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.
Graphical Abstract
Similar content being viewed by others
Data Availability
Applicable.
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
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
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
Alves, B. J. R., Boddey, R. M., & Urquiaga, S. (2003). The success of BNF in soybean in Brazil. Plant and Soil, 252, 1–9.
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.
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.
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.
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
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
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.
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.
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.
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
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.
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
Carlisle, S. M., & Trevors, J. T. (1988). Glyphosate in the environment. Water, Air, and Soil Pollution, 39, 409–420.
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.
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
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
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
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
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
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.
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
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
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.
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
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
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
Maidak, B. L., Olsen, G. J., Larsen, N., et al. (1997). The RDP (ribosomal database project). Nucleic Acids Research, 25, 109–110.
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
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.
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
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
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
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
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
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.
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
Pearson, W. R., & Lipman, D. J. (1988). Improved tools for biological sequence comparison. Proceedings of the National Academy of Sciences, 85, 2444–2448.
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
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
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
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
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
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.
Winnepenninckx, B. (1993). Extraction of high molecular weight DNA from molluscs. Trends in Genetics, 9, 407.
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
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
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.
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
Zhan, H., Feng, Y., Fan, X., & Chen, S. (2018). Recent advances in glyphosate biodegradation. Applied Microbiology and Biotechnology, 102, 5033–5043.
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
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.
Author information
Authors and Affiliations
Corresponding author
Ethics declarations
Conflict of interest
The authors declare no conflict of interest, financial or otherwise.
Ethical Approval and Consent to Participate
Not applicable.
Human and Animal Rights
No Animals/Humans were used for studies that are the basis of this research.
Additional information
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
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
Received:
Accepted:
Published:
DOI: https://doi.org/10.1007/s11270-021-05367-x