High-throughput sequencing analysis of microbial community diversity in response to indica and japonica bar-transgenic rice paddy soils


Autoři: Meidan He aff001;  Jiachao Zhang aff002;  Linbo Shen aff003;  Lixin Xu aff001;  Wenjie Luo aff001;  Dong Li aff001;  Nanxin Zhai aff001;  Jianfa Zhao aff001;  Yan Long aff004;  Xinwu Pei aff004;  Qianhua Yuan aff001
Působiště autorů: Hainan Key Laboratory for Sustainable Utilization of Tropical Bio-resources, Institute of Tropical Agriculture and Forestry, Hainan University, Haikou, China aff001;  College of Food Science and Technology, Hainan University, Haikou, China aff002;  Institute of Tropical Bioscience and Biotechnology, Chinese Academy of Tropical Agriculture, Haikou, China aff003;  Ministry of Agriculture Key Laboratory on Safety Assessment (Molecular) of Agriculture Genetically Modified Organisms, Biotechnology Research Institute, Chinese Academy of Agriculture Sciences, Beijing, China aff004
Vyšlo v časopise: PLoS ONE 14(9)
Kategorie: Research Article
doi: https://doi.org/10.1371/journal.pone.0222191

Souhrn

Potential environmental risks of genetically modified (GM) crops have raised concerns. To better understand the effect of transgenic rice on the bacterial community in paddy soil, a field experiment was carried out using pairs of rice varieties from two subspecies (indica and japonica) containing bar transgene with herbicide resistance and their parental conventional rice. The 16S rRNA gene of soil genomic DNA from different soil layers at the maturity stage was sequenced using high-throughput sequencing on the Illumina MiSeq platform to explore the microbial community diversity among different rice soils. There were no significant differences in diversity indices between transgenic japonica rice and its sister conventional rice (japonica pair) among different soil layers, but, significant differences was observed between transgenic indica rice and its conventional rice (indica pair) in the topsoil layer around concentrated rice roots according to the ace diversity index. Though the japonica rice soil and indica rice soil were shared several key genera, including Rivibacter, Anaeromyxobacter, Roseomonas, Geobacter, Thiobacillus, Clostridium, and Desulfobulbus, the primary bacterial genera in indica rice soil were different from those in japonica rice. Synechococcus and Dechloromonas were present in japonica rice samples, while Chloronema, Flexibacter, and Blastocatella were observed in indica rice soil. Moreover, the abundance of genera between GM and non-GM varieties in japonica rice was significantly different from indica rice, and several bacterial communities influenced these differences. Anaerovorax was more abundant in transgenic japonica rice soil than conventional rice soil, while it was deficient in transgenic indica rice soil compared to conventional rice soil, and opposite responses to Deferrisoma were in that of indica rice. Thus, we concluded that transgenic indica and japonica rice had different effects on soil bacteria compared with their corresponding sister conventional rice. However, these composition and abundance difference only occurred for a few genera but had no effect on the primary genera and soil characteristics were mainly contributed to these differences. Thus, differences in bacterial community structure can be ignored when evaluating the impacts of transgenic rice in the complex soil microenvironment.

Klíčová slova:

Biology and life sciences – Organisms – Eukaryota – Plants – Grasses – Rice – Genetically modified plants – Genetically modified crops – Bacteria – Bioengineering – Biotechnology – Genetic engineering – Genetically modified organisms – Plant biotechnology – Plant science – Plant ecology – Plant-environment interactions – Rhizosphere – Agriculture – Agricultural soil science – Ecology – Community ecology – Community structure – Research and analysis methods – Animal studies – Experimental organism systems – Plant and algal models – Engineering and technology – Ecology and environmental sciences – Soil science – Soil ecology


Zdroje

1. James C. Global Status of Commercialized Biotech/GM Crops in 2017:Biotech Crop Adoption Surges as Economic Benefits Accumulate in 22 Years: ISAAA; 2018 [cited 2018 Sep 22]. Available from: http://www.isaaa.org/resources/publications/annualreport/2017/default.asp.

2. Brookes G, Barfoot P. Economic impact of GM crops: The global income and production effects 1996–2012. Gm Crops & Food. 2014;5(1):65–75. doi: 10.4161/gmcr.28098 24637520

3. Lu BR, Yang X, Ellstrand NC. Fitness correlates of crop transgene flow into weedy populations: a case study of weedy rice in China and other examples. Evol Appl. 2016;9(7):857–70. doi: 10.1111/eva.12377 27468304

4. Mao J, Sun X, Cheng JH, Shi YJ, Wang XZ, Qin JJ, et al. A 52-week safety study in cynomolgus macaques for genetically modified rice expressing Cry1Ab/1Ac protein. Food Chem Toxicol. 2016;95:1–11. doi: 10.1016/j.fct.2016.06.015 27338709

5. Domingo JL. Safety assessment of GM plants: An updated review of the scientific literature. Food Chem Toxicol. 2016;95:12–8. doi: 10.1016/j.fct.2016.06.013 27317828

6. Tothova T, Sobekova A, Holovska K, Legath J, Pristas P, Javorsky P. Natural glufosinate resistance of soil microorganisms and GMO safety. Cent Eur J Biol. 2010;5(5):656–63. doi: 10.2478/s11535-010-0042-0

7. Katie Eastham JS. Genetically modified organisms (GMOs): The significance of gene flow through pollen transfer. Environmental issue report: the European Science Foundation and the European Environment Agency, 2002 28.

8. Tsatsakis AM, Nawaz MA, Tutelyan VA, Golokhvast KS, Kalantzi O-I, Chung DH, et al. Impact on environment, ecosystem, diversity and health from culturing and using GMOs as feed and food. Food Chem Toxicol. 2017. doi: 10.1016/j.fct.2017.06.033 28645870

9. Chun YJ, Kim HJ, Park KW, Jeong SC, Lee B, Back K, et al. Two-year field study shows little evidence that PPO-transgenic rice affects the structure of soil microbial communities. Biol Fertil Soils. 2012;48(4):453–61. doi: 10.1007/s00374-011-0626-5

10. Heuer H, Kroppenstedt RM, Lottmann J, Berg G, Smalla K. Effects of T4 lysozyme release from transgenic potato roots on bacterial rhizosphere communities are negligible relative to natural factors. Appl Environ Microbiol. 2002;68(3):1325–35. doi: 10.1128/AEM.68.3.1325-1335.2002 11872484

11. Oliveira AP, Pampulha ME, Bennett JP. A two-year field study with transgenic Bacillus thuringiensis maize: effects on soil microorganisms. Sci Total Environ. 2008;405(1–3):351–7. Epub 2008/07/29. doi: 10.1016/j.scitotenv.2008.05.046 18656246

12. Wu WX, Liu W, Lu HH, Chen YX, Medha D, Janice T. Use of 13C labeling to assess carbon partitioning in transgenic and nontransgenic (parental) rice and their rhizosphere soil microbial communities. FEMS Microbiol Ecol. 2009;67(1):93–102. Epub 2008/12/04. doi: 10.1111/j.1574-6941.2008.00599.x 19049503

13. Yang B, Chen H, Liu X, Ge F, Chen Q. Bt cotton planting does not affect the community characteristics of rhizosphere soil nematodes. Applied Soil Ecology. 2014;73:156–64. doi: 10.1016/j.apsoil.2013.09.001

14. Zhang YJ, Xie M, Wu G, Peng DL, Yu WB. A 3-year field investigation of impacts of Monsanto’s transgenic Bt-cotton NC 33B on rhizosphere microbial communities in northern China. Applied Soil Ecology. 2015;89:18–24. doi: 10.1016/j.apsoil.2015.01.003

15. Dohrmann AB, Küting M, Jünemann S, Jaenicke S, Schlüter A, Tebbe CC. Importance of rare taxa for bacterial diversity in the rhizosphere of Bt- and conventional maize varieties. Isme Journal. 2013;7(1):37. doi: 10.1038/ismej.2012.77 22791236

16. Sohn SI, Oh YJ, Kim BY, Cho HS. Effects of CaMSRB2-Expressing Transgenic Rice Cultivation on Soil Microbial Communities. J Microbiol Biotechnol. 2016;26(7):1303–10. Epub 2016/04/20. doi: 10.4014/jmb.1601.01058 27090184

17. Sahoo RK, Ansari MW, Tuteja R, Tuteja N. Salt tolerant SUV3 overexpressing transgenic rice plants conserve physicochemical properties and microbial communities of rhizosphere. Chemosphere. 2015;119:1040–7. doi: 10.1016/j.chemosphere.2014.08.011 25303666

18. Li P, Dong J, Yang S, Bai L, Wang J, Wu G, et al. Impact of β-carotene transgenic rice with four synthetic genes on rhizosphere enzyme activities and bacterial communities at different growth stages. Eur J Soil Biol. 2014;65:40–6. doi: 10.1016/j.ejsobi.2014.09.002

19. Li P, Ye S, Liu H, Pan A, Ming F, Tang X. Cultivation of Drought-Tolerant and Insect-Resistant Rice Affects Soil Bacterial, but Not Fungal, Abundances and Community Structures. Front Microbiol [Internet]. 2018; 9:[1390 p.]. doi: 10.3389/fmicb.2018.01390 30008701

20. Dunfield KE, Germida JJ. Impact of genetically modified crops on soil- and plant-associated microbial communities. Journal of environmental quality. 2004;33(3):806–15. doi: 10.2134/jeq2004.0806 15224914

21. Andreote FD, Mendes R, Dini-Andreote F, Rossetto PB, Labate CA, Pizzirani-Kleiner AA, et al. Transgenic tobacco revealing altered bacterial diversity in the rhizosphere during early plant development. Antonie Van Leeuwenhoek. 2008;93(4):415–24. doi: 10.1007/s10482-007-9219-6 18181027

22. Zhu W, Lu H, Hill J, Guo X, Wang H, Wu W. (1)(3)C pulse-chase labeling comparative assessment of the active methanogenic archaeal community composition in the transgenic and nontransgenic parental rice rhizospheres. FEMS Microbiol Ecol. 2014;87(3):746–56. Epub 2013/11/26. doi: 10.1111/1574-6941.12261 24266498

23. Doornbos R, van Loon L, Bakker PHM. Impact of root exudates and plant defense signaling on bacterial communities in the rhizosphere. A review. Agronomy for Sustainable Development. 2012;32(1):227–43. doi: 10.1007/s13593-011-0028-y

24. Duke SO. Taking stock of herbicide-resistant crops ten years after introduction. Pest Manage Sci. 2010;61(3):211–8. doi: 10.1002/ps.1024 15660452

25. Christ B, Weng JK, Guyer L, Hochstrasser R, Francisco R, Hörtensteiner S, et al. Non-specific activities of the major herbicide-resistance gene BAR. Nature Plants. 2017;3(12). doi: 10.1038/s41477-017-0061-1 29180815

26. White J, Chang SY, Bibb MJ, Bibb MJ. A cassette containing the bar gene of Streptomyces hygroscopicus: a selectable marker for plant transformation. Nucleic Acids Res. 1990;18(4):1062. doi: 10.1093/nar/18.4.1062 2315036

27. Wu JR, Yu MZ, Xu JH, Du J, Ji F, Dong F, et al. Impact of Transgenic Wheat with wheat yellow mosaic virus Resistance on Microbial Community Diversity and Enzyme Activity in Rhizosphere Soil. Plos One. 2014;9(6). doi: 10.1371/journal.pone.0098394 24897124

28. Liu W, Hao Lu H, Wu W, Kun Wei Q, Xu Chen Y, Thies JE. Transgenic Bt rice does not affect enzyme activities and microbial composition in the rhizosphere during crop development. Soil Biol Biochem. 2008;40(2):475–86. doi: 10.1016/j.soilbio.2007.09.017

29. Song YN, Su J, Chen R, Lin Y, Wang F. Diversity of Microbial Community in a Paddy Soil with cry1Ac/cpti Transgenic Rice. Pedosphere. 2014;24(3):349–58. doi: 10.1016/S1002-0160(14)60021-7

30. Jia S, Wang F, Shi L, Yuan Q, Liu W, Liao Y, et al. Transgene flow to hybrid rice and its male-sterile lines. Transgenic Res. 2007;16(4):491–501. doi: 10.1007/s11248-006-9037-z 17443417

31. Yuan QH, Shi L, Wang F, Cao B, Qian Q, Lei XM, et al. Investigation of rice transgene flow in compass sectors by using male sterile line as a pollen detector. Theoretical & Applied Genetics. 2007;115(4):549–60. doi: 10.1007/s00122-007-0588-z 17622509

32. Xiao G, Yuan L, Sun SSM. Strategy and utilization of a herbicide resistance gene in two-line hybrid rice. Mol Breed. 2007;20(3):287–92. doi: 10.1007/s11032-007-9091-0

33. Edwards A. H. The semi-micro Kjeldahl method for the determination of nitrogen in coal. Journal of Chemical Technology & Biotechnology Biotechnology. 2010;4(6):330–40. doi: 10.1002/jctb.5010040610

34. Dennis KL, Wang Y, Blatner NR, Wang S, Saadalla A, Trudeau E, et al. Adenomatous Polyps Are Driven by Microbe-Instigated Focal Inflammation and Are Controlled by IL-10–Producing T Cells. Cancer Res. 2013;73(19):5905–13. doi: 10.1158/0008-5472.CAN-13-1511 23955389

35. Xu N, Tan G, Wang H, Gai X. Effect of biochar additions to soil on nitrogen leaching, microbial biomass and bacterial community structure. Eur J Soil Biol. 2016;74:1–8. doi: 10.1016/j.ejsobi.2016.02.004

36. Edgar RC. UPARSE: highly accurate OTU sequences from microbial amplicon reads. Nat Methods. 2013;10(10):996–8. Epub 2013/08/21. doi: 10.1038/nmeth.2604 23955772

37. Schloss PD, Gevers D, Westcott SL. Reducing the Effects of PCR Amplification and Sequencing Artifacts on 16S rRNA-Based Studies. PLoS One. 2011;6(12):e27310. doi: 10.1371/journal.pone.0027310 22194782

38. Lozupone C, Knight R. UniFrac: a New Phylogenetic Method for Comparing Microbial Communities. Appl Environ Microbiol.2006;71(12): 8228–35. doi: 10.1128/AEM.71.12.8228–8235.2005

39. Hong C, Si Y, Xing Y, Li Y. Illumina MiSeq sequencing investigation on the contrasting soil bacterial community structures in different iron mining areas. Environ Sci Pollut Res Int. 2015;22(14):10788–99. doi: 10.1007/s11356-015-4186-3 25761991

40. Clergue B, Amiaud B, Pervanchon F, Lasserrejoulin F, Plantureux S. Biodiversity: Function and Assessment in Agricultural Areas: A Review. Agronomie. 2005;25(1):6119–25. doi: 10.1007/978-90-481-2666-8_21

41. Gurr GM, Wratten SD, Luna JM. Multi-function agricultural biodiversity: pest management and other benefits. Basic Appl Ecol. 2003;4(2):107–16. doi: 10.1078/1439-1791-00122

42. Angle JS. Release of transgenic plants: biodiversity and population-level considerations. Mol Ecol. 1994;3(1):45–50. doi: 10.1111/j.1365-294x.1994.tb00042.x

43. Dunfield KE, Germida JJ. Impact of genetically modified crops on soil- and plant-associated microbial communities. J Environ Qual. 2004;33(3):806–15. Epub 2004/07/01. doi: 10.2134/jeq2004.0806 15224914

44. Arias-Martín M, García M, Luciáñez MJ, Ortego F, Castañera P, Farinós GP. Effects of three-year cultivation of Cry1Ab-expressing Bt maize on soil microarthropod communities. Agric, Ecosyst Environ. 2016;220:125–34. doi: 10.1016/j.agee.2015.09.007

45. Zhou D, Xu L, Gao S, Guo J, Luo J, You Q, et al. Cry1Ac Transgenic Sugarcane Does Not Affect the Diversity of Microbial Communities and Has No Significant Effect on Enzyme Activities in Rhizosphere Soil within One Crop Season. Frontiers in plant science. 2016;7(265). doi: 10.3389/fpls.2016.00265 27014291

46. Han C, Liu B, Zhong W. Effects of transgenic Bt rice on the active rhizospheric methanogenic archaeal community as revealed by DNA-based stable isotope probing. J Appl Microbiol. 2018. Epub 2018/05/31. doi: 10.1111/jam.13939 29846995

47. Song L, Zhao DG, Jin DC. Impact of T8 Transgenic Rice Containing an Isopentenyl Transferase Gene on Soil Bacterial Biomass. Advanced Materials Research. 2012;455–456:1404–9. doi: 10.4028/www.scientific.net/AMR.455-456.1404

48. Khan MS, Sadat SU, Jan A, Munir I. Impact of TransgenicBrassica napusHarboring the Antifungal Synthetic Chitinase (NiC) Gene on Rhizosphere Microbial Diversity and Enzyme Activities. Frontiers in plant science. 2017;8:1307. doi: 10.3389/fpls.2017.01307 28791039

49. Mocali S, Dentice A, Marcucci A, Benedetti A. The impact of post-harvest treatments of transgenic eggplant residues on soil quality and microbial diversity. Ultrasound Med Biol. 2009;53(5):296–307.

50. George TS, Richardson AE, Li SS, Gregory PJ, Daniell TJ. Extracellular release of a heterologous phytase from roots of transgenic plants: does manipulation of rhizosphere biochemistry impact microbial community structure? FEMS Microbiol Ecol. 2009;70(3):433–45. Epub 2009/09/12. doi: 10.1111/j.1574-6941.2009.00762.x 19744239

51. Lu GH, Tang CY, Hua XM, Cheng J, Wang GH, Zhu YL, et al. Effects of an EPSPS-transgenic soybean line ZUTS31 on root-associated bacterial communities during field growth. PLoS One. 2018;13(2):25. doi: 10.1371/journal.pone.0192008 29408918

52. Schmalenberger A, Tebbe CC. Bacterial community composition in the rhizosphere of a transgenic, herbicide-resistant maize (Zea mays) and comparison to its non-transgenic cultivar Bosphore. FEMS Microbiol Ecol. 2002;40(1):29–37. doi: 10.1111/j.1574-6941.2002.tb00933.x 19709208

53. Sohn SI, Oh YJ, Ahn BO, Ryu TH, Cho HS, Park JS, et al. Soil Microbial Community Assessment for the Rhizosphere Soil of Herbicide Resistant Genetically Modified Chinese Cabbage. Korean Journal of Environmental Agriculture. 2012;31(1):52–9. doi: 10.5338/KJEA.2012.31.1.52

54. Sohn SI, Kwon JS, Woen HY, Noh HJ, Kim KH, Baek HJ, et al. Assessment of Microbial Community in the Rhizoplane and Rhizosphere Soil of Herbicide-Resistant Transgenic Perilla. Journal of the Korean Society of International Agriculture. 2009. doi: 10.12719/KSIA.2016.28.4.443

55. Rousk J, Brookes PC, Bååth E. The microbial PLFA composition as affected by pH in an arable soil. Soil Biol Biochem. 2010;42(3):516–20. doi: 10.1016/j.soilbio.2009.11.026

56. Noah F, Jackson RB. The diversity and biogeography of soil bacterial communities. Proc Natl Acad Sci U S A. 2006;103(3):626–31. doi: 10.1073/pnas.0507535103 16407148

57. Trungchanh T, MichioTsutsumi, KinkichiKurihara. Comparative study on the response of Indica and Japonica rice plants to ammonium and nitrate nitrogen. Soil Sci Plant Nutr. 1981;27(1):83–92. doi: 10.1080/00380768.1981.10431257

58. Zhang J, Liu Y-X, Zhang N, Hu B, Jin T, Xu H, et al. NRT1.1B is associated with root microbiota composition and nitrogen use in field-grown rice. Nat Biotechnol. 2019;37(6):676–84. doi: 10.1038/s41587-019-0104-4 31036930

59. Hazen TC, editor Field-Integrated Studies of Long-Term Sustainability of Chromium Bioreduction at Hanford 100H Site. AGU Fall Meeting; 2006.

60. Wu Q, Knowles R, Niven DF. O2 regulation of denitrification in Flexibacter canadensis. Can J Microbiol. 1994;40(40):916–21. doi: 10.1139/m94-147

61. Lucas JA, Garcíavillaraco A, Ramos B, Garcíacristobal J, Algar E, Gutierrezmañero J. Structural and functional study in the rhizosphere of Oryza sativa L. plants growing under biotic and abiotic stress. J Appl Microbiol. 2013;115(1):218–35. doi: 10.1111/jam.12225 23594253

62. Tripathi BM, Kim M, Laihoe A, Shukor NA, Rahim RA, Go R, et al. pH dominates variation in tropical soil archaeal diversity and community structure. FEMS Microbiol Ecol. 2013;86(2):303–11. doi: 10.1111/1574-6941.12163 23773164

63. Long XE, Yao H, Wang J, Huang Y, Singh BK, Zhu YG. Community structure and soil pH determine chemoautotrophic carbon dioxide fixation in drained paddy soils. Environ Sci Technol. 2015;49(12):7152–60. doi: 10.1021/acs.est.5b00506 25989872

64. Duan G-L, Ding L-J, Cui H-L, Zhu Y-G, Nie S-A, Long X-E. Microbiomes inhabiting rice roots and rhizosphere. 2019. doi: 10.1093/femsec/fiz040

65. Mendes R, Garbeva P, Raaijmakers JM. The rhizosphere microbiome: significance of plant beneficial, plant pathogenic, and human pathogenic microorganisms. FEMS Microbiol Rev. 2013;37(5):634–63. doi: 10.1111/1574-6976.12028 23790204


Článek vyšel v časopise

PLOS One


2019 Číslo 9
Nejčtenější tento týden