The effect of natural products used as pesticides on the soil microbiota: OECD 216 nitrogen transformation test fails to identify effects that were detected via q-PCR microbial abundance measurement.

OECD 216 test natural products pesticides ecotoxicity soil microorganisms

Journal

Pest management science
ISSN: 1526-4998
Titre abrégé: Pest Manag Sci
Pays: England
ID NLM: 100898744

Informations de publication

Date de publication:
20 Jan 2024
Historique:
revised: 23 12 2023
received: 22 09 2023
accepted: 02 01 2024
medline: 20 1 2024
pubmed: 20 1 2024
entrez: 20 1 2024
Statut: aheadofprint

Résumé

Natural products present an environmentally attractive alternative to synthetic pesticides which have been implicated in the off-target effect. Currently, the assessment of pesticide toxicity on soil microorganisms relies on the OECD 216 N transformation assay (OECD stands for the Organisation Economic Co-operation and Development, which is a key international standard-setting organisation). We tested the hypotheses that (i) the OECD 216 assay fails to identify unacceptable effects of pesticides on soil microbiota compared to more advanced molecular and standardized tests, and (ii) the natural products tested (dihydrochalcone, isoflavone, aliphatic phenol, and spinosad) are less toxic to soil microbiota compared to a synthetic pesticide compound (3,5-dichloraniline). We determined the following in three different soils: (i) ammonium (NH All pesticides tested exhibited limited persistence, with spinosad demonstrating the highest persistence. None of the pesticides tested showed clear dose-dependent effects on NH Our findings strongly advocate for a revision of the current regulatory framework regarding the toxicity of pesticides to soil microbiota, which should integrate advanced and well-standardized tools. © 2024 The Authors. Pest Management Science published by John Wiley & Sons Ltd on behalf of Society of Chemical Industry.

Sections du résumé

BACKGROUND BACKGROUND
Natural products present an environmentally attractive alternative to synthetic pesticides which have been implicated in the off-target effect. Currently, the assessment of pesticide toxicity on soil microorganisms relies on the OECD 216 N transformation assay (OECD stands for the Organisation Economic Co-operation and Development, which is a key international standard-setting organisation). We tested the hypotheses that (i) the OECD 216 assay fails to identify unacceptable effects of pesticides on soil microbiota compared to more advanced molecular and standardized tests, and (ii) the natural products tested (dihydrochalcone, isoflavone, aliphatic phenol, and spinosad) are less toxic to soil microbiota compared to a synthetic pesticide compound (3,5-dichloraniline). We determined the following in three different soils: (i) ammonium (NH
RESULTS RESULTS
All pesticides tested exhibited limited persistence, with spinosad demonstrating the highest persistence. None of the pesticides tested showed clear dose-dependent effects on NH
CONCLUSION CONCLUSIONS
Our findings strongly advocate for a revision of the current regulatory framework regarding the toxicity of pesticides to soil microbiota, which should integrate advanced and well-standardized tools. © 2024 The Authors. Pest Management Science published by John Wiley & Sons Ltd on behalf of Society of Chemical Industry.

Identifiants

pubmed: 38243771
doi: 10.1002/ps.7961
doi:

Types de publication

Journal Article

Langues

eng

Sous-ensembles de citation

IM

Subventions

Organisme : European Commission
Organisme : H2020-ITN-EID-MSCA project ARISTO
ID : 956496

Informations de copyright

© 2024 The Authors. Pest Management Science published by John Wiley & Sons Ltd on behalf of Society of Chemical Industry.

Références

Rasool S, Rasool T and Gani KM, A review of interactions of pesticides within various interfaces of intrinsic and organic residue amended soil environment. Chem Eng J Adv 11:100301 (2022).
Storck V, Karpouzas DG and Martin-Laurent F, Towards a better pesticide policy for the European Union. Sci Total Environ 575:1027-1033 (2017).
Rani L, Thapa K, Kanojia N, Sharma N, Singh S, Grewal AS et al., An extensive review on the consequences of chemical pesticides on human health and environment. J Clean Prod 283:124657 (2021).
Karpouzas DG, Papadopoulou E, Ipsilantis I, Friedel I, Petric I, Udikovic-Kolic N et al., 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 (2014).
Silva V, Mol HGJ, Zomer P, Tienstra M, Ritsema CJ and Geissen V, Pesticide residues in European agricultural soils-a hidden reality unfolded. Sci Total Environ 653:1532-1545 (2019).
Pietrzak D, Kania J, Malina G, Kmiecik E and Wątor K, Pesticides from the EU first and second watch lists in the water environment. Clean-Soil, Air, Water 47:1800376 (2019).
Karas PA, Baguelin C, Pertile G, Papadopoulou ES, Nikolaki S, Storck V et al., Assessment of the impact of three pesticides on microbial dynamics and functions in a lab-to-field experimental approach. Sci Total Environ 637:636-646 (2018).
Katsoula A, Vasileiadis S, Sapountzi M and Karpouzas DG, The response of soil and phyllosphere microbial communities to repeated application of the fungicide iprodione: accelerated biodegradation or toxicity? FEMS Microbiol Ecol 96:fiaa056 (2020).
Sim JX, Drigo B, Doolette CL, Vasileiadis S, Karpouzas DG and Lombi E, Impact of twenty pesticides on soil carbon microbial functions and community composition. Chemosphere 307:135820 (2022).
Arakere UC, Jagannath S, Krishnamurthy S, Chowdappa S and Konappa N, Microbial bio-pesticide as sustainable solution for management of pests: achievements and prospects. Biopesticides 2:183-200 (2022).
Acheuk F, Basiouni S, Shehata AA, Dick K, Hajri H, Lasram S et al., Status and prospects of botanical biopesticides in Europe and Mediterranean countries. Biomolecules 12:311 (2022).
Horikoshi R, Goto K, Mitomi M, Oyama K, Sunazuka T and Ōmura S, Identification of pyripyropene a as a promising insecticidal compound in a microbial metabolite screening. J Antibiot 70:272-276 (2017).
Keswani C, Singh HB, García-Estrada C, Caradus J, He YW, Mezaache-Aichour S et al., Antimicrobial secondary metabolites from agriculturally important bacteria as next-generation pesticides. Appl Microbiol Biotechnol 104:1013-1034 (2020).
Riviere C, Dihydrochalcones: occurrence in the plant kingdom, chemistry and biological activities. Stud Nat Prod Chem 51:253-381 (2016).
Cárdenas-Laverde D, Barbosa-Cornelio R and Coy-Barrera E, Antifungal activity against Fusarium oxysporum of botanical end-products: an integration of chemical composition and antifungal activity datasets to identify antifungal bioactives. Plan Theory 10:2563 (2021).
Ingham JL, Tahara S and Harborne JB, Fungitoxic isoflavones from Lupinus albus and other Lupinus species. Z Naturforsch C 38:194-200 (1983).
Olea AF, Rubio J, Sedan C, Carvajal D, Nuñez M, Espinoza L et al., Antifungal activity of 2-allylphenol derivatives on the Botrytis cinerea strain: assessment of possible action mechanism. Int J Mol Sci 24:6530 (2023).
Thompson GD, Dutton R and Sparks TC, Spinosad-a case study: an example from a natural products discovery programme. Pest Manag Sci 56:696-702 (2000).
Badri DV, Chaparro JM, Zhang R, Shen Q and Vivanco JM, Application of natural blends of phytochemicals derived from the root exudates of Arabidopsis to the soil reveal that phenolic-related compounds predominantly modulate the soil microbiome. J Biol Chem 288:4502-4512 (2013).
Spyrou IM, Karpouzas DG and Menkissoglu-Spiroudi U, Do botanical pesticides alter the structure of the soil microbial community? Microb Ecol 58:715-727 (2009).
Selim S, Martin-Laurent F, Rouard N, Gianinazzi S and Van Tuinen D, Impact of a new biopesticide produced by Paenibacillus sp. strain B2 on the genetic structure and density of soil bacterial communities. Pest Manag Sci 63:269-275 (2007).
Ipsilantis I, Samourelis C and Karpouzas DG, The impact of biological pesticides on arbuscular mycorrhizal fungi. Soil Biol Biochem 45:147-155 (2012).
Pino-Otín MR, Val J, Ballestero D, Navarro E, Sánchez E, González-Coloma A et al., Ecotoxicity of a new biopesticide produced by Lavandula luisieri on non-target soil organisms from different trophic levels. Sci Total Environ 671:83-93 (2019).
Singh S, Gupta R, Kumari M and Sharma S, Nontarget effects of chemical pesticides and biological pesticide on rhizospheric microbial community structure and function in Vigna radiata. Environ Sci Pollut Res 22:11290-11300 (2015).
Van Der Heijden MG, Bardgett RD and Van Straalen NM, The unseen majority: soil microbes as drivers of plant diversity and productivity in terrestrial ecosystems. Ecol Lett 11:296-310 (2008).
Timmis K and Ramos JL, The soil crisis: the need to treat as a global health problem and the pivotal role of microbes in prophylaxis and therapy. J Microbial Biotechnol 14:769-797 (2021).
Fernández-Calviño D, Rousk J, Bååth E, Bollmann UE, Bester K and Brandt KK, Short-term toxicity assessment of a triazine herbicide (terbutryn) underestimates the sensitivity of soil microorganisms. Soil Biol Biochem 154:108130 (2021).
OECD, 216, OECD Guideline for the Testing of Chemicals. Test No. 216: Soil Microorganisms: Nitrogen Transformation Test. Organisation for Economic Co-operation and Development, Paris, Paris (2000).
Karpouzas DG, Assessing the effects of pesticides on the soil microbial community: advances, standardization of methods and the need for a new regulatory framework, in Pesticides in Soils: Occurrence, Fate, Control and Remediation, ed. by Rodríguez-Cruz MS and Sánchez-Martín MJ. Cham, Springer, pp. 81-105 (2021).
Thiour-Mauprivez C, Martin-Laurent F, Calvayrac C and Barthelmebs L, Effects of herbicide on non-target microorganisms: towards a new class of biomarkers? Sci Total Environ 684:314-325 (2019).
EFSA Panel on Plant Protection Products and their Residues (PPR), Ockleford C, Adriaanse P, Berny P, Brock T, Duquesne S et al., Scientific opinion addressing the state of the science on risk assessment of plant protection products for in-soil organisms. EFSA J 15:e04690 (2017).
Karpouzas DG, Vryzas Z and Martin-Laurent F, Pesticide soil microbial toxicity: setting the scene for a new pesticide risk assessment for soil microorganisms (IUPAC technical report). Pure Appl Chem 94:1161-1194 (2022).
ISO 17601, Soil quality - Estimation of abundance of selected microbial gene sequences by quantitative real time PCR from DNA directly extracted from soil Geneva (2016).
Karpouzas DG, Tsiamis G, Trevisan M, Ferrari F, Malandain C, Sibourg O et al., "LOVE TO HATE" pesticides: felicity or curse for the soil microbial community? An FP7 IAPP Marie curie project aiming to establish tools for the assessment of the mechanisms controlling the interactions of pesticides with soil microorganisms. Environ Sci Pollut Res 23:18947-18951 (2016).
Silva MCP, Semenov AV, Schmitt H, van Elsas JD and Salles JF, Microbe-mediated processes as indicators to establish the normal operating range of soil functioning. Soil Biol Biochem 57:995-1002 (2013).
Alves RJE, Minh BQ, Urich T, von Haeseler A and Schleper C, Unifying the global phylogeny and environmental distribution of ammonia-oxidising archaea based on amoA genes. Nat Commun 9:1517 (2018).
Abell GC, Robert SS, Frampton DM, Volkman JK, Rizwi F, Csontos J et al., High-throughput analysis of ammonia oxidizer community composition via a novel, amoA-based functional gene array. PloS One 7:e51542 (2012).
Daims H, Lebedeva EV, Pjevac P, Han P, Herbold C, Albertsen M et al., Complete nitrification by Nitrospira bacteria. Nature 528:504-509 (2015).
Liu T, Wang Z, Wang S, Zhao Y, Wright AL and Jiang X, Responses of ammonia-oxidizers and comammox to different long-term fertilization regimes in a subtropical paddy soil. Eur J Soil Biol 93:103087 (2019).
Orellana LH, Chee-Sanford JC, Sanford RA, Löffler FE and Konstantinidis KT, Year-round shotgun metagenomes reveal stable microbial communities in agricultural soils and novel ammonia oxidizers responding to fertilization. Appl Environ Microbiol 84:e01646-e01717 (2018).
Prosser JI, Hink L, Gubry-Rangin C and Nicol GW, Nitrous oxide production by ammonia oxidizers: physiological diversity, niche differentiation and potential mitigation strategies. Glob Change Biol 26:103-118 (2020).
Domsch KH, Interactions of Soil Microbes and Pesticides. Symp Biol Hun 11:337 (1972).
Fang W, Wang X, Huang B, Zhang D, Liu J, Zhu J et al., Comparative analysis of the effects of five soil fumigants on the abundance of denitrifying microbes and changes in bacterial community composition. Ecotoxicol Environ Saf 187:109850 (2020).
Feld L, Hjelmsø MH, Nielsen MS, Jacobsen AD, Rønn R, Ekelund F et al., Pesticide side effects in an agricultural soil ecosystem as measured by amoA expression quantification and bacterial diversity changes. PloS One 10:e0126080 (2015).
Puglisi E, Vasileiadis S, Demiris K, Bassi D, Karpouzas DG, Capri E et al., Impact of fungicides on the diversity and function of non-target ammonia-oxidizing microorganisms residing in a litter soil cover. Microb Ecol 64:692-701 (2012).
Vasileiadis S, Puglisi E, Papadopoulou ES, Pertile G, Suciu N, Pappolla RA et al., Blame it on the metabolite: 3,5-dichloroaniline rather than the parent compound is responsible for the decreasing diversity and function of soil microorganisms. Appl Environ Microbiol 84:e01536-e01618 (2018).
Gopal M, Gupta A, Arunachalam V and Magu SP, Impact of azadirachtin, an insecticidal allelochemical from neem on soil microflora, enzyme and respiratory activities. Bioresour Technol 98:3154-3158 (2007).
ISO 10381-6, Soil Quality - Sampling - Part 6: Guidance on the Collection, Handling and Storage of Soil Under Aerobic Conditions for the Assessment of Microbiological Processes, Biomass and Diversity in the Laboratory Geneva (2009).
FOCUS, Forum for the Coordination of pesticide fate models and their use, Generic Guidance for Tier 1 FOCUS Ground Water Assessments pp 66 (2014).
Kandeler E and Gerber H, Short-term assay of soil urease activity using colorimetric determination of ammonium. Biol Fertil Soils 6:68-72 (1988).
Doane TA and Horwáth WR, Spectrophotometric determination of nitrate with a single reagent. Anal Lett 36:2713-2722 (2003).
Asensio-Ramos M, Hernández-Borges J, Ravelo-Pérez LM and Rodriguez-Delgado MA, Evaluation of a modified QuEChERS method for the extraction of pesticides from agricultural, ornamental, and forestal soils. Anal Bioanal Chem 396:2307-2319 (2010).
Fierer N, Jackson JA, Vilgalys R and Jackson RB, Assessment of soil microbial community structure by use of taxon-specific quantitative PCR assays. Appl Environ Microbiol 71:4117-4120 (2005).
White TJ, Bruns T, Lee SJWT and Taylor J, Amplification and direct sequencing of fungal ribosomal RNA genes for phylogenetics, in PCR protocols: A guide to methods and applications, (eds). Innis MA, Gelfand DH, Sninsky JJ and White TJ. Academic Press, Inc., New York, Vol. 18, pp. 315-322 (1990).
Francis CA, Roberts KJ, Beman JM, Santoro AE and Oakley BB, Ubiquity and diversity of ammonia-oxidizing archaea in water columns and sediments of the ocean. Proc Natl Acad Sci USA 102:14683-14688 (2005).
Rotthauwe JH, Witzel KP and Liesack W, The ammonia monooxygenase structural gene amoA as a functional marker: molecular fine-scale analysis of natural ammonia-oxidizing populations. Appl Environ Microbiol 63:4704-4712 (1997).
FOCUS, Guidance document on estimating persistence and degradation kinetics from environmental fate studies on pesticides in EU registration, Report of the FOCUS Work Group on Degradation Kinetics, EC Document Reference Sanco/10058/ 2005 version 2.0 pp. 434 (2006).
Ranke J, Lindenberger K and Lehmann R, mkin: Kinetic Evaluation of Chemical Degradation Data. R package version 0.9 (2018).
Alonso-Gato M, Astray G, Mejuto JC and Simal-Gandara J, Essential oils as antimicrobials in crop protection. Antibiotics 10:34 (2021).
Adak T and Mukherjee I, Investigating role of abiotic factors on spinosad dissipation. Bull Environ Contam Toxicol 96:125-129 (2016).
De Bernardi A, Marini E, Casucci C, Tiano L, Marcheggiani F, Ciani M et al., Ecotoxicological effects of a synthetic and a natural insecticide on earthworms and soil bacterial community. Environ Adv 8:100225 (2022).
Hale KA and Portwood DE, The aerobic soil degradation of spinosad - a novel natural insect control agent. J Environ Sci Health B 31:477-484 (1996).
Telesiński A, Michalcewicz W, Płatkowski M, Stręk M, Onyszko M and Wiśniewska J, The side-effect of organic insecticide spinosad on biochemical and microbiological properties of clay soil. J Ecol Eng 16:191-197 (2015).
Fogg P, Boxall AB and Walker A, Degradation of pesticides in biobeds: the effect of concentration and pesticide mixtures. J Agric Food Chem 51:5344-5349 (2003).
Papazlatani CV, Karas PA, Tucat G and Karpouzas DG, Expanding the use of biobeds: degradation and adsorption of pesticides contained in effluents from seed-coating, bulb disinfestation and fruit-packaging activities. J Environ Manage 248:109221 (2019).
Pantelelis I, Karpouzas DG, Menkissoglu-Spiroudi U and Tsiropoulos N, Influence of soil physicochemical and biological properties on the degradation and adsorption of the nematicide fosthiazate. J Agric Food Chem 54:6783-6789 (2006).
Walker A, Jurado-Exposito M, Bending GD and Smith VJR, Spatial variability in the degradation rate of isoproturon in soil. Environ Pollut 111:407-415 (2001).
Kaur R, Singh D, Kumari A, Sharma G, Rajput S, Arora S et al., Pesticide residues degradation strategies in soil and water: a review. Int J Environ Sci Technol 20:3537-3560 (2023).
Xu Z, Zhang T, Wang S and Wang Z, Soil pH and C/N ratio determines spatial variations in soil microbial communities and enzymatic activities of the agricultural ecosystems in Northeast China: Jilin Province case. Appl Soil Ecol 155:103629 (2020).
Delgado-Baquerizo M, Oliverio AM, Brewer TE, Benavent-González A, Eldridge DJ, Bardgett RD et al., A global atlas of the dominant bacteria found in soil. Science 359:320-325 (2018).
Fierer N, Embracing the unknown: disentangling the complexities of the soil microbiome. Nat Rev Microbiol 15:579-590 (2017).
Chaplain V, Mamy L, Vieublé L, Mougin C, Benoit P, Barriuso E et al., Fate of pesticides in soils: Toward an integrated approach of influential factors. Pesticides in the modern world - Risks and benefits 29:535-560 (2011).
Rice PJ, Koskinen WC and Carrizosa MJ, Effect of soil properties on the degradation of isoxaflutole and the sorption−desorption of isoxaflutole and its diketonitrile degradate. J Agric Food Chem 52:7621-7627 (2004).
Asl RMZ, Niakousari M, Gahruie HH, Saharkhiz MJ and Khaneghah AM, Study of two-stage ohmic hydro-extraction of essential oil from Artemisia aucheri Boiss.: antioxidant and antimicrobial characteristics. Food Res Int 107:462-469 (2018).
Tu XF, Hu F, Thakur K, Li XL, Zhang YS and Wei ZJ, Comparison of antibacterial effects and fumigant toxicity of essential oils extracted from different plants. Ind Crops Prod 124:192-200 (2018).
Mohiddin GJ, Srinivasulu M, Subramanyam K, Madakka M, Meghana D and Rangaswamy V, Influence of insecticides flubendiamide and spinosad on biological activities in tropical black and red clay soils. 3 Biotech 5:13-21 (2015).
Zhang M, Wang W, Bai SH, Zhou X, Teng Y and Xu Z, Antagonistic effects of nitrification inhibitor 3, 4-dimethylpyrazole phosphate and fungicide iprodione on net nitrification in an agricultural soil. Soil Biol Biochem 116:167-170 (2018).
Papadopoulou ES, Tsachidou B, Sułowicz S, Menkissoglu-Spiroudi U and Karpouzas DG, Land spreading of wastewaters from the fruit-packaging industry and potential effects on soil microbes: effects of the antioxidant ethoxyquin and its metabolites on ammonia oxidizers. Appl Environ Microbiol 82:747-755 (2016).

Auteurs

Alexandre Pedrinho (A)

Department of Biochemistry and Biotechnology, Laboratory of Plant and Environmental Biotechnology, University of Thessaly, Larissa, Greece.
Metabolic Insights Ltd, Ness Ziona, Israel.

Panagiotis A Karas (PA)

Department of Biochemistry and Biotechnology, Laboratory of Plant and Environmental Biotechnology, University of Thessaly, Larissa, Greece.

Alexandros Kanellopoulos (A)

Department of Biochemistry and Biotechnology, Laboratory of Plant and Environmental Biotechnology, University of Thessaly, Larissa, Greece.

Emma Feray (E)

Department of Biochemistry and Biotechnology, Laboratory of Plant and Environmental Biotechnology, University of Thessaly, Larissa, Greece.
National Museum of Natural History, Paris, France.

Ido Korman (I)

Metabolic Insights Ltd, Ness Ziona, Israel.

Gal Wittenberg (G)

Metabolic Insights Ltd, Ness Ziona, Israel.

Ofir Ramot (O)

Metabolic Insights Ltd, Ness Ziona, Israel.

Dimitrios G Karpouzas (DG)

Department of Biochemistry and Biotechnology, Laboratory of Plant and Environmental Biotechnology, University of Thessaly, Larissa, Greece.

Classifications MeSH