Nicosulfuron Application in Agricultural Soils Drives the Selection Towards NS-tolerant Microorganisms Harboring Various Levels of Sensitivity to Nicosulfuron

Overview

Journal Environ Sci Pollut Res Int

Publisher Springer

Specialties Environmental Health
Toxicology

Date 2015 Nov 1

PMID 26517995

Citations 6

Authors

Ines Petric

Dimitrios G Karpouzas

David Bru

Nikolina Udikovic-Kolic

Ellen Kandeler

Simonida Djuric

Fabrice Martin-Laurent

Affiliations

Soon will be listed here.

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

BAUERLE R, FRUENDLICH M, Stormer F, Umbarger H . CONTROL OF ISOLEUCINE, VALINE AND LEUCINE BIOSYNTHESIS. II. ENDPRODUCT INHIBITION BY VALINE OF ACETOHYDROXY ACID SYNTHETASE IN SALMONELLA TYPHIMURIUM. Biochim Biophys Acta. 1964; 92:142-9. View

Ibdah M, Bar-Ilan A, Livnah O, Schloss J, Barak Z, Chipman D . Homology modeling of the structure of bacterial acetohydroxy acid synthase and examination of the active site by site-directed mutagenesis. Biochemistry. 1996; 35(50):16282-91. DOI: 10.1021/bi961588i. View

Udikovic-Kolic N, Scott C, Martin-Laurent F . Evolution of atrazine-degrading capabilities in the environment. Appl Microbiol Biotechnol. 2012; 96(5):1175-89. DOI: 10.1007/s00253-012-4495-0. View

Zhang H, Mu W, Hou Z, Wu X, Zhao W, Zhang X . Biodegradation of nicosulfuron by the bacterium Serratia marcescens N80. J Environ Sci Health B. 2012; 47(3):153-60. DOI: 10.1080/03601234.2012.632249. View

Jacobsen C, Hjelmso M . Agricultural soils, pesticides and microbial diversity. Curr Opin Biotechnol. 2014; 27:15-20. DOI: 10.1016/j.copbio.2013.09.003. View

Mukherjee A, Bordoloi N . 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 Pollut Res Int. 2012; 19(8):3380-8. DOI: 10.1007/s11356-012-0862-8. View

Perriere G, Gouy M . WWW-query: an on-line retrieval system for biological sequence banks. Biochimie. 1996; 78(5):364-9. DOI: 10.1016/0300-9084(96)84768-7. View

De Felice M, Griffo G, Lago C, Limauro D, Ricca E . Detection of the acetolactate synthase isozymes I and III of Escherichia coli K12. Methods Enzymol. 1988; 166:241-4. DOI: 10.1016/s0076-6879(88)66032-0. View

Lin X, Zhao Y, Fu Q, Umashankara M, Feng Z . Analysis of culturable and unculturable microbial community in bensulfuron-methyl contaminated paddy soils. J Environ Sci (China). 2009; 20(12):1494-500. DOI: 10.1016/s1001-0742(08)62555-3. View

10.

Nye T, Lio P, Gilks W . A novel algorithm and web-based tool for comparing two alternative phylogenetic trees. Bioinformatics. 2005; 22(1):117-9. DOI: 10.1093/bioinformatics/bti720. View

11.

Gurtler V, Stanisich V . New approaches to typing and identification of bacteria using the 16S-23S rDNA spacer region. Microbiology (Reading). 1996; 142 ( Pt 1):3-16. DOI: 10.1099/13500872-142-1-3. View

12.

Lang Z, Shen J, Cai S, Zhang J, He J, Li S . Expression, characterization, and site-directed mutation of a multiple herbicide-resistant acetohydroxyacid synthase (rAHAS) from Pseudomonas sp. Lm10. Curr Microbiol. 2011; 63(2):145-50. DOI: 10.1007/s00284-011-9953-x. View

13.

Thompson J, Gibson T, Plewniak F, Jeanmougin F, Higgins D . The CLUSTAL_X windows interface: flexible strategies for multiple sequence alignment aided by quality analysis tools. Nucleic Acids Res. 1998; 25(24):4876-82. PMC: 147148. DOI: 10.1093/nar/25.24.4876. View

14.

Nelson D, Duxbury T . The distribution of acetohydroxyacid synthase in soil bacteria. Antonie Van Leeuwenhoek. 2007; 93(1-2):123-32. DOI: 10.1007/s10482-007-9186-y. View

15.

Janssen P . Identifying the dominant soil bacterial taxa in libraries of 16S rRNA and 16S rRNA genes. Appl Environ Microbiol. 2006; 72(3):1719-28. PMC: 1393246. DOI: 10.1128/AEM.72.3.1719-1728.2006. View

16.

Bending G, Rodriguez-Cruz M, Lincoln S . Fungicide impacts on microbial communities in soils with contrasting management histories. Chemosphere. 2007; 69(1):82-8. DOI: 10.1016/j.chemosphere.2007.04.042. View

17.

Allievi L, Gigliotti C . Response of the bacteria and fungi of two soils to the sulfonylurea herbicide cinosulfuron. J Environ Sci Health B. 2001; 36(2):161-75. DOI: 10.1081/PFC-100103741. View

18.

Topp E, Chapman R, Devers-Lamrani M, Hartmann A, Marti R, Martin-Laurent F . Accelerated Biodegradation of Veterinary Antibiotics in Agricultural Soil following Long-Term Exposure, and Isolation of a Sulfamethazine-degrading sp. J Environ Qual. 2013; 42(1):173-8. DOI: 10.2134/jeq2012.0162. View

19.

Martin-Laurent F, Kandeler E, Petric I, Djuric S, Karpouzas D . 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 Res Int. 2012; 20(2):1203-5. DOI: 10.1007/s11356-012-1368-0. View

20.

Kirk J, Beaudette L, Hart M, Moutoglis P, Klironomos J, Lee H . Methods of studying soil microbial diversity. J Microbiol Methods. 2004; 58(2):169-88. DOI: 10.1016/j.mimet.2004.04.006. View