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The Impact of Pesticides on the Microbial Community of Agrosoddy-Podzolic Soil

  • DEGRADATION, REHABILITATION, AND CONSERVATION OF SOILS
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Abstract

The impact of three types of pesticides (herbicide metribuzin, insecticide imidacloprid, and fungicide benomyl) on the structure of microbial complexes and indicators of biological activity of agrosoddy-podzolic soil (Moscow oblast) has been assessed using the method of next-generation sequencing (NGS). The pesticides have been applied both separately and together at one- and tenfold rates. It has been found that pesticides have a greater impact on the fungal community in comparison with the prokaryotic community; in the latter, only changes in the abundances of the phyla of Actinobacteria and Proteobacteria have been observed. The study of fungal communities with the use of molecular-genetic analysis has revealed two dominant divisions of fungi in all soil samples: Ascomycota (72.6 ± 8.0%) and Basidiomycota (26.0 ± 7.7%). Moreover, in the samples treated with tenfold rate of pesticides (both in mixture and separately), the abundances of representatives of the Basidiomycota division have increased. Pesticide application has a short-term stimulating effect on the carbon content of microbial biomass. It has been shown that insecticide imidacloprid stimulates nitrogen fixation, whereas other types of pesticides do not affect this factor.

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REFERENCES

  1. A. I. Dryakhlov, “The effect of soil herbicide Triflurex and Rhizotorfin on nitrogen-fixing activity and yield of soybean seeds,” Maslichn. Kul’t., No. 1 (150), 1–5 (2012).

  2. L. L. Shishov, V. D. Tonkonogov, I. I. Lebedeva, and M. I. Gerasimova, Classification and Diagnostic System of Russian Soils (Oikumena, Smolensk, 2004) [in Russian].

    Google Scholar 

  3. N. A. Manucharova, Hydrolytic Prokaryotic Complexes of Terrestrial Ecosystems (UniversitetskayaKniga, Moscow, 2014) [in Russian].

    Google Scholar 

  4. T. A. Adebayo, O. A. Ojo, and O. A. Olaniran, “Effects of two insecticides Karate1 and Thiodan1 on population dynamics of four different soil microorganisms,” Res. J. Biol. Sci. 2, 557–560 (2007).

    Google Scholar 

  5. M. Allegrini, M. C. Zabaloy, and E. del V. Gómez, “Ecotoxicological assessment of soil microbial community tolerance to glyphosate,” Sci. Total Environ. 533, 60–68 (2015). https://doi.org/10.1016/j.scitotenv.2015.06.096

    Article  Google Scholar 

  6. A. Alvarez, J. M. Saez, J. S. Davila Costa, V. L. Colin, M. S. Fuentes, S. A. Cuozzo, and M. J. Amoroso, “Actinobacteria: current research and perspectives for bioremediation of pesticides and heavy metals,” Chemosphere 166, 41–62 (2017). https://doi.org/10.1016/j.chemosphere.2016.09.070

    Article  Google Scholar 

  7. A. Alvarez-Martin, S. L. Hilton, G. D. Bending, M. S. Rodriguez-Cruz, and M. J. Sanchez-Martin, “Changes in activity and structure of the soil microbial community after application of azoxystrobin or pirimicarb and an organic amendment to an agricultural soil,” Appl. Soil Ecol. 106, 47–57 (2016). .https://doi.org/10.1016/j.apsoil.2016.05.00

    Article  Google Scholar 

  8. J. P. E. Anderson and K. H. Domsch, “A physiological method for the quantitative measurement of microbial biomass in soils,” Soil Biol. Biochem. 10, 215–221 (1978). https://doi.org/10.1016/0038-0717(78)90099-8

    Article  Google Scholar 

  9. J. Barriuso, S. Marin, and R. P. Mellado, “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 (4), 1021–1030 (2010). https://doi.org/10.1111/j.1462-2920.2009.02146.x

    Article  Google Scholar 

  10. G. M. B. Bohm, B. J. R. Alves, S. Urquiaga, R. M. Boddey, G. R. Xavier, F. Hax, and C. V. Rombaldi, “Glyphosate- and imazethapyr-induced effects on yield, nodule mass and biological nitrogen fixation in field-grown glyphosate-resistant soybean,” Soil Biol. Biochem. 41, 420–422 (2009). https://doi.org/10.1016/j.soilbio.2008.11.002

    Article  Google Scholar 

  11. R. H. Bromilow, A. A. Evans, P. H. Nicholls, A. D. Todd, and G. G. Briggs, “The effect on soil fertility of repeated applications of pesticides over 20 years,” Pesticide Sci. 48, 63–72 (1996). https://doi.org/10.1002/(SICI)1096-9063(199609)48:1<63::AID-PS442>3.0.CO;2-I

    Article  Google Scholar 

  12. M. D. Busse, A. W. Ratcliff, C. J. Shestak, and R. F. Powers, “Glyphosate toxicity and the effects of long-term vegetation control on soil microbial communities,” Soil Biol. Biochem. 33, 1777–1789 (2001). https://doi.org/10.1016/S0038-0717(01)00103-1

    Article  Google Scholar 

  13. E. Chanika, D. Georgiadou, E. Soueref, P. Karas, E. Karanasios, N. G. Tsiropoulos, and D. G. Karpouzas, “Isolation of soil bacteria able to hydrolyze both organophosphate and carbamate pesticides,” Bioresour. Technol. 102, 3184–3192 (2011). https://doi.org/10.1016/j.biortech.2010.10.145

    Article  Google Scholar 

  14. A. Channabasava, H. C. Lakshman, and M. A. Jorquera, “Effect of fungicides on association of arbuscular mycorrhiza fungus Rhizophagusfasciculatus and growth of proso millet (Panicummiliaceum L.),” J. Soil Sci. Plant Nutr. 15 (1), 35–45 (2015). https://doi.org/10.4067/S0718-95162015005000004

    Article  Google Scholar 

  15. S. K. Chen, C. A. Edwards, and S. Subler, “Effect of fungicides benomyl, captan and chlorothalonil on soil microbial activity and nitrogen dynamics in laboratory incubations,” Soil Biol. Biochem. 33, 1971–1980 (2001).

    Article  Google Scholar 

  16. M. Cycon, Z. Piotrowska-Seget, A. Kaczynska, and J. Kozdroj, “Microbiological characteristics of a loamy sand soil exposed to tebuconazole and λ-cyhalothrin under laboratory conditions,” Ecotoxicology 15 (8), 639–646 (2006).

    Article  Google Scholar 

  17. A. C. Das and D. Mukherjee, “Soil application of insecticides influences microorganisms and plant nutrients,” Appl. Soil Ecol. 14, 55–62 (2000).

    Article  Google Scholar 

  18. M. Druille, M. Omacini, R. A. Golluscio, and M. N. Cabello, “Arbuscular mycorrhizal fungi are directly and indirectly affected by glyphosate application,” Appl. Soil Ecol. 72, 143–149 (2013). https://doi.org/10.1016/j.apsoil.2013.06.011

    Article  Google Scholar 

  19. D. Efimova, A. Tyakht, A. Popenko, A. Vasilyev, I. Altukhov, N. Dovidchenko, and D. Alexeev, “Knomics-Biota—a system for exploratory analysis of human gut microbiota data,” BioData Min. 11, 1–7 (2018). https://doi.org/10.1186/s13040-018-0187-3

    Article  Google Scholar 

  20. D. W. Fadrosh, B. Ma, P. Gajer, N. Sengamalay, S. Ott, R. M. Brotman, and J. Ravel, “An improved dual-indexing approach for multiplexed 16S rRNA gene sequencing on the Illumina MiSeq platform,” Microbiome 2, 6 (2014). https://doi.org/10.1186/2049-2618-2-6

    Article  Google Scholar 

  21. R. L. Haney, S. A. Senseman, and F. M. Hons, “Effect of roundup ultra on microbial activity and biomass from selected soils,” J. Environ. Qual. 31, 730–735 (2000). https://doi.org/10.2134/jeq2002.7300

    Article  Google Scholar 

  22. S. Hussain, T. Siddique, M. Saleem, M. Arshad, and A. Khalid, “Impact of pesticides on soil microbial diversity, enzymes, and biochemical reactions,” in Advances in Agronomy (Academic, London, 2009), pp. 159–200.

    Google Scholar 

  23. G. Imfeld and S. Vuilleumier, “Measuring the effects of pesticides on bacterial communities in soil: a critical review,” Eur. J. Soil Biol. 49, 22–30 (2012). https://doi.org/10.1016/j.ejsobi.2011.11.010

    Article  Google Scholar 

  24. I. Ipsilantis, C. Samourelis, and D. G. Karpouzas, “The impact of biological pesticides on arbuscular mycorrhizal fungi,” Soil Biol. Biochem. 45, 147–155 (2012). https://doi.org/10.1016/j.soilbio.2011.08.007

    Article  Google Scholar 

  25. IUSS Working Group WRB, World Reference Base for Soil Resources, World Soil Resources Reports No. 103 (UN Food and Agriculture Organization, Rome, 2006).

  26. C. S. Jacobsen and M. H. Hjelmsø, “Agricultural soils, pesticides and microbial diversity,” Curr. Opin. Biotechnol. 27, 15–20 (2014). https://doi.org/10.1016/j.copbio.2013.09.003

    Article  Google Scholar 

  27. T. K. Jana, N. C. Debnath, and R. K. Basak, “Effect of insecticides on decomposition of organic matter, ammonification and nitrification in a fluventicUstochrept,” J. Indian Soc. Soil Sci. 46, 133–134 (1998).

    Google Scholar 

  28. P. K. Jena, T. K. Adhya, and R. V. Rao, “Influence of carbaryl on nitrogenase activity and combinations of butachlor and carbofuran on nitrogen-fixing micro-organisms in paddy soils,” Pest Manage. Sci. 19, 179–184 (1987). https://doi.org/10.1002/ps.2780190303

    Article  Google Scholar 

  29. H. Jin, J. J. Germida, and F. L. Walley, “Suppressive effects of seed-applied fungicides on arbuscular mycorrhizal fungi (AMF) differ with fungicide mode of action and AMF species,” Appl. Soil Ecol. 72 (10), 22–30 (2013). https://doi.org/10.1016/j.apsoil.2013.05.013

    Article  Google Scholar 

  30. A. Katayama, K. Funasaka, and K. Fujie, “Changes in the respiratory quinone profile of a soil treated with pesticides,” Biol. Fertil. Soils 33, 454–459 (2001). https://doi.org/10.1007/s003740100355

    Article  Google Scholar 

  31. R. J. Kremer and N. E. Means, “Glyphosate and glyphosate-resistant crop interactions with rhizosphere microorganisms,” Eur. J. Agron. 31, 153–161 (2009). https://doi.org/10.1016/j.eja.2009.06.004

    Article  Google Scholar 

  32. Y. Li, “Treating wheat seeds with neonicotinoid insecticides does not harm the rhizosphere microbial community,” PloS One 13 (12), (2018). https://doi.org/10.1371/journal.pone.0205200

    Article  Google Scholar 

  33. C.-C. Lo, “Effect of pesticides on soil microbial community,” J. Environ. Sci. Health, Part B 45, 348–359 (2010). https://doi.org/10.1080/03601231003799804

    Article  Google Scholar 

  34. M. V. Martinez-Toledo, V. Salmeron, and J. Gonzalez-Lopez, “Effect of an organophosphorus insecticide, profenofos, on agricultural soil microflora,” Chemosphere 24, 71–80 (1992).

    Article  Google Scholar 

  35. T. B. Moorman, “A review of pesticide effects on microorganisms and microbial processes related to soil fertility,” J. Prod. Agric. 2, 14–23 (1989). https://doi.org/10.2134/jpa1989.0014

    Article  Google Scholar 

  36. P. K. Mukherjee, J. Chandra, M. Retuerto, M. Sikaroodi, R. E. Brown, R. Jurevic, et al., “Oral mycobiome analysis of HIV-infected patients: identification of P-ichia as an antagonist of opportunistic fungi,” PLoSPathog. 10, e1003996 (2014). https://doi.org/10.1371/journal.ppat.1003996

    Article  Google Scholar 

  37. M. Panettieri, L. Lazaro, R. López-Garrido, J. M. Murillo, and E. Madejón, “Glyphosate effect on soil biochemical properties under conservation tillage,” Soil Tillage Res. 133, 16–24 (2013). https://doi.org/10.1016/j.still.2013.05.007

    Article  Google Scholar 

  38. J. R. Powell, R. G. Campbell, K. E. Dunfield, R. H. Gulden, M. M. Hart, D. J. Levy-Booth, and P. M. Antunes, “Effect of glyphosate on the tripartite symbiosis formed by Glomus intraradices, Bradyrhizobiumjaponicum, and genetically modified soybean,” App-l. Soil Ecol. 41, 128–136 (2009). https://doi.org/10.1016/j.apsoil.2008.10.002

    Article  Google Scholar 

  39. A. W. Ratcliff, M. D. Busse, and C. J. Shestak, “Changes in microbial community structure following herbicide (glyphosate) additions to forest soils,” Appl. Soil Ecol. 34, 114–124 (2006). https://doi.org/10.1016/j.apsoil.2006.03.002

    Article  Google Scholar 

  40. W. Riah, K. Laval, E. Laroche-Ajzenberg, C. Mougin, X. Latour, and I. Trinsoutrot-Gattin, “Effects of pesticides on soil enzymes: a review,” Environ. Chem. Lett. 12, 257–273 (2014). https://doi.org/10.1007/s10311-014-0458-2

    Article  Google Scholar 

  41. M. Ros, M. Goberna, J. L. Moreno, T. Hernandez, C. Garcia, H. Insam, and J. A. Pascual, “Molecular and physiological bacterial diversity of a semi-arid soil contaminated with different levels of formulated atrazine,” Appl. Soil Ecol. 34, 93–102 (2006). https://doi.org/10.1016/j.apsoil.2006.03.010

    Article  Google Scholar 

  42. M. T. Rose, T. R. Cavagnaro, C. A. Scanlan, T. J. Rose, T. Vancov, S. Kimber, and L. van Zwieten, “Impact of herbicides on soil biology and function,” Adv. Agron. 136, 133–220 (2016). https://doi.org/10.1016/bs.agron.2015.11.005

    Article  Google Scholar 

  43. R. P. Schreiner and G. J. Bethlenfalvay, “Mycorrhizae, biocides, and biocontrol 3. Effects of three different fungicides on developmental stages of three AM fungi,” Biol. Fertil. Soils 24, 18–26 (1997). https://doi.org/10.1007/BF01420215

    Article  Google Scholar 

  44. W. V. Sigler and R. F. Turco, “The impact of chlorothalonil application on soil bacterial and fungal populations as assessed by denaturing gradient gel electrophoresis,” Appl. Soil Ecol. 21, 107–118 (2002).https://doi.org/10.1016/S0929-1393(02)00088-4

    Article  Google Scholar 

  45. M. Srinivasulu and D. R. Ortiz, “Effect of pesticides on bacterial and fungal populations in Ecuadorian tomato cultivated soils,” Environ. Process. 4, 93–105 (2017).

    Article  Google Scholar 

  46. D. L. Tyess, P. J. Shea, and A. M. Parkhurst, “Mineralization potential of atrazine and degradation intermediates from clustered characteristics in inoculated soils,” Soil Sediment Contam. 15, 87–102 (2006).

    Article  Google Scholar 

  47. M. Wang, Y. Liu, Q. Wang, M. Gong, X. Y. P. Hua, S. Hu, and Y. Yang, “Impacts of methamidophos on the biochemical, catabolic and genetic characteristics of soil microbial communities,” Soil Biol. Biochem. 40, 778–788 (2008).

    Article  Google Scholar 

  48. R. Wang, H. Zhang, L. Sun, G. Qi, S. Chen, and X. Zhao, “Microbial community composition is related to soil biological and chemical properties and bacterial wilt outbreak,” Sci. Rep. 7, 1–10 (2017). https://doi.org/10.1038/s41598-017-00472-6

    Article  Google Scholar 

  49. IUSS Working Group WRB, World Reference Base for Soil Resources 2014, Update 2015, International Soil Classification System for Naming Soils and Creating Legends for Soil Maps, World Soil Resources Reports No. 106 (UN Food and Agriculture Organization, Rome, 2015), p. 192.

  50. M. C. Zabaloy, et al., “Herbicides in the soil environment: linkage between bioavailability and microbial ecology,” in Herbicides, Theory and Applications, Ed. by S. Soloneski and M. L. Larramendy (Rijeka, 2011), pp. 161–192.

    Google Scholar 

  51. R. M. Zablotowicz and K. N. Reddy, “Nitrogenase activity, nitrogen content, and yield responses to glyphosate in glyphosate-resistant soybean,” Crop Prot. 26, 370–376 (2007). https://doi.org/10.1016/j.cropro.2005.05.013

    Article  Google Scholar 

  52. L. H. S. Zobiole, R. J. Kremer, R. S. Oliveira, and J. Constantin, “Glyphosate affects micro-organisms in rhizospheres of glyphosate-resistant soybeans,” J. Appl. Microbiol. 110, 118–127 (2010). https://doi.org/10.1111/j.1365-2672.2010.04864.x

    Article  Google Scholar 

  53. L. H. S. Zobiole, R. S. Oliveira, R. J. Kremer, J. Constantin, T. Yamada, C. Castro, and A. Oliveira, “Effect of glyphosate on symbiotic N2 fixation and nickel concentration in glyphosate-resistant soybeans,” Appl. Soil Ecol. 44, 176–180 (2010). https://doi.org/10.1016/j.apsoil.2009.12.003

    Article  Google Scholar 

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Funding

The study was supported by the Russian Foundation for Basic Research (project nos. 18-016-00130a and 18-316-00054 mol_a).

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Authors and Affiliations

  1. Lomonosov Moscow State University, 119991, Moscow, Russia

    A. A. Astaykina, R. A. Streletskii, M. N. Maslov, A. A. Belov & A. L. Stepanov

  2. All-Russia Institute of Phytopathology, 143050, Bol’shie Vyazemy, Moscow oblast, Russia

    A. A. Astaykina & V. S. Gorbatov

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  1. A. A. Astaykina
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  2. R. A. Streletskii
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Astaykina, A.A., Streletskii, R.A., Maslov, M.N. et al. The Impact of Pesticides on the Microbial Community of Agrosoddy-Podzolic Soil. Eurasian Soil Sc. 53, 696–706 (2020). https://doi.org/10.1134/S1064229320050038

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