxicity under Application of Plant Growth Promoting Rhizobacterium in Soil Contaminated with Heavy Metal. Biol Bull 46:381–386

    Article  CAS  Google Scholar 

  • Singer E, Bushnell B, Coleman-Derr D, Bowman B, Bowers RM, Levy A, Gies EA, Cheng JF, Copeland A, Klenk HP, Hallam SJ, Hugenholtz P, Tringe SG, Woyke T (2016) High-resolution phylogenetic microbial community profiling. Isme J 10:2020–2032

    Article  Google Scholar 

  • Song FS, Ni DH, Li H, Duan YB, Yang YC, Ni JL, Lu XZ, Wei PC, Li L, Yang JB (2014) A novel synthetic Cry1Ab gene resists rice insect pests. Genet Mol Res 13:2394–2408

    Article  CAS  Google Scholar 

  • Tremblay J, Singh K, Fern A, Kirton ES, He SM, Woyke T, Lee J, Chen F, Dangl JL, Tringe SG (2015) Primer and platform effects on 16S rRNA tag sequencing. Front Microbiol 6

  • Wang Q, Garrity GM, Tiedje JM, Cole JR (2007) Naive Bayesian classifier for rapid assignment of rRNA sequences into the new bacterial taxonomy. Appl Environ Microbiol 73:5261–5267

    Article  CAS  Google Scholar 

  • Wang S, Pablo GP, Ye J, Huang DF (2012) Abundance and diversity of nitrogen-fixing bacteria in rhizosphere and bulk paddy soil under different duration of organic management. World J Microbiol Biotechnol 28:493–503

    Article  Google Scholar 

  • Wen ZL, Yang MK, Du MH, Zhong ZZ, Lu YT, Wang GH, Hua XM, Fazal A, Mu CH, Yan SF, Zhen Y, Yang RW, Qi JL, Hong Z, Lu GH, Yang YH (2019) Enrichments/Derichments of Root-Associated Bacteria Related to Plant Growth and Nutrition Caused by the Growth of an EPSPS-Transgenic Maize Line in the Field. Front Microbiol:10

  • Wen ZL, Yang MK, Fazal A, Liao YH, Cheng LR, Hua XM, Hu DQ, Shi JS, Yang RW, Lu GH, Qi JL, Hong Z, Qian QP, Yang YH (2020) Differential impacts on bacterial composition and abundance in rhizosphere compartments between Al-tolerant and Al-sensitive soybean genotypes in acidic soil. J Microbiol Biotechnol 30:1169–1179

    Article  Google Scholar 

  • Yang TY, Liu GL, Li YC, Zhu SM, Zou AL, Qi JL, Yang YH (2012) Rhizosphere microbial communities and organic acids secreted by aluminum-tolerant and aluminum-sensitive soybean in acid soil. Biol Fertil Soils 48:97–108

    Article  CAS  Google Scholar 

  • Zhang YJ, Xie M, Peng DL (2013) Effects of transgenic crops on soil microorganisms: a review. Ying Yong Sheng Tai Xue Bao 24:2685–2690

    CAS  Google Scholar 

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Acknowledgment

We are grateful to Prof. Xuehui Dong of College of Agronomy and Biotechnology, China Agriculture University, for providing maize seeds of transgenic insect-resistant maize 2A5 and its control variety Z58.

Funding

This work was supported by the grants from National Important Science & Technology Specific Project (2016ZX08011-003), the National Natural Science Foundation of China (31870495), and the Program for Changjiang Scholars and Innovative Research Team in University from the Ministry of Education of China (IRT_14R27).

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Contributions

YHY, GHL, and JLQ conceived and designed the experiments; AF, ZLW, MKY, and YHL performed experiments and analyzed data; JYF, CH, XW, WCJ, FA, DQH, TMY, and ZH contributed to the resources; AF wrote the manuscript; YHY and GHL contributed to reviewing and editing the manuscript.

Corresponding authors

Correspondence to Guihua Lu, Jinliang Qi or Yonghua Yang.

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Ethics statement

The Ministry of Agriculture of the People’s Republic of China issued permission for the location. The field studies did not involve endangered species. The experimental field was not protected or privately owned in any way.

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All authors participated and approved the final manuscript to be published.

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The authors declare that they have no known competing financial interests or personal relationships that could have appeared to influence the work reported in this paper.

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Fazal, A., Wen, Z., Yang, M. et al. Deciphering the rhizobacterial assemblages under the influence of genetically engineered maize carrying mcry genes. Environ Sci Pollut Res 28, 60154–60166 (2021). https://doi.org/10.1007/s11356-021-14901-7

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