DOI QR코드

DOI QR Code

Relative Effect of Glyphosate on Glyphosate-Tolerant Maize Rhizobacterial Communities is Not Altered by Soil Properties

  • Barriuso, Jorge (Centro Nacional de Biotecnologia (CSIC), c/ Darwin 3, Campus de la Universidad Autonoma) ;
  • Mellado, Rafael P. (Centro Nacional de Biotecnologia (CSIC), c/ Darwin 3, Campus de la Universidad Autonoma)
  • Received : 2011.07.18
  • Accepted : 2011.10.11
  • Published : 2012.02.28

Abstract

The rhizobacterial composition varies according to the soil properties. To test if the effect of herbicides on the rhizobacterial communities of genetically modified NK603 glyphosate-tolerant maize varies according to different soil locations, a comparison was made between the effects of glyphosate (Roundup Plus), a post-emergence applied herbicide, and a pre-emergence applied herbicide (GTZ) versus untreated soil. The potential effect was monitored by direct amplification, cloning, and sequencing of the soil DNA encoding 16S rRNA, and high-throughput DNA pyrosequencing of the bacterial DNA coding for the 16S rRNA hypervariable V6 region. The results obtained using three different methods to analyze the herbicide effect on the rhizobacterial communities of genetically modified NK603 maize were comparable to those previously obtained when glyphosate-tolerant maize was grown in soil with different characteristics. Both herbicides decreased the bacterial diversity in the rhizosphere, with Actinobacteria being the taxonomic group most affected. The results suggest that both herbicides affected the structure of the maize rhizobacterial community, but glyphosate was environmentally less aggressive.

Keywords

References

  1. Acosta-Martinez, V., S. E. Dowb, Y. Sun, D. Wester, and V. Allen. 2010. Pyrosequencing analysis for characterization of soil bacterial populations as affected by an integrated livestockcotton production system. Appl. Soil Ecol. 45: 3-25.
  2. Altschul, S. F., T. L. Madden, A. A. Schaffer, J. Zhang, Z. Zhang, W. Miller, and D. J. Lipman. 1997. Gapped BLAST and PSI-BLAST: A new generation of protein database search programs. Nucleic Acids Res. 25: 3389-3402. https://doi.org/10.1093/nar/25.17.3389
  3. Amann, R. I., W. Ludwig, and K. H. Schleifer. 1995. Phylogenetic identification and in situ detection of individual microbial cells without cultivation. Microbiol. Rev. 59: 143-169.
  4. Barriuso, J., S. Marin, and R. P. Mellado. 2010. Effect of the herbicide glyphosate on glyphosate-tolerant maize rhizobacterial communities: A comparison with pre-emergency applied herbicide consisting of a combination of acetochlor and terbuthylazine. Environ. Microbiol. 12: 1021-1030. https://doi.org/10.1111/j.1462-2920.2009.02146.x
  5. Descalzo, R. C., Z. K. Punja, C. A. Levesque, and J. E. Rahe. 1998. Glyphosate treatment of bean seedlings causes short-term increases in Pythium populations and damping off potential in soils. Appl. Soil Ecol. 8: 25-33. https://doi.org/10.1016/S0929-1393(97)00069-3
  6. Edgar, R. C. 2004. MUSCLE: Multiple sequence alignment with high accuracy and high throughput. Nucleic Acids Res. 32: 1792-1797. https://doi.org/10.1093/nar/gkh340
  7. Fang, M., R. J. Kremere, P. P. Motavalli, and G. Davis. 2005. Bacterial diversity in rhizospheres of nontransgenic and transgenic corn. Appl. Environ. Microbiol. 71: 4132-4136. https://doi.org/10.1128/AEM.71.7.4132-4136.2005
  8. Gans, J., M. Woilinsky, and J. Dunbar. 2005. Computational improvement reveal great bacterial diversity and high metal toxicity in soil. Science 309: 1387-1390. https://doi.org/10.1126/science.1112665
  9. Gimsing, A. L., O. K. Borggaard, O. S. Jacobsen, J. Aamand, and J. Sørensen. 2004. Chemical and microbiological soil characteristics controlling glyphosate mineralization in Danish surface soils. Appl. Soil Ecol. 27: 233-242. https://doi.org/10.1016/j.apsoil.2004.05.007
  10. Hamady, M., C. Lozupone, and R. Knight. 2010. Fast UniFrac: Facilitating high-throughput phylogenetic analyses of microbial communities including analysis of pyrosequencing and PhyloChip data. ISME J. 4: 17-27. https://doi.org/10.1038/ismej.2009.97
  11. Heck, G. R., C. L. Armstrong, J. D. Astwood, C. F. Behr, J. T. Bookout, S. M. Brown, et al. 2005. Development and characterisation of a CP4 EPSPS-based, glyphosate-tolerant corn event NK603. Crop Sci. 45: 329-339. https://doi.org/10.2135/cropsci2005.0329
  12. Hodgson, D. A. 2000. Primary metabolism and its control in streptomycetes: A most unusual group of bacteria. Adv. Microb. Physiol. 42: 47-238.
  13. Huse, S. M., J. A. Huber, H. G. Morrison, M. L. Sogin, and D. M. Welch. 2007. Accuracy and quality of massively parallel DNA pyrosequencing. Genome Biol. 8: R143. https://doi.org/10.1186/gb-2007-8-7-r143
  14. Huse, S. M., D. M. Welch, H. G. Morrison, and M. L. Sogin. 2010. Ironing out the wrinkles in the rare biosphere through improved OUT clustering. Environ. Microbiol. 12: 1889-1898. https://doi.org/10.1111/j.1462-2920.2010.02193.x
  15. Huson, D. H., D. C. Richter, S. Mitra, A. F. Auch, and S. C. Schuster. 2009. Methods for comparative metagenomics. BMC Bioinformatics 10: S12.
  16. Jangid, K., M. A. Williams, A. J. Franzluebbers, J. S. Sanderlin, J. H. Reeves, M. B. Jenkins, et al. 2008. Relative impacts of land-use, management intensity and fertilization upon soil microbial community structure in agricultural systems. Soil Biol. Biochem. 40: 2843-2853. https://doi.org/10.1016/j.soilbio.2008.07.030
  17. Kielak, A. M., J. A. van Veen, and G. A. Kowalchuk. 2010. Comparative analysis of acidobacterial genomic fragments from terrestrial and aquatic metagenomic libraries, with emphasis on acidobacteria subdivision 6. Appl. Environ. Microbiol. 76: 6769-6777. https://doi.org/10.1128/AEM.00343-10
  18. Kremer, R. J. and N. E. Means. 2009. Glyphosate and glyphosateresistant crop interactions with rhizosphere microorganisms, Eur. J. Agron. 31: 153-161. https://doi.org/10.1016/j.eja.2009.06.004
  19. Kremer, R. J., N. E. Means, and S. J. Kim. 2005. Glyphosate affects soybean root exudation and rhizosphere microorganisms. Int. J. Environ. Anal. Chem. 85: 1165-1174. https://doi.org/10.1080/03067310500273146
  20. Levesque, C. A. and J. E. Rahe. 1992. Herbicide interactions with fungal root pathogens, with special reference to glyphosate. Annu. Rev. Phytopathol. 30: 597-602.
  21. Liu, C. M., P. A. McLean, C. C. Sookdeo, and F. C. Cannon. 1991. Degradation of the herbicide glyphosate by members of the family Rhizobiaceae. Appl. Environ. Microbiol. 57: 1799- 1804.
  22. Locke, M. A., R. M. Zablotowicz, and K. N. Reddy. 2008. Integrating soil conservation practices and glyphosate-resistant crops: Impact on soil. Pest. Manag. Sci. 64: 457-469. https://doi.org/10.1002/ps.1549
  23. Ludwig, W., O. Strunk, R. Westram, L. Richter, H. Meier, Yadhukumar, et al. 2004. ARB: A software environment for sequence data. Nucleic Acids Res. 32: 1363-1371. https://doi.org/10.1093/nar/gkh293
  24. Margulies, M., M. Egholm, W. E. Altman, S. Attiya, J. S. Bader, L. A. Bemben, et al. 2005. Genome sequencing in microfabricated high-density picolitre reactors. Nature 437: 376-380. https://doi.org/10.1038/nature03959
  25. Mijangos, M., J. M. Becerril, I. Albizu, L. Epelde, and C. Garbisu. 2009. Effects of glyphosate on rhizosphere soil microbial communities under two different plant compositions by cultivationdependent and -independent methodologies. Soil Biol. Biochem. 41: 505-513. https://doi.org/10.1016/j.soilbio.2008.12.009
  26. Roesch, L. F. W., R. R. Fulthorpe, A. Riva, G. Casella, A. K. M. Hadwin, A. D. Kent, et al. 2007. Pyrosequencing enumerates and contrast soil microbial diversity. ISME J. 1: 283-290. https://doi.org/10.1038/ismej.2007.53
  27. Schloss, P. D. 2010. The effects of alignment quality, distance calculation method, sequence filtering, and region on the analysis of 16S rRNA gene-based studies. PLoS Comput. Biol. 6: e1000844. https://doi.org/10.1371/journal.pcbi.1000844
  28. Schloss, P. D. and J. Handelsman. 2005. Introducing DOTUR, a computer program for defining operational taxonomic units and estimating species richness. Appl. Environ. Microbiol. 71: 1501-1506. https://doi.org/10.1128/AEM.71.3.1501-1506.2005
  29. Sidhu, R. S., B. G. Hammond, R. L. Fuchs, J. Mutz, L. R. Holden, B. George, and T. Olson. 2000. Glyphosphate-tolerant corn: The composition and feeding value of grain from glyphosphatetolerant corn is equivalent to that of conventional corn (Zea mays L.). J. Agric. Food Chem. 48: 2305-2312. https://doi.org/10.1021/jf000172f
  30. Sluszny, C., E. R. Graber, and Z. Gerstl. 1999. Sorption of striazine herbicides in organic matter amended soils: Fresh and incubated systems. Water Air Soil Poll. 115: 395-410. https://doi.org/10.1023/A:1005105020757
  31. Sogin, M. L., H. G. Morison, J. L. Huber, D. Welch, S. M. Huse, P. R. Neal, et al. 2006. Microbial diversity in the deep sea and the unexplored "rare biosphere". Proc. Natl. Acad. Sci. USA 103: 12115-12120. https://doi.org/10.1073/pnas.0605127103
  32. Sun, Y., Y. Cai, L. Liu, F. Yu, M. L. Farrell, W. McKendree, and W. Farmerie. 2009. ESPRIT: Estimating species richness using large collections of 16S rRNA pyrosequences. Nucleic Acids Res. 37: e76. https://doi.org/10.1093/nar/gkp285
  33. Thompson, J. D., T. J. Gibson, F. Plewniak, F. Jeanmougin, and D. G. Higgins. 1997. The CLUSTAL_X Windows interface: Flexible strategies for multiple sequence alignment aided by quality analysis tools. Nucleic Acids Res. 25: 4876-4882. https://doi.org/10.1093/nar/25.24.4876
  34. Val, G., S. Marin, and R. P. Mellado. 2009. A sensitive method to monitor Bacillus subtilis and Streptomyces coelicolor-related bacteria in maize rhizobacterial communities: The use of genome-wide microarrays. Microbial Ecol. 58: 108-115. https://doi.org/10.1007/s00248-008-9451-2
  35. Weaver, M. A., L. J. Krutz, R. M. Zablotowicz, and K. N. Reddy. 2007. Effects of glyphosate on soil microbial communities and its mineralization in a Mississippi soil. Pest Manag. Sci. 63: 388-393. https://doi.org/10.1002/ps.1351

Cited by

  1. Effect of Herbicide Combinations on Bt-Maize Rhizobacterial Diversity vol.24, pp.11, 2014, https://doi.org/10.4014/jmb.1405.05054
  2. Looking for Rhizobacterial Ecological Indicators in Agricultural Soils Using 16S rRNA metagenomic Amplicon Data vol.11, pp.10, 2012, https://doi.org/10.1371/journal.pone.0165204
  3. The effects of glyphosate, glufosinate, paraquat and paraquat-diquat on soil microbial activity and bacterial, archaeal and nematode diversity vol.8, pp.None, 2018, https://doi.org/10.1038/s41598-018-20589-6
  4. Effects of a glyphosate-based herbicide on soil animal trophic groups and associated ecosystem functioning in a northern agricultural field vol.9, pp.None, 2012, https://doi.org/10.1038/s41598-019-44988-5
  5. Soil pH, nitrogen, phosphatase and urease activities in response to cover crop species, termination stage and termination method vol.7, pp.1, 2012, https://doi.org/10.1016/j.heliyon.2021.e05980