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The effects of herbicide application on two soil phosphate solubilizing bacteria: Pantoea agglomerans and Serratia rubidaea

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The application of synthetic pesticides is one of the fastest acting tools at farmers' disposal to prevent and mitigate the threats posed by plant pests in agriculture. However, the effects of these above-ground applications of pesticides are known to be detrimental to some belowground, non-target soil biota. At present, the effects many pesticides have on key functional microbial groups associated with phosphate (P) solubilization in the soil are still largely unknown. The purpose of this study was to compare the effects of two herbicides, glyphosate, and paraquat, on phosphate solubilizing bacteria (PSB) with and without pH adjustment (after herbicide addition) since pH is a major indicator of P solubilization. In our assay, two PSB strains (Pantoea agglomerans and Serratia rubidaea) were chosen to assess their ability to solubilize tricalcium phosphate (TCP) by using the vanadate-molybdate method (to measure the amount of P solubilized) in the presence of glyphosate (5.4 g/L and 10.8 g/L) or paraquat (2 g/L and 4 g/L) separately. To assess the effect of PSB treated by the herbicides, a growth experiment using PSB inoculated wheat seedlings was performed under greenhouse conditions (25 °C, light 16 h/8 h dark). After four weeks, wheat above-ground growth parameters were measured. Our results showed that even under recommended doses of glyphosate (5.4 g/L) and paraquat (2 g/L), a decrease in P solubilization activity was observed in P. agglomerans and S. rubidaea. Whilst paraquat affected TCP solubilization more than glyphosate with and without pH adjustment, there was a significant decrease (p < 0.05) in TCP solubilization, up to 39% and 93% in the presence of glyphosate and paraquat, respectively, for S. rubidaea, and up to 45% and 95% in the presence of glyphosate and paraquat, respectively, for P. agglomerans. The effect of the herbicides on the PSB had the same results as in the greenhouse test on wheat seedling growth, confirming that these herbicides have both above and belowground negative effects, despite being used at recommended doses.

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References

  • Ahemad M, Khan M (2011a) Toxicological assessment of selective pesticides towards plant growth promoting activities of phosphate solubilizing Pseudomonas aeruginosa. Acta Microbiol Immunol Hung 58:169–187

    Article  CAS  Google Scholar 

  • Ahemad M, Khan MS (2011b) Effect of pesticides on plant growth promoting traits of greengram-symbiont, Bradyrhizobium sp. strain MRM6. Bull Environ Contam Toxicol 86:384–388

    Article  CAS  Google Scholar 

  • Ahemad M, Khan MS(2012) Effects of pesticides on plant growth promoting traits of Mesorhizobium strain MRC4. J Saudi Soc Agric Sci 11:63–71. https://doi.org/10.1016/j.jssas.2011.10.001

    Article  CAS  Google Scholar 

  • Ahemad M, Khan MS (2011c) Ecotoxicological assessment of pesticides towards the plant growth promoting activities of Lentil (Lens esculentus)-specific Rhizobium sp. strain MRL3. Ecotoxicology 20:661–669

    Article  CAS  Google Scholar 

  • Ahemad M, Kibret M (2014) Mechanisms and applications of plant growth promoting rhizobacteria: current perspective. J King Saud Univ - Sci 26:1–20. https://doi.org/10.1016/j.jksus.2013.05.001

    Article  Google Scholar 

  • Aliyat FZ, Maldani M, El Guilli M et al. (2022) Phosphate solubilizing bacteria isolated from phosphate solid sludge and their ability to solubilize three inorganic phosphate forms: calcium, iron, and aluminum phosphates. Microorganisms 10:980. https://doi.org/10.3390/microorganisms10050980

    Article  CAS  Google Scholar 

  • Anzuay MS, Ciancio MGR, Ludueña LM et al. (2017) Growth promotion of peanut (Arachis hypogaea L.) and maize (Zea mays L.) plants by single and mixed cultures of efficient phosphate solubilizing bacteria that are tolerant to abiotic stress and pesticides. Microbiol Res 199:98–109. https://doi.org/10.1016/j.micres.2017.03.006

    Article  CAS  Google Scholar 

  • Bajpai PD, Rao WVBS (1971) Phosphate solubilising bacteria: PART I. solubilisation of phosphate in liquid culture by selected bacteria as affected by different pH values. Soil Sci Plant Nutr 17:41–43

    Article  Google Scholar 

  • Bakker AW, Schippers B (1987) Microbial cyanide production in the rhizosphere in relation to potato yield reduction and Pseudomonas spp-mediated plant growth-stimulation. Soil Biol Biochem 19:451–457

    Article  CAS  Google Scholar 

  • Behera BC, Yadav H, Singh SK et al. (2017) Phosphate solubilization and acid phosphatase activity of Serratia sp. isolated from mangrove soil of Mahanadi river delta, Odisha, India. J Genet Eng Biotechnol 15:169–178

    Article  CAS  Google Scholar 

  • Bünemann EK (2015) Assessment of gross and net mineralization rates of soil organic phosphorus–a review. Soil Biol Biochem 89:82–98

    Article  Google Scholar 

  • Calvert GM, Karnik J, Mehler L et al. (2008) Acute pesticide poisoning among agricultural workers in the United States, 1998–2005. Am J Ind Med 51:883–898. https://doi.org/10.1002/ajim.20623

    Article  Google Scholar 

  • Castagno LN, Estrella MJ, Sannazzaro AI et al. (2011) Phosphate‐solubilization mechanism and in vitro plant growth promotion activity mediated by Pantoea eucalypti isolated from Lotus tenuis rhizosphere in the Salado River Basin (Argentina). J Appl Microbiol 110(5):1151–1165

    Article  CAS  Google Scholar 

  • Conde-Cid M, Paradelo R, Fernández-Calviño D et al. (2017) Retention of quaternary ammonium herbicides by acid vineyard soils with different organic matter and Cu contents. Geoderma 293:26–33. https://doi.org/10.1016/j.geoderma.2017.01.027

    Article  CAS  Google Scholar 

  • Dan X, Gao Z, Fu B et al. (2013) Effect of pyrimorph on soil enzymatic activities and respiration. Eur J Soil Biol 56:44–48

    Article  Google Scholar 

  • Das AC (2017) Microbial phosphate solubility as influenced by pyrethroid insecticide in tea soil of the Himalayan terai region of West Bengal. J Crop Weed 13:52–59

    Google Scholar 

  • Gauger WK, MacDonald JM, Adrian NR et al. (1986) Characterization of a streptomycete growing on organophosphate and carbamate insecticides. Arch Environ Contam Toxicol 15:137–141

    Article  CAS  Google Scholar 

  • Gaur AC, Rana JPS, others (1990) Effect of insecticides on wheat crop inoculated with phosphate solubilizing bacteria (PSB) and VAM fungi. In: Trends in mycorrhizal research. Proceedings of the National Conference on Mycorrhiza, held at Haryana Agricultural University, Hisar, India, Feb. 14–16, 1990

  • Gordon SA, Weber RP (1951) Colorimetric estimation of indoleacetic acid. Plant Physiol 26:192

    Article  CAS  Google Scholar 

  • Gyaneshwar P, Kumar GN, Parekh LJ, Poole PS (2002) Role of soil microorganisms in improving P nutrition of plants. Plant Soil 245:83–93

    Article  CAS  Google Scholar 

  • Harris JN, New PB, Martin PM (2006) Laboratory tests can predict beneficial effects of phosphate-solubilising bacteria on plants. Soil Biol. Biochem. 38(7):1521–1526

    Article  CAS  Google Scholar 

  • Joseph S, Jisha MS (2007) Selected pesticides inhibit phosphate solubilizing activity of Gluconacetobacter sp . and Burkholderia plantarii. Asian J Bio Sci 2:149–155

    Google Scholar 

  • Kalam A, Tah J, Mukherjee AK (2004) Pesticide effects on microbial population and soil enzyme activities during vermicomposting of agricultural waste. J Environ Biol 25:20–208.

    Google Scholar 

  • Kapoor K, Arora L (1996) Observations on growth responses of cyanobacteria under the influence of herbicides. Pollut Res 15:343–351

    CAS  Google Scholar 

  • Khan MS, Zaidi, A, Ahmad E (2014) Mechanism of phosphate solubilization and physiological functions of phosphate-solubilizing microorganisms. In: Khan M, Zaidi A, Musarrat J (eds) Phosphate solubilizing microorganisms. Springer, Cham. pp 31–62. https://doi.org/10.1007/978-3-319-08216-5_2

  • Khan S, Shahid M, Khan MS et al. (2020) Fungicide-tolerant plant growth-promoting rhizobacteria mitigate physiological disruption of white radish caused by fungicides used in the field cultivation. Int J Environ Res Public Health 17:7251

    Article  Google Scholar 

  • Kumar S, Stecher G, Tamura K (2016) MEGA7: molecular evolutionary genetics analysis version 7.0 for bigger datasets. Mol Biol Evol 33:1870–1874

    Article  CAS  Google Scholar 

  • Kumar V, Singh S, Upadhyay N (2019) Effects of organophosphate pesticides on siderophore producing soils microorganisms. Biocatal Agric Biotechnol 21:101359

    Article  Google Scholar 

  • Li W, Lybrand DB, Xu H et al. (2020) A trichome-specific, plastid-localized Tanacetum cinerariifolium Nudix protein hydrolyzes the natural pyrethrin pesticide biosynthetic intermediate trans-chrysanthemyl diphosphate. Front Plant Sci 11:482

    Article  Google Scholar 

  • López-Arredondo DL, Herrera-Estrella L (2012) Engineering phosphorus metabolism in plants to produce a dual fertilization and weed control system. Nat Biotechnol 30:889–893

    Article  Google Scholar 

  • Maldani M, Aliyat FZ, Ben Massaoud B et al. (2021) Effects of pesticides use (Glyphosate and Paraquat) on biological nitrogen fixation. Water Air Soil Pollut 323:10

    Google Scholar 

  • Maldani M, Ben Messaoud B, Nassiri L, Ibijbijen J (2018a) Influence of paraquat on four rhizobacteria strains: pantoea agglomerans, Rhizobium nepotum, Rhizobium radiobacter and Rhizobium tibeticum. Open Environ Sci 10:48–55. https://doi.org/10.2174/1876325101810010048

    Article  Google Scholar 

  • Maldani M, Messaoud BB, Nassiri, Laila I jamal (2018b) Assessment of the resistance of four nitrogen-fixing Bacteria to glyphosate. Atlas J Biol 546–550. https://doi.org/10.5147/ajb.v0i0.176.

  • Maldani M, Dekaki EM, Nassiri L et al(2017) State of art on the use of pesticides in Meknes region, Morocco. Am J Agric Biol Sci 4(6):138–148

    Google Scholar 

  • Murphy M, Riley JP (1962) A modified single solution method for the determination of phosphate in natural waters. Anal Chim Acta 27:31–36. https://doi.org/10.1016/S0003-2670(00)88444-5

    Article  CAS  Google Scholar 

  • Naik K, Mishra S, Srichandan H et al. (2019) Plant growth promoting microbes: potential link to sustainable agriculture and environment. Biocatal Agric Biotechnol 21:101326. https://doi.org/10.1016/j.bcab.2019.101326

    Article  Google Scholar 

  • Nasreen AN, Ustafa GM, Shfaq MA (2005) Mortality of Chrysoperla carnea (Stephens) (Neuroptera: Chrysopidae) after exposure to some insecticides; laboratory studies. South Pac Stud 26:1–6

    Google Scholar 

  • Nautiyal CS (1999) An effcient microbiological growth medium for screening phosphate solubilizing microorganisms. FEMS Microbiol Lett. 170 170:265–270

    Article  CAS  Google Scholar 

  • Panhwar QA, Jusop S, Naher UA et al. (2013) Application of potential phosphate-solubilizing bacteria and organic acids on phosphate solubilization from phosphate rock in aerobic rice. Sci World J 2013:1–10

    Article  Google Scholar 

  • Pateiro-Moure M, Nóvoa-Muñoz JC, Arias-Estévez M et al. (2009) Quaternary herbicides retention by the amendment of acid soils with a bentonite-based waste from wineries. J Hazard Mater 164:769–775. https://doi.org/10.1016/j.jhazmat.2008.08.071

    Article  CAS  Google Scholar 

  • Pham CH, Min J, Gu MB (2004) Pesticide induced toxicity and stress response in bacterial cells. Bull Environ Contam Toxicol 72:380–386

    Article  CAS  Google Scholar 

  • Plassard C, Robin A, LC E et al. (2015) Améliorer la biodisponibilité du phosphore: comment valoriser les compétences des plantes et les mécanismes biologiques du sol? Innov Agron 43:115–138

    Google Scholar 

  • Premono ME, Moawad AM, Vlek PLG (1996) Effect of phosphate-solubilizing Pseudomonas putida on the growth of maize and its survival in the rhizosphere. (No. REP-12113. CIMMYT.)

  • Ramani V (2011) Effect of pesticides on phosphate solubilization by Bacillus sphaericus and Pseudomonas cepacia. Pestic Biochem Physiol 99:232–236. https://doi.org/10.1016/j.pestbp.2011.01.001

    Article  CAS  Google Scholar 

  • Rashidipour M, Maleki A, Kordi S et al. (2019) Pectin/chitosan/tripolyphosphate nanoparticles: efficient carriers for reducing soil sorption, cytotoxicity, and mutagenicity of paraquat and enhancing its herbicide activity. J Agric Food Chem 67:5736–5745. https://doi.org/10.1021/acs.jafc.9b01106.

    Article  CAS  Google Scholar 

  • Rathore P (2014) chelation effect on phosphate solubilizing activity by Citrobacter freundii MTCC 6738. Int J Appl Nat Sci 3:103–108

    Google Scholar 

  • Roberts TR, Dyson JS, Lane MCG (2002) Deactivation of the biological activity of paraquat in the soil environment: a review of long-term environmental fate. J Agric Food Chem 50:3623–3631. https://doi.org/10.1021/jf011323x

    Article  CAS  Google Scholar 

  • Saitou N, Nei M (1987) The neighbor-joining method: a new method for reconstructing phylogenetic trees. Mol Biol Evol 4:406425

    Google Scholar 

  • Schwyn B, Neilands JB (1987) Universal chemical assay for the detection and determination of siderophores. Anal Biochem 160:47–56

    Article  CAS  Google Scholar 

  • Shafiani S, Malik A (2003) Tolerance of pesticides and antibiotic resistance in bacteria isolated from wastewater- irrigated soil. World J Microbiol Biotechnol 19:897–901

    Article  CAS  Google Scholar 

  • Shahid M, Khan MS (2018) Glyphosate induced toxicity to chickpea plants and stress alleviation by herbicide tolerant phosphate solubilizing Burkholderia cepacia PSBB1 carrying multifarious plant growth promoting activities. 3 Biotech 8:1–17.

    Article  Google Scholar 

  • Shahid M, Zaidi A, Ehtram A, Khan MS (2019) In vitro investigation to explore the toxicity of different groups of pesticides for an agronomically important rhizosphere isolate Azotobacter vinelandii. Pestic Biochem Physiol 157:33–44

    Article  CAS  Google Scholar 

  • Subhashree S, Adak T, Baran Bagchi TB et al. (2016) Effect of pretilachlor on soil enzyme activities in tropical rice soil. Bull Environ Contam Toxicol 98:439–445

    Google Scholar 

  • Talbot HW, Johnson LM, Munnecke DM (1984) Glyphosate utilization by Pseudomonas sp. and Alcaligenes sp. isolated from environmental sources. Curr Microbiol 10(5):255–259

    Article  CAS  Google Scholar 

  • Tang Z, Kong N, Ouyang J et al. (2020) Phosphorus science-oriented design and synthesis of multifunctional nanomaterials for biomedical applications. Matter 2(2):297–322

    Article  CAS  Google Scholar 

  • Thiour-mauprivez C, Martin-laurent F, Calvayrac C, Barthelmebs L (2019) Science of the total environment effects of herbicide on non-target microorganisms: towards a new class of biomarkers? Sci Total Environ 684:314–325. https://doi.org/10.1016/j.scitotenv.2019.05.230

    Article  CAS  Google Scholar 

  • Tripathi, S, Srivastava P, Devi RS, Bhadouria R (2020) Influence of synthetic fertilizers and pesticides on soil health and soil microbiology. In Agrochemicals detection, treatment and remediation. Butterworth-Heinemann. pp. 25–54

  • Tulabaev BD (1972) Effect of different doses of herbicides on microflora of sierozem-meadow soil of cotton crops. Uzbekskii Biologicheskii Zhurnal 14(1):11–14

    Google Scholar 

  • Wang C, Lin X, Li L et al. (2017) Glyphosate shapes a dinoflagellate-associated bacterial community while supporting algal growth as sole phosphorus source. Front microbiol 8:2530

    Article  Google Scholar 

  • Wassila R, Laval K, Laroche-Ajzenberg E et al. (2014) Effects of pesticides on soil enzymes: a review. Environ Chem Lett 12:257–273

    Article  Google Scholar 

  • Wickham H (2016) ggplot2: Elegant Graphics for Data Analysis. Springer-Verlag New York. Retrieved from https://ggplot2.tidyverse.org.

  • Yaohua H, Hui Z, Pankaj B et al. (2019) Paraquat degradation from contaminated environments: current achievements and perspectives. Frontiers in Microbiology 10:1754

    Article  Google Scholar 

  • Zhang F, Qiao Z, Yao C et al. (2021) Effects of the novel HPPD-inhibitor herbicide QYM201 on enzyme activity and microorganisms, and its degradation in soil. Ecotoxicology 30:80–90

    Article  CAS  Google Scholar 

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Acknowledgements

Our special thanks to the Environment & Soil Microbiology Unit, Department of Biology, Faculty of Sciences, Moulay Ismail University, Meknes, Morocco, and all those who helped us to accomplish this work. M.M was a recipient of a Ph.D. fellowship under the Erasmus + KA107 (2018-1-IT02-KA107-047799) Project at the University of Messina, Italy.

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Maldani, M., Aliyat, F.Z., Morabito, M. et al. The effects of herbicide application on two soil phosphate solubilizing bacteria: Pantoea agglomerans and Serratia rubidaea. Ecotoxicology 32, 720–735 (2023). https://doi.org/10.1007/s10646-023-02681-4

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