Soil pH mediates the impact of pesticides on bacterial communities, diversity, and abundance
Status PubMed-not-MEDLINE Jazyk angličtina Země Švýcarsko Médium electronic-ecollection
Typ dokumentu časopisecké články
PubMed
41623639
PubMed Central
PMC12858249
DOI
10.3389/fmicb.2025.1670425
Knihovny.cz E-zdroje
- Klíčová slova
- bacteria, diversity, fungicides, herbicides, real-time PCR, rhizobia,
- Publikační typ
- časopisecké články MeSH
INTRODUCTION: Pesticides are widely used in agriculture, yet their non-target effects on soil microbial communities remain poorly understood. This study investigates the short-term impact of five herbicides and three fungicides used for the protection of legumes on the composition and diversity of soil bacteria, with special focus on rhizobia. METHODS: Using three distinct soils from ecologically maintained fields, we assessed changes in bacterial communities and total bacterial abundance in response to different active substances under controlled conditions, 2 weeks after pesticide application. Bacterial diversity was analyzed by amplifying and sequencing the V4 region of the 16S rRNA gene via Illumina paired-end amplicon sequencing. Real-time PCR was used to assess total abundance of bacteria. RESULTS: Our results show that pesticide effects on bacteria are highly context-dependent, influenced significantly by soil and pH. Significant changes in bacterial diversity were detected only in one soil, whereas in another soil no significant differences among individual pesticides and the untreated control were found. In this soil, particularly the CORUM and pendimethalin-based products, Stomp 400 SC and Sharpen 40 SC, consistently reduced bacterial diversity, while some pesticides had a neutral effect. Rhizobial diversity remained largely unaffected, suggesting greater resilience compared to general bacterial communities. Regarding bacterial community composition, only some pesticides significantly affected bacterial community structure in each soil, and the pesticides showing this effect differed among soils. Redundancy analysis revealed that pH was a stronger driver of bacterial community structure than soil type or pesticide identity, explaining over 60% of community variability. CONCLUSION: These findings highlight the complex interactions between pesticides, soil characteristics, and microbial communities. Our results support considering soil pH when selecting pesticides to support sustainable soil management and minimize ecological disruption.
Czech Agrifood Research Center Prague Czechia
Faculty of Science J E Purkyně University in Ústí nad Labem České Mládeže Ústí nad Labem Czechia
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Adetutu E. M., Ball A. S., Osborn A. M. (2008). Azoxystrobin and soil interactions: degradation and impact on soil bacterial and fungal communities. J. Appl. Microbiol. 105, 1777–1790. doi: 10.1111/j.1365-2672.2008.03948.x, PubMed DOI
Afata T. N., Mekonen S., Sogn T. A., Pandey M. K., Janka E., Tucho G. T. (2024). Examining the effect of agrochemicals on soil microbiological activity, micronutrient availability, and uptake by maize ( DOI
Aioub A. A. A., Elesawy A. E., Ammar E. E. (2022). Plant growth promoting rhizobacteria (PGPR) and their role in plant-parasitic nematodes control: a fresh look at an old issue. J. Plant Dis. Prot. 129, 1305–1321. doi: 10.1007/s41348-022-00642-3 DOI
Akter S., Hulugalle N. R., Jasonsmith J., Strong C. L. (2023). Changes in soil microbial communities after exposure to neonicotinoids: a systematic review. Environ. Microbiol. Rep. 15, 431–444. doi: 10.1111/1758-2229.13193, PubMed DOI PMC
Al-Ani M. A. M., Hmoshi R. M., Kanaan I. A., Thanoon A. A. (2019). Effect of pesticides on soil microorganisms. J. Phys. Conf. Ser 1294:72007. doi: 10.1088/1742-6596/1294/7/072007 DOI
Alatassi G., Baysal Ö., Silme R. S., Örnek G. P., Örnek H., Can A. (2025). Pesticide degradation capacity of a novel strain belonging to Serratia sarumanii with its genomic profile. Biodegradation. doi: 10.1007/s10532-025-10144-2 PubMed DOI PMC
Allievi L., Gigliotti C., Salardi C., Valsecchi G., Brusa T., Ferrari A. (1996). Influence of the herbicide bentazon on soil microbial community. Microbiol. Res. 151, 105–111. doi: 10.1016/S0944-5013(96)80064-4, PubMed DOI
Ampe F., Omar N. B., Moizan C., Wacher C., Guyot J. P. (1999). Polyphasic study of the spatial distribution of microorganisms in Mexican pozol, a fermented maize dough, demonstrates the need for cultivation independent methods to investigate traditional fermentations. Appl. Environ. Microbiol. 65, 5464–5473. doi: 10.1128/AEM.65.12.5464-5473.1999, PubMed DOI PMC
Bradbury E. S., Holland-Moritz H., Gill A., Havrilla C. A. (2024). Plant and soil microbial composition legacies following indaziflam herbicide treatment. Front. Microbiol. 15:1450633. doi: 10.3389/fmicb.2024.1450633, PubMed DOI PMC
Bystrianský L., Hujslová M., Hršelová H., Řezáčová V., Němcová L., Šimsová J., et al. (2019). Observations on two microbial life strategies in soil: planktonic and biofilm-forming microorganisms are separable. Soil Biol. Biochem. 136:107535. doi: 10.1016/j.soilbio.2019.107535 DOI
Caporaso J. G., Lauber C. L., Walters W. A., Berg-Lyons D., Huntley J., Fierer N. (2012). Ultra-high-throughput microbial community analysis on the Illumina HiSeq and MiSeq platforms. ISME J. 6, 1621–1624. doi: 10.1038/ismej.2012.8, PubMed DOI PMC
Caporaso J. G., Lauber C. L., Walters W. A., Berg-Lyons D., Lozupone C. A., Turnbaugh P. J. (2011). Global patterns of 16S rRNA diversity at a depth of millions of sequences per sample. Proc. Natl. Acad. Sci. 108, 4516–4522. doi: 10.1073/pnas.1000080107, PubMed DOI PMC
Chang J., Shen F.-T., Lai W.-A., Liao C.-S., Chen W.-C. (2023). Co-exposure of dimethomorph and imidacloprid: effects on soil bacterial communities in vineyard soil. Front. Microbiol. 14:1249167. doi: 10.3389/fmicb.2023.1249167, PubMed DOI PMC
Chia X. K., Hadibarata T., Kristanti R. A. (2024). The function of microbial enzymes in breaking down soil contaminated with pesticides: a review. Bioprocess Biosyst. Eng. 47, 597–620. doi: 10.1007/s00449-024-02978-6, PubMed DOI PMC
Constancias F., Terrat S., Saby N. P., Horrigue W., Villerd J., Guillemin J. P., et al. (2015). Mapping and determinism of soil microbial community distribution across an agricultural landscape. Microbiology 4, 505–517. doi: 10.1002/mbo3.255, PubMed DOI PMC
Cook A. M. (1987). Biodegration of DOI
Daisley B. A., Smith M., Muter O., Gloor G. B., Reid G. (2022). Deteriorating microbiomes in agriculture – the unintended consequences of pesticide use. Front. Microbiol. 1: 6. doi: 10.20517/mrr.2021.08 PubMed DOI PMC
El-Sayed B. B., Moustafa E. S., Shoukry M. E., Waseem A. G. (2018). Biodegradation of organochlorine pesticides by DOI
Fierer N., Bradford M. A., Jackson R. B. (2007). Toward an ecological classification of soil bacteria. Ecology 88, 1354–1364. doi: 10.1890/05-1839, PubMed DOI
Fox J. E., Gulledge J., Engelhaupt E., Burow M. E., McLachlan J. A. (2007). Pesticides reduce symbiotic efficiency of nitrogen-fixing rhizobia and host plants. Biol. Sci. 104, 10282–10287. doi: 10.1073/pnas.0611710104, PubMed DOI PMC
Fuchs B., Saikkonen K., Damerau A., Yang B., Helander M. (2023). Herbicide residues in soil decrease microbe-mediated plant protection. Plant Biol. 25, 571–578. doi: 10.1111/plb.13517, PubMed DOI
Grady E. N., MacDonald J., Liu L., Richman A., Yuan Z. C. (2016). Current knowledge and perspectives of PubMed DOI PMC
Gundi V. A., Narasimha G., Reddy B. R. (2005). Interaction effects of insecticides on microbial populations and dehydrogenase activity in a black clay soil. J. Environ. Sci. Health 40, 269–283. doi: 10.1081/PFC-200045550, PubMed DOI
Hammer Ø., Harper D., Ryan P. (2001). PAST: paleontological statistics software package for education and data analysis. Palaeontol. Electron. 4, 1–9.
Hartmann M., Fliessbach A., Oberholzer H. R., Widmer F. (2006). Ranking the magnitude of crop and farming system effects on soil microbial biomass and genetic structure of bacterial communities. FEMS Microbiol. Ecol. 57, 378–388. doi: 10.1111/j.1574-6941.2006.00132.x, PubMed DOI
Hashem A., Tabassum B., Fathi A. E. (2019). PubMed DOI PMC
Hussain S., Siddique T., Saleem M., Arshad M., Khalid A. (2009). Chapter 5 impact of pesticides on soil microbial diversity, enzymes, and biochemical reactions. Adv. Agron. 102, 159–200. doi: 10.1016/S0065-2113(09)01005-0 DOI
Jeyaseelan A., Murugesan K., Thayanithi S., Palanisamy S. B. (2024). A review of the impact of herbicides and insecticides on the microbial communities. Environ. Res. 245:118020. doi: 10.1016/j.envres.2023.118020, PubMed DOI
Jongman R. H., ter Braak C. L. F., van Tongeren O. F. R. (1987). Data analysis in community and landscape ecology. Wageningen: Pudoc.
Khmelevtsova L., Konstantinova E., Karchava S., Klimova M., Azhogina T., Polienko E., et al. (2023). Influence of pesticides and mineral fertilizers on the bacterial community of arable soils under pea and chickpea crops. Agronomy 13:750. doi: 10.3390/agronomy13030750 DOI
Lehmann A., Zheng W., Rillig M. C. (2017). Soil biota contributions to soil aggregation. Nat. EcoL. Evol. 1, 1828–1835. doi: 10.1038/s41559-017-0344-y, PubMed DOI PMC
Lenoir I., Lounes-Hadj Sahraoui A., Fontaine J. (2016). Arbuscular mycorrhizal fungal-assisted phytoremediation of soil contaminated with persistent organic pollutants: a review. Eur. J. Soil Sci. 67, 624–640. doi: 10.1111/ejss.12375 DOI
Levy-Booth D. J., Campbell R. G., Gulden R. H., Hart M. M., Powell J. R., Klironomos J. N., et al. (2007). Cycling of extracellular DNA in the soil environment. Soil Biol. Biochem. 39, 2977–2991. doi: 10.1016/j.soilbio.2007.06.020 DOI
Lü X., Peng X. W., Hu Q., Ma A. Z., Jiang Z. P., Wei Y. (2013). Isolation of quizalofop-p-ethyl-degrading bacteria from soil by DGGE-colony in situ hybridization. Huan Jing Ke Xue 34, 263–270. PubMed
Lu J., Yang F., Wang S., Ma H., Liang J., Chen Y. (2017). Co-existence of rhizobia and diverse non-rhizobial bacteria in the rhizosphere and nodules of Dalbergia odorifera seedlings inoculated with PubMed DOI PMC
Ma Y., Suo Y., Qi H., Tang F., Wang M. (2024). Effects of rhizobium inoculation on rhizosphere soil microbial communities, physicochemical properties, and enzyme activities in caucasian clover under field conditions. Agronomy 14:2880. doi: 10.3390/agronomy14122880 DOI
Madigan M. T., Martinko J. M., Bender K. S., Buckley D. H., Stahl D. A. (2015). Brock biology of microorganisms. 14th Edn. London: Pearson Education.
Maino J. L., Thia J., Hoffmann A. A., Umina P. A. (2023). Estimating rates of pesticide usage from trends in herbicide, insecticide, and fungicide product registrations. Crop Prot. 163:106125. doi: 10.1016/j.cropro.2022.106125 DOI
Martínez-Toledo M. V., Salmerón V., Rodelas B., Pozo C., González-López J. (1998). Effects of the fungicide Captan on some functional groups of soil microflora. Appl. Soil Ecol. 7, 245–255. doi: 10.1016/S0929-1393(97)00026-7 DOI
Masson-Boivin C., Sachs J. L. (2018). Symbiotic nitrogen fixation by rhizobia—the roots of a success story. Curr. Opin. Plant Biol. 44, 7–15. doi: 10.1016/j.pbi.2017.12.001, PubMed DOI
Medo J., Maková J., Medová J., Lipková N., Cinkocki R., Omelka R., et al. (2021). Changes in soil microbial community and activity caused by application of dimethachlor and linuron. Sci. Rep. 11:12786. doi: 10.1038/s41598-021-91755-6, PubMed DOI PMC
Mehlich A. (1984). Mehlich 3 soil test extractant. A modification of the Mehlich 2 extractant. Commun. Soil Sci. Plant Anal. 15, 1409–1416. doi: 10.1080/00103628409367568 DOI
Meidl P., Lehmann A., Bi M., Breitenreiter C., Benkrama J., Li E., et al. (2024). Combined application of up to ten pesticides decreases key soil processes. Environ. Sci. Pol. 31, 11995–12004. doi: 10.1007/s11356-024-31836-x, PubMed DOI PMC
Muyzer G., de Wall E. C., Uitterlinden A. G. (1993). Profiling of complex microbial populations by denaturing gradient gel electrophoresis analysis of polymerase chain reaction-amplified genes coding for 16S rRNA. Appl. Environ. Microbiol. 59, 695–700. doi: 10.1128/aem.59.3.695-700.1993, PubMed DOI PMC
Nannipieri P., Ascher J., Ceccherini M. T., Landi L., Pietramellara G., Renella G. (2003). Microbial diversity and soil functions. Eur. J. Soil Sci. 54, 655–670. doi: 10.1046/j.1351-0754.2003.0556.x DOI
Ni B., Xiao L., Lin D., Zhang T.-L., Zhang Q., Liu Y., et al. (2025). Increasing pesticide diversity impairs soil microbial functions. Proc. Natl. Acad. Sci. USA 122:e2419917122. doi: 10.1073/pnas.2419917122, PubMed DOI PMC
Nielsen K. M., Johnsen P. J., Bensasson D., Daffonchio D. (2007). Release and persistence of extracellular DNA in the environment. Environ. Biosaf. Res. 6, 37–53. doi: 10.1051/ebr:2007031, PubMed DOI
Nikitin D. A., Semenov M. V., Chernov T. I., Ksenofontova N. A., Zhelezova A. D., Ivanova E. A., et al. (2022). Microbiological indicators of soil ecological functions: a review. Eurasian Soil Sci. 55, 221–234. doi: 10.1134/S1064229322020090 DOI
Onwona-Kwakye M., Plants-Paris K., Keita K., Lee J., Brink P. J. V.d., Hogarh J. N., et al. (2020). Pesticides decrease bacterial diversity and abundance of irrigated rice fields. Microorganisms 8:318. doi: 10.3390/microorganisms8030318, PubMed DOI PMC
Pagano M. C., Kyriakides M., Kuyper T. W. (2023). Effects of pesticides on the arbuscular mycorrhizal symbiosis. Agrochemicals 2, 337–354. doi: 10.3390/agrochemicals2020020 DOI
Paniagua-López M., Jiménez-Pelayo C., Gómez-Fernández G. O., Herrera-Cervera J. A., López-Gómez M. (2023). Reduction in the use of some herbicides favors nitrogen fixation efficiency in PubMed DOI PMC
Peña B., Hilber I., Sosa D., Escobar A. C., Bucheli T. D. (2025). Extended pesticide soil monitoring in Cuban potato ( PubMed DOI PMC
Pietramellara G., Ascher J., Borgogni F., Ceccherini M. T., Guerri G., Nannipieri P. (2009). Extracellular DNA in soil and sediment: fate and ecological relevance. Biol. Fertil. Soils 45, 219–235. doi: 10.1007/s00374-008-0345-8 DOI
Qurashi A. W., Sabri A. N. (2012). Bacterial exopolysaccharide and biofilm formation stimulate chickpea growth and soil aggregation under salt stress. Braz. J. Microbiol. 43, 1183–1191. doi: 10.1590/S1517-838220120003000046, PubMed DOI PMC
R Core Team , 2022. R: A language and environment for statistical computing. Available online at: https://www.R-project.org/ (Accessed 9 September, 2022).
Řezáčová V., Czakó A., Stehlík M., Mayerová M., Šimon T., Smatanová M., et al. (2021a). Organic fertilization improves soil aggregation through increases in abundance of eubacteria and products of arbuscular mycorrhizal fungi. Sci. Rep. 11:12548. doi: 10.1038/s41598-021-91653-x, PubMed DOI PMC
Řezáčová V., Némethová E., Stehlíková I., Czakó A., Gryndler M. (2023). Arbuscular mycorrhizal fungus DOI
Řezáčová V., Řezáč M., Gryndler M., Hršelová H., Gryndlerová H., Michalová T. (2021c). Plant invasion alters community structure and decreases diversity of arbuscular mycorrhizal fungal communities. Appl. Soil Ecol. 167:104039. doi: 10.1016/j.apsoil.2021.104039 DOI
Řezáčová V., Řezáč M., Líblová Z., Michalová T., Heneberg P. (2021b). Stable colonization of native plants and early invaders by arbuscular mycorrhizal fungi after exposure to recent invaders from the Asteraceae family. Invasive Plant Sci. Manag. 14, 147–155. doi: 10.1017/inp.2021.17 DOI
Řezáčová V., Slavíková R., Konvalinková T., Zemková L., Řezáč M., Gryndler M., et al. (2019). Geography and habitat predominate over climate influences on arbuscular mycorrhizal fungal communities of mid-European meadows. Mycorrhiza 29, 567–579. doi: 10.1007/s00572-019-00921-2, PubMed DOI
Saha J., Chowdhury A., Chaudhuri S. (1991). Stimulation of heterotrophic dinitrogen fixation in barley root association by the herbicide pendimethalin and its metabolic transformation by Azotobacter spp. Soil Biology and Biochemistry, 23, 569–573.
Santos A., Flores M. (1995). Effects of glyphosate on nitrogen fixation of free-living heterotrophic bacteria. Lett. Appl. Microbiol. 20, 349–352. doi: 10.1111/j.1472-765X.1995.tb01318.x DOI
Senabio J. A., da Silva R. C., Pinheiro D. G., de Vasconcelos L. G., Soares M. A. (2024). The pesticides carbofuran and picloram alter the diversity and abundance of soil microbial communities. PLoS One 19:e0314492. doi: 10.1371/journal.pone.0314492, PubMed DOI PMC
Sim J. X. F., Drigo B., Doolette C. L., Vasileiadis S., Karpouzas D. G., Lombi E. (2022). Impact of twenty pesticides on soil carbon microbial functions and community composition. Chemosphere 307:135820. doi: 10.1016/j.chemosphere.2022.135820, PubMed DOI
Stanley H., Maduike E., Okerentugba P. (2013). Effect of herbicide (atrazine and paraquat) application on soil bacterial population. Sky J. Soil Sci. Envir. Mana. 2, 101–105.
Strandberg M., Scott-Fordsmand J. J. (2004). Effects of pendimethalin at lower trophic levels-a review. Ecotoxicol. Environ. Saf. 57, 190–201. doi: 10.1016/j.ecoenv.2003.07.010, PubMed DOI
ter Braak C. J. F., Šmilauer P. (2018). Canoco reference manual and user’s guide: Software for ordination (version 5.10). Wageningen: Biometris Wageningen University & Research.
Tripathi B. M., Stegen J. C., Kim M., Dong K., Adams J. M., Lee Y. K. (2018). Soil pH mediates the balance between stochastic and deterministic assembly of bacteria. ISME J. 12, 1072–1083. doi: 10.1038/s41396-018-0082-4, PubMed DOI PMC
Vainberg S., McClay K., Masuda H., Root D., Condee C., Zylstra G. J., et al. (2006). Biodegradation of ether pollutants by PubMed DOI PMC
Větrovský T., Baldrian P., Morais D. (2018). SEED 2: a user-friendly platform for amplicon high-throughput sequencing data analyses. Bioinformatics 34, 2292–2294. doi: 10.1093/bioinformatics/bty071, PubMed DOI PMC
Wan N. F., Fu L., Dainese M., Kiær L. P., Hu Y. Q., Xin F., et al. (2025). Pesticides have negative effects on non-target organisms. Nat. Commun. 16:1360. doi: 10.1038/s41467-025-56732-x, PubMed DOI PMC
Wan W., Tan J., Wang Y., Qin Y., He H., Wu H., et al. (2020). Responses of the rhizosphere bacterial community in acidic crop soil to pH: changes in diversity, composition, interaction, and function. Sci. Total Environ. 700:134418. doi: 10.1016/j.scitotenv.2019.134418, PubMed DOI
Wang X., Lu Z., Miller H., Liu J., Hou Z., Liang S., et al. (2020). Fungicide azoxystrobin induced changes on the soil microbiome. Appl. Soil Ecol. 145:103343. doi: 10.1016/j.apsoil.2019.08.005 DOI
Wang H., Ren W., Xu Y., Wang X., Ma J., Sun Y., et al. (2024). Long-term herbicide residues affect soil multifunctionality and the soil microbial community. Ecotoxicol. Environ. Saf. 283:116783. doi: 10.1016/j.ecoenv.2024.116783, PubMed DOI
Wang Z., Zhao F., Zhai W., Yi X., Guo H., Liang Y., et al., 2023. Saline-alkaline stress altered pesticide persistence in soil: insight from soil bacterial community. Available online at SSRN: https://ssrn.com/abstract=4755816 or 10.2139/ssrn.4755816 DOI
Xia Q., Rufty T., Shi W. (2020). Soil microbial diversity and composition: links to soil texture and associated properties. Soil Biol. Biochem. 149:107953. doi: 10.1016/j.soilbio.2020.107953 DOI
Xiong R., He X., Gao N., Li Q., Qiu Z., Hou Y., et al. (2024). Soil pH amendment alters the abundance, diversity, and composition of microbial communities in two contrasting agricultural soils. Microbiol. Spectr. 12, e0416523–e0416523. doi: 10.1128/spectrum.04165-23, PubMed DOI PMC
Yu Z., Lu T., Qian H. (2023). Pesticide interference and additional effects on plant microbiomes. Sci. Total Environ. 888:164149. doi: 10.1016/j.scitotenv.2023.164149, PubMed DOI
Zhou X., He Z., Liang Z., Stoffella P. J., Fan J., Yang Y., et al. (2011). Long-term use of copper-containing fungicide affects microbial properties of citrus grove soils. Soil Sci. Soc. Am. J. 75, 898–906. doi: 10.2136/sssaj2010.0321 DOI