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Nicosulfuron application in agricultural soils drives the selection towards NS-tolerant microorganisms harboring various levels of sensitivity to nicosulfuron

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Abstract

The action mode of sulfonylurea herbicides is the inhibition of the acetohydroxyacid synthase (AHAS) required for the biosynthesis of amino acids valine and isoleucine in plants. However, this enzyme is also present in a range of non-targeted organisms, among which soil microorganisms are known for their pivotal role in ecosystem functioning. In order to assess microbial toxicity of sulfonylurea herbicide nicosulfuron (NS), a tiered microcosm (Tier I) to field (Tier II) experiment was designed. Soil bacteria harboring AHAS enzyme tolerant to the herbicide nicosulfuron were enumerated, isolated, taxonomically identified, and physiologically characterized. Results suggested that application of nicosulfuron drives the selection towards NS-tolerant bacteria, with increasing levels of exposure inducing an increase in their abundance and diversity in soil. Tolerance to nicosulfuron was shown to be widespread among the microbial community with various bacteria belonging to Firmicutes (Bacillus) and Actinobacteria (Arthrobacter) phyla representing most abundant and diverse clusters. While Arthrobacter bacterial population dominated community evolved under lower (Tier II) nicosulfuron selection pressure, it turns out that Bacillus dominated community evolved under higher (Tier I) nicosulfuron selection pressure. Different NS-tolerant bacteria likewise showed different levels of sensitivity to the nicosulfuron estimated by growth kinetics on nicosulfuron. As evident, Tier I exposure allowed selection of populations able to better cope with nicosulfuron. One could propose that sulfonylureas-tolerant bacterial community could constitute a useful bioindicator of exposure to these herbicides for assessing their ecotoxicity towards soil microorganisms.

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References

  1. Allievi L, Gigliotti C (2001) Response of the bacteria and fungi of two soils to the sulfonylurea herbicide cinosulfuron. J Environ Sci Heal B 36:161–175

  2. Bauerle RH, Freundlich M, Umbarger HE, Stormer FC (1964) Control of isoleucine valine + leucine biosynthesis.II. endproduct inhibition by valine of acetohydroxy acid synthetase in salmonella typhimurium. Biochim Biophys Acta 92:142–149

  3. Bending GD, Rodriguez-Cruz MS, Lincoln SD (2007) Fungicide impacts on microbial communities in soils with contrasting management histories. Chemosphere 69:82–88

  4. Blank H, Wängberg SA, Molander S (1988) Pollution-induced community tolerance-a new ecotoxicological tool. In: Cairns JJ, Pratt JR (eds) Functional testing of aquatic biota for estimating hazards of chemicals. American Society for Testing and Materials, Philadelphia, pp 219–230

  5. Boldt TS, Jacobsen CS (1998) Different toxic effects of the sulfonylurea herbicides metsulfuron methyl, chlorsulfuron and thifensulfuron methyl on fluorescent pseudomonads isolated from an agricultural soil. FEMS Microbiol Lett 161:29–35

  6. Burnet M, Hodgson B (1991) Differential-effects of the sulfonylurea herbicides chlorsulfuron and sulfometuron methyl on microorganisms. Arch Microbiol 155:521–525

  7. Crouzet O, Batisson I, Besse-Hoggan P, Bonnemoy F, Bardot C, Poly F, Bohatier J, Mallet C (2010) Response of soil microbial communities to the herbicide mesotrione: a dose-effect microcosm approach. Soil Biol Biochem 42:193–202

  8. De Felice M, Griffo G, Lago CT, Limauro D, Ricca E (1988) Detection of the acetolactate synthase isozyme-i and isozyme-iii of Escherichia-coli-k12. Method Enzymol 166:241–244

  9. Duggleby RG, Pang SS (2000) Acetohydroxyacid synthase. J Biochem Mol Biol 33:1–36

  10. El Azhari N, Devers-Lamrani M, Chatagnier G, Rouard N, Martin-Laurent F (2010) Molecular analysis of the catechol-degrading bacterial community in a coal wasteland heavily contaminated with PAHs. J Hazard Mater 177:593–601

  11. Elisakova V, Patek M, Holatko J, Nesvera JN, Leyval D, Goergen JL, Delaunay S (2005) Feedback-resistant acetohydroxy acid synthase increases valine production in Corynebacterium glutamicum. Appl Environ Microb 71:207–213

  12. Forlani G, Mantelli M, Branzoni M, Nielsen E, Favilli F (1995) Differential sensitivity of plant-associated bacteria to sulfonylurea and imidazolinone herbicides. Plant Soil 176:243–253

  13. Friedberg D, Seijffers J (1988) Sulfonylurea-resistant mutants and natural tolerance of cyanobacteria. Arch Microbiol 150:278–281

  14. Gianfreda L, Rao MA (2011) The influence of pesticides on soil enzymes. Soil Enzymology, Soil Biology 22. Springer-Verlag, Berlin Heidelberg, pp 293–312

  15. Gurtler V, Stanisich VA (1996) New approaches to typing and identification of bacteria using the 16S-23S rDNA spacer region. Microbiol-Sgm 142:3–16

  16. Huang X, He J, Sun XF, Sun JQ, Li YF, Shen JJ, Li SP (2010) Characterization and molecular mechanism of a naturally occurring metsulfuron-methyl resistant strain of Pseudomonas aeruginosa. World J Microb Biot 26:515–521

  17. Ibdah M, BarIlan A, Livnah O, Schloss JV, Barak Z, Chipman DM (1996) Homology modeling of the structure of bacterial acetohydroxy acid synthase and examination of the active site by site-directed mutagenesis. Biochemistry 35:16282–16291

  18. Jacobsen CS, Hjelmso MH (2014) Agricultural soils, pesticides and microbial diversity. Curr Opin Biotech 27:15–20

  19. Janssen PH (2006) Identifying the dominant soil bacterial taxa in libraries of 16S rRNA and 16S rRNA genes. Appl Environ Microb 72:1719–1728

  20. Karpouzas DG, Kandeler E, Bru D, Friedel I, Auer Y, Kramer S, Vasileiadis S, Petric I, Udikovic-Kolic N, Djuric S, Martin-Laurent F (2014a) A tiered assessment approach based on standardized methods to estimate the impact of nicosulfuron on the abundance and function of the soil microbial community. Soil Biol Biochem 75:282–291

  21. Karpouzas DG, Papadopoulou E, Ipsilantis I, Friedel I, Petric I, Udikovic-Kolic N, Djuric S, Kandeler E, Menkissoglu-Spiroudi U, Martin-Laurent F (2014b) Effects of nicosulfuron on the abundance and diversity of arbuscular mycorrhizal fungi used as indicators of pesticide soil microbial toxicity. Ecol Indic 39:44–53

  22. Kirk JL, Beaudette LA, Hart M, Moutoglis P, Khironomos JN, Lee H, Trevors JT (2004) Methods of studying soil microbial diversity. J Microbiol Methods 58:169–188

  23. Lang ZF, Shen JJ, Cai S, Zhang J, He J, Li SP (2011) Expression, characterization, and site-directed mutation of a multiple herbicide-resistant acetohydroxyacid synthase (rAHAS) from Pseudomonas sp Lm10. Curr Microbiol 63:145–150

  24. LaRossa RA, Schloss JV (1984) The sulfonylurea herbicide sulfometuron methyl is an extremely potent and selective inhibitor of acetolactate synthase in salmonella-typhimurium. J Biol Chem 259:8753–8757

  25. Lin X, Zhao Y, Fu Q, Umashankara ML, Feng Z (2008) Analysis of culturable and unculturable microbial community in bensulfuron-methyl contaminated paddy soils. J Environ Sci (China) 20(12):1494–500

  26. Martin-Laurent F, Kandeler E, Petric I, Djuric S, Karpouzas DG (2013) ECOFUN-MICROBIODIV: an FP7 European project for developing and evaluating innovative tools for assessing the impact of pesticides on soil functional microbial diversity-towards new pesticide registration regulation? Environ Sci Pollut R 20:1203–1205

  27. Mukherjee AK, Bordoloi NK (2012) Biodegradation of benzene, toluene, and xylene (BTX) in liquid culture and in soil by Bacillus subtilis and Pseudomonas aeruginosa strains and a formulated bacterial consortium. Environ Sci and Pollut R 19:3380–3388

  28. Nelson DR, Duxbury T (2008) The distribution of acetohydroxyacid synthase in soil bacteria. Anton Leeuw Int J G 93:123–132

  29. Niemi RM, Heiskanen I, Ahtiainen JH, Rahkonen A, Mantykoski K, Welling L, Laitinen P, Ruuttunen P (2009) Microbial toxicity and impacts on soil enzyme activities of pesticides used in potato cultivation. Appl Soil Ecol 41:293–304

  30. Nye TMW, Lio P, Gilks WR (2006) A novel algorithm and web-based tool for comparing two alternative phylogenetic trees. Bioinformatics 22:117–119

  31. Perriere G, Gouy M (1996) WWW-Query: an on-line retrieval system for biological sequence banks. Biochimie 78:364–369

  32. Saeki M, Toyota K (2004) Effect of bensulfuron-methyl (a sulfonylurea herbicide) on the soil bacterial community of a paddy soil microcosm. Biol Fert Soils 40:110–118

  33. Seghers D, Siciliano SD, Top EM, Verstraete W (2005) Combined effect of fertilizer and herbicide applications on the abundance, community structure and performance of the soil methanotrophic community. Soil Biol Biochem 37:187–193

  34. Tapia LS, Bauman TT, Harvey RG, Kells JJ, Kapusta G, Loux MM, Lueschen WE, Owen MDK, Hageman LH, Strachan SD (1997) Postemergence herbicide application timing effects on annual grass control and corn (Zea mays) grain yield. Weed Sci 45:138–143

  35. Thompson JD, Gibson TJ, Plewniak F, Jeanmougin F, Higgins DG (1997) The CLUSTAL_X windows interface: flexible strategies for multiple sequence alignment aided by quality analysis tools. Nucleic Acids Res 25:4876–4882

  36. Topp E, Chapman R, Devers-Lamrani M, Hartmann A, Marti R, Martin-Laurent F, Sabourin L, Scott A, Sumarah M (2013) Accelerated biodegradation of veterinary antibiotics in agricultural soil following long-term exposure, and isolation of a sulfamethazine-degrading Microbacterium sp. J Environ Qual 42:173–178

  37. Udikovic-Kolic N, Scott C, Martin-Laurent F (2012) Evolution of atrazine-degrading capabilities in the environment. Appl Microbiol Biotechnol 96:1175–1189

  38. Xie XM, Liao M, Huang CY, Liu WP (2004) Effects of bensulfuron-methyl on soil microbial activity and biochemical characteristics in paddy. Chinese J Rice Sci 18:67–72

  39. Zhang H, Mu WH, Hou ZG, Wu X, Zhao WW, Zhang XH, Pan HY, Zhang SH (2012) Biodegradation of nicosulfuron by the bacterium Serratia marcescens N80. J Environ Sci Heal B 47:153–160

  40. Zhou Q, Liu W, Zhang Y, Liu KK (2007) Action mechanisms of acetolactate synthase-inhibiting herbicides. Pestic Biochem Phys 89:89–96

  41. Zohar Y, Einav M, Chipman DM, Barak Z (2003) Acetohydroxyacid synthase from Mycobacterium avium and its inhibition by sulfonylureas and imidazolinones. BBA-Proteins Proteom 1649:97–105

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Acknowledgments

This study was financed within the frame of the SEEERA.NET PLUS project no. ERA 216/1ECOFUN-MICROBIODIV: Development and evaluation of innovative tools to estimate the ecotoxicological impact of low-dose pesticide application in agriculture on soil functional microbial biodiversity (http://plus.see-era.net//pjc/fundedprojects.html). We would like to thank Ralf Hanatscheck and Christian Schache from Project Management Agency c/o German Aerospace Center (DLR, Bonn, Germany) for their assistance all along the project.

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Correspondence to Ines Petric.

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All the participants listed as co-authors have contributed significantly in the execution and interpretation of the reported study. All co-authors have seen and approved the final version of the manuscript and have agreed to its submission for publication in the journal Environmental Science and Pollution Research. Research presented in the manuscript did involve neither human participants nor animals.

Conflict of Interest

The authors declare that they have no competing interests.

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Responsible editor: Philippe Garrigues

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Petric, I., Karpouzas, D.G., Bru, D. et al. Nicosulfuron application in agricultural soils drives the selection towards NS-tolerant microorganisms harboring various levels of sensitivity to nicosulfuron. Environ Sci Pollut Res 23, 4320–4333 (2016). https://doi.org/10.1007/s11356-015-5645-6

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Keywords

  • Agricultural soil
  • Sulfonylurea herbicides
  • Nicosulfuron
  • Ecotoxicology
  • Microbial community
  • Tolerant bacteria
  • AHAS enzyme