Skip to main content

Limited effect of planting transgenic rice on the soil microbiome studied by continuous 13CO2 labeling combined with high-throughput sequencing

Applied Microbiology and Biotechnology volume 103, pages 4217–4227 (2019)Cite this article

Abstract

The planting of transgenic rice has aroused ongoing controversy, due to the public anxiety surrounding the potential risk of transgenic rice to health and the environment. The soil microbial community plays an important environmental role in the plant-soil-microbe system; however, few studies have focused on the effect of transgenic rice on the soil rhizospheric microbiome. We labeled transgenic gene rice (TT51, transformed with Cry1Ab/1Ac gene), able to produce the Bt (Bacillus thuringiensis) toxin, its parental variety (Minghui 63), and a non-parental variety (9931) with 13CO2. The DNA of the associated soil rhizospheric microbes was extracted, subjected to density gradient centrifugation, followed by high-throughput sequencing of bacterial 16S rRNA gene. Unweighted unifrac analysis of the sequencing showed that transgenic rice did not significantly change the soil bacterial community structure compared with its parental variety. The order Opitutales, affiliated to phylum Verrucomicrobia and order Sphingobacteriales, was the main group of labeled bacteria in soil planted with the transgenic and parental varieties, while the orders Pedosphaerales, Chthoniobacteraceae, also affiliated to Verrucomicrobia, and the genus Geobacter, affiliated to class Deltaproteobacteria, dominated in the soil of the non-parental rice variety. The non-significant difference in soil bacterial community structure of labeled microbes between the transgenic and parental varieties, but the comparatively large difference with the non-parental variety, suggests a limited effect of planting transgenic Bt rice on the soil microbiome.

This is a preview of subscription content, access via your institution.

Access options

Buy single article

Instant access to the full article PDF.

USD 39.95

Price excludes VAT (USA)
Tax calculation will be finalised during checkout.

Fig. 1
Fig. 2
Fig. 3
Fig. 4

References

  • Ahn JH, Choi MY, Kim BY, Lee JS, Song J, Kim GY, Weon HY (2014) Effects of water-saving irrigation on emissions of greenhouse gases and prokaryotic communities in rice paddy soil. Microb Ecol 68:271–283

    Article  CAS  PubMed  Google Scholar 

  • Ai C, Liang G, Sun J, Wang X, He P, Zhou W, He X (2015) Reduced dependence of rhizosphere microbiome on plant-derived carbon in 32-year long-term inorganic and organic fertilized soils. Soil Biol Biochem 80:70–78

    Article  CAS  Google Scholar 

  • Breidenbach B, Brenzinger K, Brandt FB, Blaser MB, Conrad R (2017) The effect of crop rotation between wetland rice and upland maize on the microbial communities associated with roots. Plant Soil 419:435–445

    Article  CAS  Google Scholar 

  • Chen M, Shelton A, Ye GY (2011) Insect-resistant genetically modified rice in China: from research to commercialization. Annu Rev Entomol 56:81–101

    Article  CAS  PubMed  Google Scholar 

  • Chin K-J, Liesack W, Janssen PH (2001) Opitutus terrae gen. nov., sp. nov., to accommodate novel strains of the division ‘Verrucomicrobia’ isolated from rice paddy soil. Int J Syst Evol Micr 51:1965–1968

    Article  CAS  Google Scholar 

  • Chun YJ, Kim HJ, Park KW, Jeong SC, Lee B, Back K, Kim HM (2012) Two-year field study shows little evidence that PPO-transgenic rice affects the structure of soil microbial communities. Biol Fert Soils 48:453–461

    Article  Google Scholar 

  • Collet S, Reim A, Ho A, Frenzel P (2015) Recovery of paddy soil methanotrophs from long term drought. Soil Biol Biochem 88:69–72

    Article  CAS  Google Scholar 

  • Dennis PG, Miller AJ, Hirsch PR (2010) Are root exudates more important than other sources of rhizodeposits in structuring rhizosphere bacterial communities? FEMS Microbiol Ecol 72:313–327

    Article  CAS  PubMed  Google Scholar 

  • Fang DF, Wang B, Wang Y (2012) Effect of vegetation of transgenic Bt rice lines and their straw amendment on soil enzymes, respiration, functional diversity and community structure of soil microorganisms under field conditions. J Environ Sci 24:1259–1270

    Article  CAS  Google Scholar 

  • FAO (2014) FAOSTAT database 2014. https://faostat3faoorg/download/Q/QC/E Accessed 9 January 2016

  • 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 

  • Gschwendtner S, Engel M, Lueders T, Buegger F, Schloter M (2016) Nitrogen fertilization affects bacteria utilizing plant-derived carbon in the rhizosphere of beech seedlings. Plant Soil 407:203–215

    Article  CAS  Google Scholar 

  • Haichar FZ, Marol C, Berge O, Rangelcastro JI, Prosser JI, Balesdent J, Heulin T, Achouak W (2008) Plant host habitat and root exudates shape soil bacterial community structure. ISME J 2:1221–1230

    Article  CAS  PubMed  Google Scholar 

  • Han C, Zhong W, Shen W, Cai Z, Liu B (2013) Transgenic Bt rice has adverse impacts on CH4 flux and rhizospheric methanogenic archaeal and methanotrophic bacterial communities. Plant Soil 369:297–316

    Article  CAS  Google Scholar 

  • Hannula SE, Boer WD, Veen JAV (2014) Do genetic modifications in crops affect soil fungi? A review. Biol Fert Soils 50:433–446

    Article  CAS  Google Scholar 

  • Harris JK, Kelley ST, Pace NR (2004) New perspective on uncultured bacterial phylogenetic division OP11. Appl Environ Microb 70(2):845–849

    Article  CAS  Google Scholar 

  • Ishii S, Ikeda S, Minamisawa K, Senoo K (2010) Nitrogen cycling in rice paddy environments: past achievements and future challenges. Microbes Environ 26:282–292

    Article  Google Scholar 

  • Lee Z, Naishun B, Xueping C, Manqiu X, Feng W, Zhiping S, Changming F (2017) Effects of long-term cultivation of transgenic Bt rice (Kefeng-6) on soil microbial functioning and C cycling. Sci Rep-UK 7(1):4647

    Article  CAS  Google Scholar 

  • Li X, Zhang W, Liu T, Chen L, Chen P, Li F (2016) Changes in the composition and diversity of microbial communities during anaerobic nitrate reduction and Fe(II) oxidation at circumneutral pH in paddy soil. Soil Biol Biochem 94:70–79

    Article  CAS  Google Scholar 

  • Li YY, Chapman SJ, Nicol GW, Yao HY (2018a) Nitrification and nitrifiers in acidic soils. Soil Biol Biochem 116:290–301

    Article  CAS  Google Scholar 

  • Li Z, Naishun B, Xueping C, Manqiu X, Zhiping S, Ming N, Changming F (2018b) Soil incubation studies with Cry1Ac protein indicate no adverse effect of Bt crops on soil microbial communities. Ecotox Environ Safe 152:33

    Article  CAS  Google Scholar 

  • Liu W, Hao HL, Wu W, Qi KW, Ying XC, Thies JE (2008) Transgenic Bt rice does not affect enzyme activities and microbial composition in the rhizosphere during crop development. Soil Biol Biochem 40:475–486

    Article  CAS  Google Scholar 

  • Liu W, Wu W, Lu HH, Chen YX (2014) Carbon flux from decomposing 13C-labeled transgenic and nontransgenic parental rice straw in paddy soil. J Soils Sediments 14:1659–1668

    Article  CAS  Google Scholar 

  • Long XE, Yao H, Wang J, Huang Y, Singh BK, Zhu YG (2015) Community structure and soil pH determine chemoautotrophic carbon dioxide fixation in drained paddy soils. Environ Sci Technol 49:7152–7160

    Article  CAS  PubMed  Google Scholar 

  • Long XE, Huang Y, Chi HF, Li YY, Ahmad N, Yao HY (2018a) Nitrous oxide flux, ammonia oxidizer and denitrifier abundance and activity across three different landfill cover soils in Ningbo, China. J Clean Prod 170:288–2987

    Article  CAS  Google Scholar 

  • Long XE, Yao HY, Huang Y, Wei WX, Zhu YG (2018b) Phosphate levels influence the utilisation of rice rhizodeposition carbon and the phosphate-solubilising microbial community in a paddy soil. Soil Biol Biochem 118:103–114

    Article  CAS  Google Scholar 

  • Lu H, Wu W, Chen Y, Wang H, Devare M, Thies JE (2010) Soil microbial community responses to Bt transgenic rice residue decomposition in a paddy field. J Soils Sediments 10:1598–1605

    Article  Google Scholar 

  • Mahadevan R, Bond DR, Butler JE, Estevenuñez A, Coppi MV, Palsson BO, Schilling CH, Lovley DR (2006) Characterization of metabolism in the Fe(III)-reducing organism Geobacter sulfurreducens by constraint-based modeling. Appl Environ Microb 72:1558–1568

    Article  CAS  Google Scholar 

  • McIlroy SJ, Nielsen PH (2014) The family Saprospiraceae. Springer. Berlin Heidelberg. In The Prokaryotes – Other Major Lineages of Bacteria and the Archaea. Springer, Berlin Heidelberg, pp 863–889

    Google Scholar 

  • Peperanney C, Campbell AN, Koechli CN, Berthrong S, Buckley DH (2016) Unearthing the ecology of soil microorganisms using a high resolution DNA-SIP approach to explore cellulose and xylose metabolism in soil. Front Microbiol 7

  • Pinnell LJ, Dunford E, Ronan P, Hausner M, Neufeld JD (2014) Recovering glycoside hydrolase genes from active tundra cellulolytic bacteria. Can J Microbiol 60:469–476

    Article  CAS  PubMed  Google Scholar 

  • Qian HY, Pan JJ, Sun B (2013) The relative impact of land use and soil properties on sizes and turnover rates of soil organic carbon pools in subtropical China. Soil Use Manag 29(4):510–518

    Article  Google Scholar 

  • Rime T, Hartmann M, Stierli B, Anesio AM, Frey B (2016) Assimilation of microbial and plant carbon by active prokaryotic and fungal populations in glacial forefields. Soil Biol Biochem 98:30–41

    Article  CAS  Google Scholar 

  • Rocha UND (2010) Ecology of Acidobacteria and Verrucomicrobia in the plant-soil system. University of Groningen

  • Santana RH, Catão ECP, Lopes FAC, Constantino R, Barreto CC, Krüger RH (2015) The gut microbiota of workers of the litter-feeding termite Syntermes wheeleri (Termitidae: Syntermitinae): archaeal, bacterial, and fungal communities. Microb Ecol 70(2):545–556

    Article  PubMed  Google Scholar 

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

    Article  CAS  Google Scholar 

  • Shinji I (2001) Effect of organic fertilizer and effective microorganisms on growth, yield and quality of paddy-rice varieties. J Crop Prod 3:269–273

    Article  Google Scholar 

  • Sun M, Xiao T, Ning Z, Xiao E, Sun W (2015) Microbial community analysis in rice paddy soils irrigated by acid mine drainage contaminated water. Appl Microbiol Biot 99:2911–2922

    Article  CAS  Google Scholar 

  • Tate KR (2015) Soil methane oxidation and land-use change—from process to mitigation. Soil Biol Biochem 80:260–272

    Article  CAS  Google Scholar 

  • Tomoyuki H, Alexandra M, Yasuo I, Ralf C, W FM (2010) Identification of iron-reducing microorganisms in anoxic rice paddy soil by 13C-acetate probing. ISME J 4:267–278

  • Wang H, Ye Q, Wang W, Wu L, Wu W (2006) Cry1Ab protein from Bt transgenic rice does not residue in rhizosphere soil. Environ Pollut 143:449–455

    Article  CAS  PubMed  Google Scholar 

  • Wang H, Qingfu Y, Gan J, Wu L (2007) Biodegradation of Cry1Ab protein from Bt transgenic rice in aerobic and flooded paddy soils. J Agr Food Chem 55:1900–1904

    Article  CAS  Google Scholar 

  • Wang Y, Hu H, Huang J, Li J, Liu B, Zhang G (2013a) Determination of the movement and persistence of Cry1Ab/1Ac protein released from Bt transgenic rice under field and hydroponic conditions. Soil Biol Biochem 58:107–114

    Article  CAS  Google Scholar 

  • Wang Y, Huang J, Hu H, Li J, Liu B, Zhang G (2013b) Field and laboratory studies on the impact of two Bt rice lines expressing a fusion protein Cry1Ab/1Ac on aquatic organisms. Ecotox Environ Safe 92:87–93

    Article  CAS  Google Scholar 

  • Wang J, Chapman SJ, Yao H (2015) The effect of storage on microbial activity and bacterial community structure of drained and flooded paddy soil. J Soil Sediment 15:880–889

  • Wang J, Chapman SJ, Yao H (2016) Incorporation of 13C-labelled rice rhizodeposition into soil microbial communities under different fertilizer applications. Appl Soil Ecol 101:11–19

    Article  Google Scholar 

  • Wei M, Tan F, Zhu H, Cheng K, Wu X, Wang J, Zhao K, Tang X (2012) Impact of Bt-transgenic rice (SHK601) on soil ecosystems in the rhizosphere during crop development. Plant Soil Environ 58:217–223

    Article  CAS  Google Scholar 

  • Wu WX, Ye QF, Min H (2004) Effect of straws from Bt-transgenic rice on selected biological activities in water-flooded soil. Eur J Soil Biol 40:15–22

    Article  Google Scholar 

  • Wu WX, Liu W, Lu HH, Chen YX, Medha D, Janice T (2009) Use of 13C labeling to assess carbon partitioning in transgenic and nontransgenic (parental) rice and their rhizosphere soil microbial communities. FEMS Microbiol Ecol 67:93–102

    Article  CAS  PubMed  Google Scholar 

  • Yang CH, Crowley DE (2000) Rhizosphere microbial community structure in relation to root location and plant iron nutritional status. Appl Environ Microb 66:345–351

    Article  CAS  Google Scholar 

  • Yao H, Chapman SJ, Thornton B, Paterson E (2015) 13C PLFAs: a key to open the soil microbial black box? Plant Soil 392:3–15

    Article  CAS  Google Scholar 

  • Zhang X, Wang X, Tang Q, Li N, Liu P, Dong Y, Pang W, Yang J, Wang Z (2015) Effects of cultivation of OsrHSA transgenic rice on functional diversity of microbial communities in the soil rhizosphere. Crop J-China 3:163–167

    Article  Google Scholar 

  • Zhao X, Zhang Z, Yan J, Yu J (2007) GC content variability of eubacteria is governed by the pol III α subunit. Biochem Bioph Res Co 356:20–25

    Article  CAS  Google Scholar 

  • Zhu W, Lu H, Hill J, Guo X, Wang H, Wu W (2013) 13C pulse-chase labeling comparative assessment of the active methanogenic archaeal community composition in the transgenic and nontransgenic parental rice rhizospheres. FEMS Microb Ecol 87:746–756

    Article  CAS  Google Scholar 

Download references

Funding

This work was financially supported by the National Natural Science Foundation of China (Grant Nos. 41525002, 41701282 and 41761134085), the Strategic Priority Program of the Chinese Academy of Science (Grant No. XDB15020300), the National Ten-Thousand Talents Program of China (201829), and the Two-Hundred Talents Plan of Fujian Province, China (2018A12).

Author information

Authors and Affiliations

  1. Key Laboratory of Urban Environment and Health, Institute of Urban Environment, Chinese Academy of Sciences, Xiamen, China

    Juan Wang & Huaiying Yao

  2. Key Laboratory of Urban Environmental Processes and Pollution Control, Ningbo Urban Environment Observation and Research Station, Chinese Academy of Sciences, Ningbo, China

    Juan Wang & Huaiying Yao

  3. The James Hutton Institute, Craigiebuckler, Aberdeen, AB15 8QH, UK

    Stephen J. Chapman

  4. Institute of Nuclear Agricultural Sciences, Key Laboratory of Nuclear Agricultural Sciences of Ministry of Agriculture, Zhejiang University, Hangzhou, China

    Qingfu Ye

  5. Research Center for Environmental Ecology and Engineering, School of Environmental Ecology and Biological Engineering, Wuhan Institute of Technology, Wuhan, China

    Huaiying Yao

Authors
  1. Juan Wang
    View author publications

    You can also search for this author in PubMed Google Scholar

  2. Stephen J. Chapman
    View author publications

    You can also search for this author in PubMed Google Scholar

  3. Qingfu Ye
    View author publications

    You can also search for this author in PubMed Google Scholar

  4. Huaiying Yao
    View author publications

    You can also search for this author in PubMed Google Scholar

Corresponding author

Correspondence to Huaiying Yao.

Ethics declarations

This article does not contain any studies with human participants or animals performed by any of the authors.

Conflict of interest

The authors declare that they have no conflict of interest.

Additional information

Publisher’s note

Springer Nature remains neutral with regard to jurisdictional claims in published maps and institutional affiliations.

Electronic supplementary material

ESM 1

(PDF 497 kb)

Rights and permissions

Reprints and Permissions

About this article

Verify currency and authenticity via CrossMark

Cite this article

Wang, J., Chapman, S.J., Ye, Q. et al. Limited effect of planting transgenic rice on the soil microbiome studied by continuous 13CO2 labeling combined with high-throughput sequencing. Appl Microbiol Biotechnol 103, 4217–4227 (2019). https://doi.org/10.1007/s00253-019-09751-w

Download citation

  • Received:

  • Revised:

  • Accepted:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1007/s00253-019-09751-w

Keywords

  • Transgenic rice
  • Continuous labeling
  • DNA-SIP
  • High-throughput sequencing