Abstract
Sulfonylurea herbicides are widely used for weed control in agriculture, and they are suspected to alter microbial communities and activities in the soil. This study investigates the impact of two sulfonylurea herbicides chlorsulfuron and sulfosulfuron on microbial community and activity in two different soils taken from two sites in west part of the Slovak Republic. The soil from the Malanta site was silt-loam luvisol with pH(H2O) 5.78 while the soil from the Stefanov site was sandy-loam regosol with pH(H2O) 8.25. These soils were not treated by sulfonylurea herbicides at least for 2 years prior to the study. In laboratory assay, the herbicides were applied to soil in their maximal recommended doses 26 and 25 g per hectare of chlorsulfuron and sulfosulfuron, respectively. Their effect was evaluated on the 3rd, 7th, 14th, 28th, 56th, and 112th day after application to soil. Illumina high-throughput amplicon sequencing of the 16S rRNA gene and ITS region was used to monitor changes on prokaryotic and fungal community composition. Enzymatic activity was evaluated using 11 substrates. Physiological profile of microbial community was analyzed using Biolog© ecoplates. Significant changes in enzymatic activity caused by the application of herbicides were found during the first 28 days. The application of herbicides altered the activity of cellobiohydrolase, arylsulphatase, dehydrogenase, phosphatase, and FDA hydrolase. Chlorsulfuron caused a more varying response of enzymatic activity than sulfosulfuron, and observed changes were not the same for both soils. In Malanta soil, chlorsulfuron decreased dehydrogenase activity while it was increased in the Stefanov soil. Phosphatase activity was decreased in both soils on 7th and 14th day. There were only minor changes in prokaryotic or fungal community or physiological profiles regarding pesticide application. Differences between soils and incubation time explained most of the variability in these parameters. Diversity indices, physiological parameters, and enzymatic activity decreased over time. The results have shown that chlorsulfuron and sulfosulfuron can affect the function and activity of the soil microbial community without significant change in its composition.
Similar content being viewed by others
References
Arabet D, Tempel S, Fons M, Denis Y, Jourlin-Castelli C, Armitano J, Redelberger D, Iobbi-Nivol C, Boulahrouf A, Méjean V (2014) Effects of a sulfonylurea herbicide on the soil bacterial community. Environ Sci Pollut Res 21:5619–5627
Baldrian P (2009) Microbial enzyme-catalyzed processes in soils and their analysis. Plant Soil Environ 55:370–378
Bezuglova OS et al (2019) Effect of humic preparation on winter wheat productivity and rhizosphere microbial community under herbicide-induced stress. J Soils Sediments. https://doi.org/10.1007/s11368-018-02240-z
Brown Hugh M (1990) Mode of action, crop selectivity, and soil relations of the sulfonylurea herbicides. Pest Sci 29:263–281. https://doi.org/10.1002/ps.2780290304
Caporaso JG et al (2011) Global patterns of 16S rRNA diversity at a depth of millions of sequences per sample. Proc Natl Acad Sci 108:4516–4522
Carles L, Rossi F, Joly M, Besse-Hoggan P, Batisson I, Artigas J (2017) Biotransformation of herbicides by aquatic microbial communities associated to submerged leaves. Environ Sci Pollut Res 24:3664–3674. https://doi.org/10.1007/s11356-016-8035-9
Casida L Jr, Klein D, Santoro T (1964) Soil dehydrogenase activity. Soil Sci 98:371–376
Cassel D, Nielsen D (1986) Field capacity and available water capacity methods of soil analysis: part 1 physical and mineralogical. Methods 5:901–926
Das SK, Mukherjee I, Das SK (2017) Metsulfuron-methyl herbicide on dehydrogenase and acid phosphatase enzyme activity on three different soils. Int J Bio-Resour Stress Manag 8
Dennis PG, Kukulies T, Forstner C, Orton TG, Pattison AB (2018) The effects of glyphosate, glufosinate, paraquat and paraquat-diquat on soil microbial activity and bacterial, archaeal and nematode diversity. Sci Rep 8:2119. https://doi.org/10.1038/s41598-018-20589-6
Dilly O, Nannipieri P (2001) Response of ATP content, respiration rate and enzyme activities in an arable and a forest soil to nutrient additions. Biol Fertil Soils 34:64–72
Dollinger J, Jose S (2018) Agroforestry for soil health Agroforestry Systems 1–7
Drozd P (2010) ComEcoPaC—community ecology parameter calculator. Version 1
Duke SO (2012) Why have no new herbicide modes of action appeared in recent years? Pest Manag Sci 68:505–512
Fragoeiro S, Magan N (2008) Impact of Trametes versicolor and Phanerochaete chrysosporium on differential breakdown of pesticide mixtures in soil microcosms at two water potentials and associated respiration and enzyme activity. Int Biodeterior Biodegrad 62:376–383. https://doi.org/10.1016/j.ibiod.2008.03.003
Furtak K, Gajda AM (2017) Activity of dehydrogenases as an indicator of soil environment quality. Pol J Soil Sci 50:33
Gallitzendörfer R, Timm T, Koch D, Küsters M, Gerhartz M (2011) Simultaneous determination of 12 sulfonylurea herbicides in drinking water after SPE by LC-DAD. Chromatographia 73:813–816
García-Delgado C, Barba-Vicente V, Marín-Benito JM, Mariano Igual J, Sánchez-Martín MJ, Sonia Rodríguez-Cruz M (2019) Influence of different agricultural management practices on soil microbial community over dissipation time of two herbicides. Sci Total Environ 646:1478–1488. https://doi.org/10.1016/j.scitotenv.2018.07.395
Green VS, Stott DE, Diack M (2006) Assay for fluorescein diacetate hydrolytic activity: optimization for soil samples. Soil Biol Biochem 38:693–701
Guijarro KH, Aparicio V, De Gerónimo E, Castellote M, Figuerola EL, Costa JL, Erijman L (2018) Soil microbial communities and glyphosate decay in soils with different herbicide application history. Sci Total Environ 634:974–982. https://doi.org/10.1016/j.scitotenv.2018.03.393
Guindon S, Dufayard J-F, Lefort V, Anisimova M, Hordijk W, Gascuel O (2010) New algorithms and methods to estimate maximum-likelihood phylogenies: assessing the performance of PhyML 3.0. Syst Biol 59:307–321. https://doi.org/10.1093/sysbio/syq010
Hackett CA, Griffiths BS (1997) Statistical analysis of the time-course of Biolog substrate utilization. J Microbiol Methods 30:63–69. https://doi.org/10.1016/S0167-7012(97)00045-6
Hamady M, Lozupone C, Knight R (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
Heap I (2014) Herbicide resistant weeds. In: Integrated pest management. Springer, pp 281-301 http://hracglobal.com (2018)
Ihrmark K, Bödeker ITM, Cruz-Martinez K, Friberg H, Kubartova A, Schenck J, Strid Y, Stenlid J, Brandström-Durling M, Clemmensen KE, Lindahl BD (2012) New primers to amplify the fungal ITS2 region—evaluation by 454-sequencing of artificial and natural communities. FEMS Microbiol Ecol 82:666–677
Imfeld G, Besaury L, Maucourt B, Donadello S, Baran N, Vuilleumier S (2018) Toward integrative bacterial monitoring of metolachlor toxicity in groundwater. Front Microbiol 9:2053–2053. https://doi.org/10.3389/fmicb.2018.02053
Joshi MM, Brown HM, Romesser JA (1985) Degradation of chlorsulfuron by soil microorganisms. Weed Sci 33:888–893
Karpouzas DG et al (2014) 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. https://doi.org/10.1016/j.soilbio.2014.04.022
Kepler R et al (2018) Soil microbial communities in diverse agroecosystems exposed to glyphosate. bioRxiv:484055. https://doi.org/10.1101/484055
Kibblewhite MG, Ritz K, Swift MJ (2008) Soil health in agricultural systems. Philos Trans R Soc B Biol Sci 363:685–701
Kniss AR (2017) Long-term trends in the intensity and relative toxicity of herbicide use. Nat Commun 8:14865. https://doi.org/10.1038/ncomms14865
Lee KY, Townsend J, Tepperman J, Black M, Chui CF, Mazur B, Dunsmuir P, Bedbrook J (1988) The molecular basis of sulfonylurea herbicide resistance in tobacco. EMBO J 7:1241–1248
Lupwayi NZ, Harker KN, Clayton GW, Turkington TK, Rice WA, O’Donovan JT (2004) Soil microbial biomass and diversity after herbicide application. Can J Plant Sci 84:677–685. https://doi.org/10.4141/P03-121
Maheswari ST, Ramesh A (2007) Adsorption and degradation of sulfosulfuron in soils. Environ Monit Assess 127:97–103
Margalef O, Sardans J, Fernández-Martínez M, Molowny-Horas R, Janssens IA, Ciais P, Goll D, Richter A, Obersteiner M, Asensio D, Peñuelas J (2017) Global patterns of phosphatase activity in natural soils. Sci Rep 7:1337. https://doi.org/10.1038/s41598-017-01418-8
Medo J, Maková J, Kovácsová S, Majerčíková K, Javoreková S (2015) Effect of Dursban 480 EC (chlorpyrifos) and Talstar 10 EC (bifenthrin) on the physiological and genetic diversity of microorganisms in soil. J Environ Sci Health B 50:871–883. https://doi.org/10.1080/03601234.2015.1062659
Moretto JAS, Stehling EG, Andreote FD, Altarugio LM, Andrade PA, Fachin AL (2017) Changes in bacterial community after application of three different herbicides. FEMS Microbiol Lett 364. https://doi.org/10.1093/femsle/fnx113
Newman MM, Hoilett N, Lorenz N, Dick RP, Liles MR, Ramsier C, Kloepper JW (2016) Glyphosate effects on soil rhizosphere-associated bacterial communities. Sci Total Environ 543:155–160. https://doi.org/10.1016/j.scitotenv.2015.11.008
Niu H, Shi Y, Cai Y, Wei F, Jiang G (2009) Solid-phase extraction of sulfonylurea herbicides from water samples with single-walled carbon nanotubes disk. Microchim Acta 164:431–438
Oksanen J et al (2013) Package ‘vegan’ community ecology package, version 2
Patle P, Navnage N, Barange P (2018) Fluorescein diacetate (FDA): measure of total microbial activity and as indicator of soil quality. Int J Curr Microbiol Appl Sci 7:2103–2107
Paul EA (2014) Soil microbiology, ecology and biochemistry. Academic press
Perucci P, Scarponi L (1996) Side effects of rimsulfuron on the microbial biomass of a clay-loam soil. J Environ Q 25:610–613
R Core Team (2019) R: A language and environment for statistical computing. R Foundation for Statistical Computing, Vienna
Rachedi K et al (2018) Effect of sulfonylurea tribenuron methyl herbicide on soil Actinobacteria growth and characterization of resistant strains. Braz J Microbiol 49:79–86
Radivojević L, Jovičić JD, Šantrić L, Gašić S, Gajić JU (2014) Effects of metsulfuron-methyl on soil microbial acitvity. Arhiv Za Tehničke Nauke/Archives For Technical Sciences 1:77–82
Ratcliff AW, Busse MD, Shestak CJ (2006) Changes in microbial community structure following herbicide (glyphosate) additions to forest soils. Appl Soil Ecol 34:114–124. https://doi.org/10.1016/j.apsoil.2006.03.002
Riah-Anglet W, Trinsoutrot-Gattin I, Norini M-P, Gauthier A, Latour X, Laval K (2018) Initial state of soil microbial communities determines their stress response. J Environ Chem Eng 6:5470–5480. https://doi.org/10.1016/j.jece.2018.08.019
Rognes T, Flouri T, Nichols B, Quince C, Mahé F (2016) VSEARCH: a versatile open source tool for metagenomics. PeerJ 4:e2584
Saha S, Kulshrestha G (2008) Hydrolysis kinetics of the sulfonylurea herbicide sulfosulfuron. Int J Environ Anal Chem 88:891–898. https://doi.org/10.1080/03067310802124278
Sahoo S, Adak T, Bagchi TB, Kumar U, Munda S, Saha S, Berliner J, Jena M, Mishra BB (2017) Effect of pretilachlor on soil enzyme activities in tropical rice soil. Bull Environ Contam Toxicol 98:439–445. https://doi.org/10.1007/s00128-016-1943-z
Sarmah AK, Sabadie J (2002) Hydrolysis of sulfonylurea herbicides in soils and aqueous solutions: a review. J Agric Food Chem 50:6253–6265
Schlatter DC, Yin C, Hulbert S, Burke I, Paulitz T (2017) Impacts of repeated glyphosate use on wheat-associated bacteria are small and depend on glyphosate use history. Appl Environ Microbiol 83:e01354–e01317. https://doi.org/10.1128/AEM.01354-17
Schöler A, Jacquiod S, Vestergaard G, Schulz S, Schloter M (2017) Analysis of soil microbial communities based on amplicon sequencing of marker genes. Biol Fertil Soils 53:485–489. https://doi.org/10.1007/s00374-017-1205-1
Sofo A, Scopa A, Dumontet S, Mazzatura A, Pasquale V (2012) Toxic effects of four sulphonylureas herbicides on soil microbial biomass. J Environ Sci Health B 47:653–659. https://doi.org/10.1080/03601234.2012.669205
Sondhia S, Waseem U, Varma R (2013) Fungal degradation of an acetolactate synthase (ALS) inhibitor pyrazosulfuron-ethyl in soil. Chemosphere 93:2140–2147
Standley DM, Katoh K (2013) MAFFT multiple sequence alignment software version 7: improvements in performance and usability. Mol Biol Evol 30:772–780. https://doi.org/10.1093/molbev/mst010
Storck V, Nikolaki S, Perruchon C, Chabanis C, Sacchi A, Pertile G, Baguelin C, Karas PA, Spor A, Devers-Lamrani M, Papadopoulou ES, Sibourg O, Malandain C, Trevisan M, Ferrari F, Karpouzas DG, Tsiamis G, Martin-Laurent F (2018) Lab to field assessment of the ecotoxicological impact of chlorpyrifos, isoproturon, or tebuconazole on the diversity and composition of the soil bacterial community. Front Microbiol 9:1412–1412. https://doi.org/10.3389/fmicb.2018.01412
Tabatabai M, Bremner J (1969) Use of p-nitrophenyl phosphate for assay of soil phosphatase activity. Soil Biol Biochem 1:301–307
Thirunarayanan K, Zimdahl RL, Smika DE (1985) Chlorsulfuron adsorption and degradation in soil. Weed Sci 33:558–563
Tomco PL, Duddleston KN, Schultz EJ, Hagedorn B, Stevenson TJ, Seefeldt SS (2016) Field degradation of aminopyralid and clopyralid and microbial community response to application in Alaskan soils. Environ Toxicol Chem 35:485–493. https://doi.org/10.1002/etc.3222
Vepsäläinen M, Kukkonen S, Vestberg M, Sirviö H, Niemi RM (2001) Application of soil enzyme activity test kit in a field experiment. Soil Biol Biochem 33:1665–1672
Vetrovský T, Baldrian P, Morais D, Berger B (2018) SEED 2: a user-friendly platform for amplicon high-throughput sequencing data analyses. Bioinformatics 1:3
Wang Q, Garrity GM, Tiedje JM, Cole JR (2007) Naive Bayesian classifier for rapid assignment of rRNA sequences into the new bacterial taxonomy. Appl Environ Microbiol 73:5261–5267
Weiss S, Xu ZZ, Peddada S, Amir A, Bittinger K, Gonzalez A, Lozupone C, Zaneveld JR, Vázquez-Baeza Y, Birmingham A, Hyde ER, Knight R (2017) Normalization and microbial differential abundance strategies depend upon data characteristics. Microbiome 5:27. https://doi.org/10.1186/s40168-017-0237-y
Wołejko E, Kaczyński P, Łozowicka B, Wydro U, Borusiewicz A, Hrynko I, Konecki R, Snarska K, Dec D, Malinowski P (2017) Dissipation of S-metolachlor in plant and soil and effect on enzymatic activities. Environ Monit Assess 189:355. https://doi.org/10.1007/s10661-017-6071-7
Wołejko E, Jabłońska-Trypuć A, Wydro U, Butarewicz A, Łozowicka B (2020) Soil biological activity as an indicator of soil pollution with pesticides—a review. Appl Soil Ecol 147:103356. https://doi.org/10.1016/j.apsoil.2019.09.006
Xu J, Zhang Y, Dong F, Liu X, Wu X, Zheng Y (2014) Effects of repeated applications of chlorimuron-ethyl on the soil microbial biomass, activity and microbial community in the greenhouse. Bull Environ Contam Toxicol 92:175–182. https://doi.org/10.1007/s00128-013-1156-7
Ye S et al (2017) Co-occurrence and interactions of pollutants, and their impacts on soil remediation—a review. Crit Rev Environ Sci Technol 47:1528–1553. https://doi.org/10.1080/10643389.2017.1386951
Zhang X, Li X, Zhang C, Li X, Zhang H (2011) Ecological risk of long-term chlorimuron-ethyl application to soil microbial community: an in situ investigation in a continuously cropped soybean field in Northeast China. Environ Sci Pollut Res 18:407–415
Zhang Q, Zhu L, Wang J, Xie H, Wang J, Wang F, Sun F (2014) Effects of fomesafen on soil enzyme activity, microbial population, and bacterial community composition. Environ Monit Assess 186:2801–2812. https://doi.org/10.1007/s10661-013-3581-9
Zhao S, Guo Y, Sheng Q, Shyr Y (2014) Advanced heat map and clustering analysis using Heatmap3. BioMed Res Int 2014:6. https://doi.org/10.1155/2014/986048
Acknowledgments
Authors would thank to Henrieta Blaškovičová, Daniela Košťálová and Silvia Kovácsová for their help in laboratory.
Funding
This work was supported by agency of Slovak Ministry of Education, grant nr. VEGA 1/0661/19.
Author information
Authors and Affiliations
Corresponding author
Additional information
Responsible editor: Robert Duran
Publisher’s note
Springer Nature remains neutral with regard to jurisdictional claims in published maps and institutional affiliations.
Rights and permissions
About this article
Cite this article
Medo, J., Hricáková, N., Maková, J. et al. Effects of sulfonylurea herbicides chlorsulfuron and sulfosulfuron on enzymatic activities and microbial communities in two agricultural soils. Environ Sci Pollut Res 27, 41265–41278 (2020). https://doi.org/10.1007/s11356-020-10063-0
Received:
Accepted:
Published:
Issue Date:
DOI: https://doi.org/10.1007/s11356-020-10063-0