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Effects of Pesticides Use (Glyphosate & Paraquat) on Biological Nitrogen Fixation

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Abstract

Pesticide usage is becoming increasingly necessary to escalate agricultural productivity and meet food production needs. However, it harms in different degrees all living organisms, plants, and animals, whether terrestrial or aquatic. Soil microorganisms, are microbes belonging to microorganisms, are the first to be specifically affected by pesticides. This study aims to evaluate the impact of two herbicides, paraquat and glyphosate, on symbiotic nitrogen-fixing bacteria. Our study was carried out in the greenhouse. Bituminaria bituminosa plants were inoculated with four different nitrogen-fixing bacteria, Pantoea agglomerans, Rhizobium nepotum, Rhizobium radiobacter, and Rhizobium tibeticum, and then treated with varying herbicide concentrations were selected according to the doses recommended by the National Office of Food Safety (ONSSA) and according to a survey conducted among farmers in the Meknes region-Morocco, (0.05, 0.1, 5.4, 10.8 g/L glyphosate and 0.05, 0.1, 2, 4 g/L paraquat). After 6 months after sowing, the following parameters were evaluated: nodule number, nodule mass, nodule weight, nodule dry, and fresh weight, nitrogen content, and symbiotic efficiency. At higher doses (5.4, 10.8 g/L for glyphosate and 2, 4 g/L for paraquat), both herbicides decreased the number and the size of nodules, the weight of nodules, nitrogen content of Bituminaria bituminosa and symbiotic efficiency of the four different nitrogen-fixing bacteria studied. The effect of herbicides increased as the used concentration increased. The current research demonstrates that the decreased growth of herbicide-treated plants was caused by herbicides' direct effects on rhizobia rather than herbicides' indirect effects on Bituminaria bituminosa.

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References

  • Abd-Alla, M. H., & Omar, S. A. (1993). Herbicides effects on nodulation, growth and nitrogen yield of faba bean induced by indigenous Rhizobium leguminosarum. Zentralblmikrobiol, 148, 593–597. https://doi.org/10.1016/s0232-4393(11)80225-8

    Article  CAS  Google Scholar 

  • Abd-Alla, M. H., Omar, S. A., & Karanxha, S. (2000). The impact of pesticides on arbuscular mycorrhizal and nitrogen-fixing symbioses in legumes. Applied Soil Ecology, 14, 191–200. https://doi.org/10.1016/S0929-1393(00)00056-1

    Article  Google Scholar 

  • Albrecht, L. P., Albrecht, A. J. P., Braccini, A. L., et al. (2014). The role of glyphosate in RR soybean production and seed quality. Planta Daninha, 32, 401–407. https://doi.org/10.1590/S0100-83582014000200018

    Article  Google Scholar 

  • Alves, B. J. R., Boddey, R. M., & Urquiaga, S. (2003). The success of BNF in soybean in Brazil. Plant and Soil, 252, 1–9.

    Article  CAS  Google Scholar 

  • Ampofo, J. A., Tetteh, W., & Bello, M. (2009). Impact of commonly used agrochemicals on bacterial diversity in cultivated soils. Indian Journal of Microbiology, 49, 223–229.

    Article  CAS  Google Scholar 

  • Angelini, J., Silvina, G., Taurian, T., et al. (2013). The effects of pesticides on bacterial nitrogen fixers in peanut-growing area. Archives of Microbiology, 195, 683–692.

    Article  CAS  Google Scholar 

  • Aubernon, C., Charabidzé, D., Devigne, C., et al. (2015). Experimental study of Lucilia sericata (Diptera Calliphoridae) larval development on rat cadavers: Effects of climate and chemical contamination. Forensic Science International, 253, 125–130.

    Article  CAS  Google Scholar 

  • Bärwald Bohm, G. M., Rombaldi, C. V., Genovese, M. I., et al. (2014). Glyphosate effects on yield, nitrogen fixation, and seed quality in glyphosate-resistant soybean. Crop Science, 54, 1737–1743. https://doi.org/10.2135/cropsci2013.07.0470

    Article  CAS  Google Scholar 

  • Battisti, L., M. Potrich, A.R. Sampaio, et al. 2021. Is glyphosate toxic to bees? A meta-analytical review. Science of the Total Environment 767: 145397

  • Ben Messaoud, B. 2015. Carectérisation phénotipique et génotipique de Rhizobactéries isolées de la région Meknès-Tafilalet et favorisant la croissance de Bituminaria bituminosa

  • Berman, M. C., Llames, M. E., Minotti, P., et al. (2020). Field evidence supports former experimental claims on the stimulatory effect of glyphosate on picocyanobacteria communities. Science of the Total Environment. https://doi.org/10.1016/j.scitotenv.2019.134601

    Article  Google Scholar 

  • Bhattacharjee, R. B., Singh, A., & Mukhopadhyay, S. N. (2008). Use of nitrogen-fixing bacteria as biofertiliser for non-legumes: Prospects and challenges. Applied Microbiology and Biotechnology, 80, 199–209.

    Article  CAS  Google Scholar 

  • Bingham, A. H., & Cotrufo, M. F. (2016). Organic nitrogen storage in mineral soil: Implications for policy and management. Science of the Total Environment, 551–552, 116–126.

    Article  Google Scholar 

  • Board, J.E. 2013. A comprehensive survey of international soybean research—Genetics, physiology, agronomy and nitrogen relationships. InTech

  • Bremner, J. M., & Hauck, R. D. (1982). Advances in methodology for research on nitrogen transformations in soils. Nitrogen Agric Soils, 22, 467–502.

    CAS  Google Scholar 

  • Brockwell, J., Bottomley, P. J., & Thies, J. E. (1995). Manipulation of rhizobia microflora for improving legume productivity and soil fertility: A critical assessment. Plant and Soil, 174, 143–180. https://doi.org/10.1007/BF00032245

    Article  CAS  Google Scholar 

  • Cappello, S., Russo, D., Santisi, S., et al. (2012). Presence of hydrocarbon-degrading bacteria in the gills of mussel Mytilus galloprovincialis in a contaminated environment: A mesoscale simulation study. Chemical Ecology, 28, 239–252.

    Article  CAS  Google Scholar 

  • Cardoso, P., Alves, A., Silveira, P., et al. (2018). Bacteria from nodules of wild legume species: Phylogenetic diversity, plant growth promotion abilities and osmotolerance. Science of the Total Environment, 645, 1094–1102. https://doi.org/10.1016/j.scitotenv.2018.06.399

    Article  CAS  Google Scholar 

  • Carlisle, S. M., & Trevors, J. T. (1988). Glyphosate in the environment. Water, Air, and Soil Pollution, 39, 409–420.

    Article  CAS  Google Scholar 

  • Chanway, C. P., Shishido, M., Nairn, J., et al. (2000). Endophytic colonization and field responses of hybrid spruce seedlings after inoculation with plant growth-promoting rhizobacteria. Forest Ecology and Management, 133, 81–88.

    Article  Google Scholar 

  • Clark, S. A., & Mahanty, H. K. (1991). Influence of herbicides on growth and nodulation of white clover, Trifolium repens. Soil Biology & Biochemistry, 23, 725–730. https://doi.org/10.1016/0038-0717(91)90141-6

    Article  CAS  Google Scholar 

  • Du, Q., Zhou, L., Chen, P., et al. (2019). Relay-intercropping soybean with maize maintains soil fertility and increases nitrogen recovery efficiency by reducing nitrogen input. Crop J. https://doi.org/10.1016/j.cj.2019.06.010

    Article  Google Scholar 

  • Duke, S. O. (2011). Glyphosate degradation in glyphosate-resistant and -susceptible crops and weeds. Journal of Agriculture and Food Chemistry, 59, 5835–5841. https://doi.org/10.1021/jf102704x

    Article  CAS  Google Scholar 

  • Ermakova, I. T., Kiseleva, N. I., Shushkova, T., et al. (2010). Bioremediation of glyphosate-contaminated soils. Applied Microbiology and Biotechnology, 88, 585–594. https://doi.org/10.1007/s00253-010-2775-0

    Article  CAS  Google Scholar 

  • Fan, L., Feng, Y., Weaver, D. B., et al. (2017). Glyphosate effects on symbiotic nitrogen fixation in glyphosate-resistant soybean. Applied Soil Ecology, 121, 11–19. https://doi.org/10.1016/j.apsoil.2017.09.015

    Article  Google Scholar 

  • Flores, M., & Barbachano, M. (1992). Effects of herbicides Gramoxone, Diuron and Totacol®on growth and nodulation of three strains of Rhizobium meliloti. Science of the Total Environment, 123, 249–260.

    Article  Google Scholar 

  • Fox, J. E., Gulledge, J., Engelhaupt, E., et al. (2007). Pesticides reduce symbiotic efficiency of nitrogen-fixing rhizobia and host plants. Proceedings of the National Academy of Sciences of the United States of America, 104, 10282–10287. https://doi.org/10.1073/pnas.0611710104

    Article  CAS  Google Scholar 

  • Guijarro, K. H., Aparicio, V., De Gerónimo, E., et al. (2018). Soil microbial communities and glyphosate decay in soils with different herbicide application history. Science of the Total Environment, 634, 974–982. https://doi.org/10.1016/j.scitotenv.2018.03.393

    Article  CAS  Google Scholar 

  • Herridge, D. F., Peoples, M. B., & Boddey, R. M. (2008). Global inputs of biological nitrogen fixation in agricultural systems. Plant and Soil, 311, 1–18.

    Article  CAS  Google Scholar 

  • Kawaka, F., Dida, M. M., Opala, P. A., et al. (2014). Symbiotic efficiency of native Rhizobia Nodulating common bean (Phaseolus vulgaris L. ) in soils of Western Kenya. International Scholarly Research Notices, 2014, 1–8. https://doi.org/10.1155/2014/258497

    Article  Google Scholar 

  • King, C.A., L.C. Purcell, and E.D. Vories. 2001. Soybean: Plant growth and nitrogenase activity of glyphosate-tolerant soybean in response to foliar glyphosate applications. In: Agronomy Journal. pp 179–186

  • Lane, D.J. 1991. 16S/23S rRNA sequencing. Nucleic Acid-Based Technologies Batch System 115–175

  • Lodwig, E. M., Hosie, A. H. F., Bourde`s A, , et al. (2003). Amino-acid cycling drives nitrogen fixationinthe legume–Rhizobium symbiosis. Nature, 422, 722–726. https://doi.org/10.1038/nature01549

    Article  CAS  Google Scholar 

  • Lu, C., Z. Yang, J. Liu, et al. 2020. Chlorpyrifos inhibits nitrogen fixation in rice-vegetated soil containing Pseudomonas stutzeri A1501. Chemosphere 256: 127098

  • Ma, J., Bei, Q., Wang, X., et al. (2019). Impacts of Mo application on biological nitrogen fixation and diazotrophic communities in a flooded rice-soil system. Science of the Total Environment, 649, 686–694. https://doi.org/10.1016/j.scitotenv.2018.08.318

    Article  CAS  Google Scholar 

  • Maidak, B. L., Olsen, G. J., Larsen, N., et al. (1997). The RDP (ribosomal database project). Nucleic Acids Research, 25, 109–110.

    Article  CAS  Google Scholar 

  • Maldani, M., Ben Messaoud, B., Nassiri, L., & Ibijbijen, J. (2018). 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., Dekaki, E. M., Nassiri, L., & Ibijbijen, J. (2017a). State of art on the use of pesticides in Meknes Region, Morocco. American Journal of Agricultural Science, 4, 138–148.

    Google Scholar 

  • Maldani, M., Ben, M. B., Nassiri, L. I., & jamal, . (2017b). Assessment of the resistance of four nitrogen-fixing Bacteria to glyphosate. Atlas Journal of Biology. https://doi.org/10.5147/ajb.v0i0.176

    Article  Google Scholar 

  • Molin, W. T. (1998). Glyphosate, a unique global herbicide. J. E. Franz, M. K. Mao, and J. A. Sikorski, ACS monograph 189, 1997. 653 pp. Weed Technology, 12, 564–565. https://doi.org/10.1017/s0890037x0004433x

    Article  Google Scholar 

  • Moretti, M. L., & Hanson, B. D. (2017). Reduced translocation is involved in resistance to glyphosate and paraquat in Conyza bonariensis and Conyza canadensis from California. Weed Research, 57, 25–34. https://doi.org/10.1111/wre.12230

    Article  CAS  Google Scholar 

  • Nelson, D. W., & Sommers, L. E. (1973). Determination of total nitrogen in plant material. Agronomy Journal, 65, 109. https://doi.org/10.2134/agronj1973.00021962006500010033x

    Article  CAS  Google Scholar 

  • Newman, M. M., Hoilett, N., Lorenz, N., et al. (2016). Glyphosate effects on soil rhizosphere-associated bacterial communities. Science of the Total Environment, 543, 155–160. https://doi.org/10.1016/j.scitotenv.2015.11.008

    Article  CAS  Google Scholar 

  • Pati, B. R., Chandra, A. K., & Gupta, S. (1984). The in vitro effect of some pesticides on the nitrogen fixing bacteria isolated from the phyllosphere of some crop plants. Plant and Soil, 80, 215–225.

    Article  CAS  Google Scholar 

  • Pazos-Navarro, M., Dabauza, M., Correal, E., et al. (2011). Next generation DNA sequencing technology delivers valuable genetic markers for the genomic orphan legume species, Bituminaria Bituminosa. BMC Genetics. https://doi.org/10.1186/1471-2156-12-104

    Article  Google Scholar 

  • Pearson, W. R., & Lipman, D. J. (1988). Improved tools for biological sequence comparison. Proceedings of the National Academy of Sciences, 85, 2444–2448.

    Article  CAS  Google Scholar 

  • Reddy, K. N., Hoagland, R. E., & Zablotowicz, R. M. (2000). Effect of glyphosate on growth, chlorophyll, and nodulation in glyphosate-resistant and susceptible soybean (Glycine max) varieties. Journal of New Seeds, 2, 37–52. https://doi.org/10.1300/J153v02n03_03

    Article  Google Scholar 

  • Shankar, P.V., N.R. Shaikh, and P.S. Vishwas. 2012. Effect of different herbicides on the nodulation property of rhizobial isolates abstract : Introduction : 2.0 : materials and methods . 2: 293–299

  • Shen, W., Hu, M., Qian, D., et al. (2021). Microbial deterioration and restoration in greenhouse-based intensive vegetable production systems. Plant and Soil. https://doi.org/10.1007/s11104-021-04933-w

    Article  Google Scholar 

  • Singh, G., & Wright, D. (1999). Effects of herbicides on nodulation, symbiotic nitrogen fixation, growth and yield of pea (Pisum sativum). Journal of Agricultural Science, 133, 21–30. https://doi.org/10.1017/S0021859699006735

    Article  CAS  Google Scholar 

  • Sousa, S., M.L. Maia, L. Correira-Sá, et al. 2020. Chemistry and toxicology behind insecticides and herbicides. In Controlled release of pesticides for sustainable agriculture. New York: Springer, pp. 59–109

  • Steinrucken, H.C., and N. Amrhein. 1980. The herbicide glyphosate is a potent inhibitor of 5-enolpyruvyl- shikimic acid-3-phosphate synthase. Biochemical and Biophysical Research Communications 1207–1212

  • Tang, F. H. M., Jeffries, T. C., Vervoort, R. W., et al. (2019). Microcosm experiments and kinetic modeling of glyphosate biodegradation in soils and sediments. Science of the Total Environment, 658, 105–115. https://doi.org/10.1016/j.scitotenv.2018.12.179

    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 ? Science of the Total Environment, 684, 314–325. https://doi.org/10.1016/j.scitotenv.2019.05.230

    Article  CAS  Google Scholar 

  • Troussellier, M., Got, P., Mboup, M., et al. (2005). Daily bacterioplankton dynamics in a sub-Saharan estuary (Senegal River, West Africa): A mesocosm study. Aquatic Microbial Ecology, 40, 13–24.

    Article  Google Scholar 

  • Winnepenninckx, B. (1993). Extraction of high molecular weight DNA from molluscs. Trends in Genetics, 9, 407.

    Article  CAS  Google Scholar 

  • Xia, X., Ma, C., Dong, S., et al. (2017). Effects of nitrogen concentrations on nodulation and nitrogenase activity in dual root systems of soybean plants. Soil Sci Plant Nutr, 63, 470–482. https://doi.org/10.1080/00380768.2017.1370960

    Article  CAS  Google Scholar 

  • Xu, L., Yu, G., He, N., et al. (2018). Carbon storage in China’s terrestrial ecosystems: A synthesis. Science and Reports, 8, 1–13. https://doi.org/10.1038/s41598-018-20764-9

    Article  CAS  Google Scholar 

  • Yakimov, M. M., Cappello, S., Crisafi, E., et al. (2006). Phylogenetic survey of metabolically active microbial communities associated with the deep-sea coral Lophelia pertusa from the Apulian plateau, Central Mediterranean Sea. Deep Sea Research, Part I: Oceanographic Research Papers, 53, 62–75.

    Article  Google Scholar 

  • Yemm, E. W., Cocking, E. C., & Ricketts, R. E. (1955). The determination of amino-acids with ninhydrin. The Analyst, 80, 209–214. https://doi.org/10.1039/AN9558000209

    Article  CAS  Google Scholar 

  • Zhan, H., Feng, Y., Fan, X., & Chen, S. (2018). Recent advances in glyphosate biodegradation. Applied Microbiology and Biotechnology, 102, 5033–5043.

    Article  CAS  Google Scholar 

  • Zobiole, L. H. S., Kremer, R. J., Oliveira, R. S., & Constantin, J. (2011). Glyphosate affects chlorophyll, nodulation and nutrient accumulation of “ second generation” glyphosate-resistant soybean (Glycine max L.). Pesticide Biochemistry and Physiology, 99, 53–60. https://doi.org/10.1016/j.pestbp.2010.10.005

    Article  CAS  Google Scholar 

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Acknowledgements

Our special thanks to Environment and Valorization of Microbial and Plant Resources Unit, Department of Biology, Faculty of Sciences, Moulay Ismail University, Meknes, Morocco, and all those who helped us to accomplish this work. M. Maldani was a recipient of a Ph.D. fellowship under the Erasmus + KA107 (2018-1-IT02-KA107-047799) Project at the University of Messina, Italy. We would also like to thank the Institute of Biological Resources and Marine Biotechnology (IRBIM)-National Research Council (CNR), Messine, Italy.

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Mohamed, M., Aliyat, F.Z., Ben Messaoud, B. et al. Effects of Pesticides Use (Glyphosate & Paraquat) on Biological Nitrogen Fixation. Water Air Soil Pollut 232, 419 (2021). https://doi.org/10.1007/s11270-021-05367-x

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