Resistance to degradation and effect of the herbicide glyphosate on the bacterioplankton community of a large river system dominated by agricultural activities
Claudia Piccini
A E , Stefano Fazi B , Germán Pérez C , Giampiero Batani B , Gabriela Martínez de la Escalera A and José Roberto Sotelo-Silveira D
+ Author Affiliations
- Author Affiliations
A Departmento de Microbiología, Instituto de Investigaciones Biológicas Clemente Estable, Avenida Italia 3318, Montevideo 11600, Uruguay.
B Water Research Institute, National Research Council of Italy (IRSA-CNR), Via Salaria chilometro 29.300, Monterotondo, I-00015 Rome, Italy.
C Laboratorio de Microbiología, Departamento Biología Vegetal, Facultad de Agronomía, Universidad de la República, Avenida Garzón 809, Montevideo 12900, Uruguay.
D Departamento de Genómica, Instituto de Investigaciones Biológicas Clemente Estable, Avenida Italia 3318, Montevideo 11600, Uruguay.
E Corresponding author. Email: cpiccini@iibce.edu.uy
Marine and Freshwater Research 71(8) 1026-1032 https://doi.org/10.1071/MF19079
Submitted: 12 March 2019 Accepted: 27 August 2019 Published: 10 December 2019
Abstract
Glyphosate-based herbicides are widely used for several crops, such as transgenic soybean and forestry. The aim of this study was to determine the effect of glyphosate on the community structure of riverine bacterioplankton and to evaluate the potential of bacterioplankton to degrade the herbicide. River water to which 13C-labelled glyphosate (10, 100 µg L–1) was added or not (control) was incubated for 6 days at the temperature measured in situ (20°C). Significant differences in bacterioplankton community composition, as assessed by microfluidics-based automated ribosomal intergenic spacer analysis, were found among treatments, with differences in the presence of 100 µg L–1 of glyphosate being more pronounced, namely significant decreases in bacterial richness and diversity. The glyphosate degradation product aminomethylphosphonic acid (AMPA) was detected, accounting for 1.2% of glyphosate conversion in water with 100 µg L–1 of 13C-labelled glyphosate, together with a significant enrichment of 13C in the bacterial biomass. These findings suggest that glyphosate had a direct detrimental effect on most bacterioplankton taxa, but enriched those that were able to degrade the herbicide. Together, the results indicate that glyphosate degradation in the river assessed would be a slow process (months–years), taking place through the AMPA degradation pathway and meaning glyphosate accumulate in the ecosystem.
Additional keywords: aminomethylphosphonic acid, AMPA, internal transcribed spacer, MF-ARISA, microfluidics-based automated ribosomal intergenic spacer analysis.
References
American Public Health Association (1995). ‘Standard Methods for the Examination of Water and Wastewater’, 19th edn. (APHA, AWWA and WPCF: Washington, DC, USA.)Balthazor, T. M., and Hallas, L. E. (1986). Glyphosate-degrading microorganisms from industrial activated sludge. Applied and Environmental Microbiology 51, 432–434.
| 16346999PubMed |
Battaglin, W., Meyer, M., Kuivila, K., and Dietze, J. (2014). Glyphosate and its degradation product AMPA occur frequently and widely in US soils, surface water, groundwater, and precipitation. Journal of the American Water Resources Association 50, 275–290.
| Glyphosate and its degradation product AMPA occur frequently and widely in US soils, surface water, groundwater, and precipitation.Crossref | GoogleScholarGoogle Scholar |
Cardinale, M., Brusetti, L., Quatrini, P., Borin, S., Puglia, A. M., Rizzi, A., Zanardini, E., Sorlini, C., Corselli, C., and Daffonchio, D. (2004). Comparison of different primer sets for use in automated ribosomal intergenic spacer analysis of complex bacterial communities. Applied and Environmental Microbiology 70, 6147–6156.
| Comparison of different primer sets for use in automated ribosomal intergenic spacer analysis of complex bacterial communities.Crossref | GoogleScholarGoogle Scholar | 15466561PubMed |
Ciesielski, S., Bułkowska, K., Dabrowska, D., Kaczmarczyk, D., Kowal, P., and Możejko, J. (2013). Ribosomal intergenic spacer analysis as a tool for monitoring methanogenic archaea changes in an anaerobic digester. Current Microbiology 67, 240–248.
| Ribosomal intergenic spacer analysis as a tool for monitoring methanogenic archaea changes in an anaerobic digester.Crossref | GoogleScholarGoogle Scholar | 23525724PubMed |
Clarke, K. R. (1993). Non‐parametric multivariate analyses of changes in community structure. Australian Journal of Ecology 18, 117–143.
| Non‐parametric multivariate analyses of changes in community structure.Crossref | GoogleScholarGoogle Scholar |
Cuhra, M., Bøhn, T., and Cuhra, P. (2016). Glyphosate: too much of a good thing? Frontiers in Environmental Science 4, 28.
| Glyphosate: too much of a good thing?Crossref | GoogleScholarGoogle Scholar |
Dick, R., and Quinn, J. (1995). Glyphosate-degrading isolates from environmental samples: occurrence and pathways of degradation. Applied Microbiology and Biotechnology 43, 545–550.
| Glyphosate-degrading isolates from environmental samples: occurrence and pathways of degradation.Crossref | GoogleScholarGoogle Scholar | 7632402PubMed |
Dirección Nacional de Medio Ambiente (2015). Informe de evolución de la calidad del agua en la cuenca del Río Santa Lucía - 10 años de información (julio 2015). (DINAMA, Ministerio de Vivienda, Ordenamiento Territorial y Medio Ambiente: Montevideo, Uruguay.) Available at https://www.mvotma.gub.uy/ambiente/prevencion-y-control-para-el-cuidado-del-ambiente/estado-del-ambiente/calidad-ambiental/item/10010296-informe-de-evolucion-de-la-calidad-del-agua-en-la-cuenca-del-rio-santa-lucia-10-anos-de-informacion-julio-2015 [Verified 29 October 2019].
Duke, S. O., and Powles, S. B. (2008). Glyphosate: a once-in-a-century herbicide. Pest Management Science 64, 319–325.
| Glyphosate: a once-in-a-century herbicide.Crossref | GoogleScholarGoogle Scholar | 18273882PubMed |
Feng, J. C., and Thompson, D. G. (1990). Fate of glyphosate in a Canadian forest watershed. 2. Persistence in foliage and soils. Journal of Agricultural and Food Chemistry 38, 1118–1125.
| Fate of glyphosate in a Canadian forest watershed. 2. Persistence in foliage and soils.Crossref | GoogleScholarGoogle Scholar |
Ferguson, R. L., Buckley, E. N., and Palumbo, A. V. (1984). Response of marine bacterioplankton to differential filtration and confinement. Applied and Environmental Microbiology 47, 49–55.
| 6696422PubMed |
Fisher, M. M., and Triplett, E. W. (1999). Automated approach for ribosomal intergenic spacer analysis of microbial diversity and its application to freshwater bacterial communities. Applied and Environmental Microbiology 65, 4630–4636.
| 10508099PubMed |
Fuchs, B. M., Zubkov, M. V., Sahm, K., Burkill, P. H., and Amann, R. (2000). Changes in community composition during dilution cultures of marine bacterioplankton as assessed by flow cytometric and molecular biological techniques. Environmental Microbiology 2, 191–201.
| Changes in community composition during dilution cultures of marine bacterioplankton as assessed by flow cytometric and molecular biological techniques.Crossref | GoogleScholarGoogle Scholar | 11220305PubMed |
Giesy, J. P., Dobson, S., and Solomon, K. R. (2000). Ecotoxicological risk assessment for Roundup herbicide. Reviews of Environmental Contamination and Toxicology 167, 35–120.
| Ecotoxicological risk assessment for Roundup herbicide.Crossref | GoogleScholarGoogle Scholar |
Grandcoin, A., Piel, S., and Baures, E. (2017). AminoMethylPhosphonic acid (AMPA) in natural waters: its sources, behavior and environmental fate. Water Research 117, 187–197.
| AminoMethylPhosphonic acid (AMPA) in natural waters: its sources, behavior and environmental fate.Crossref | GoogleScholarGoogle Scholar | 28391123PubMed |
Grunewald, K., Schmidt, W., Unger, C., and Hanschmann, G. (2001). Behavior of glyphosate and aminomethylphosphonic acid (AMPA) in soils and water of reservoir Radeburg II catchment (Saxony/Germany). Journal of Plant Nutrition and Soil Science 164, 65–70.
| Behavior of glyphosate and aminomethylphosphonic acid (AMPA) in soils and water of reservoir Radeburg II catchment (Saxony/Germany).Crossref | GoogleScholarGoogle Scholar |
Guilherme, S., Santos, M. A., Gaivão, I., and Pacheco, M. (2014). DNA and chromosomal damage induced in fish (Anguilla anguilla L.) by aminomethylphosphonic acid (AMPA) – the major environmental breakdown product of glyphosate. Environmental Science and Pollution Research International 21, 8730–8739.
| DNA and chromosomal damage induced in fish (Anguilla anguilla L.) by aminomethylphosphonic acid (AMPA) – the major environmental breakdown product of glyphosate.Crossref | GoogleScholarGoogle Scholar | 24696215PubMed |
Hammer, Ø., Harper, D., and Ryan, P. (2001). Past: paleontological statistics software package for education and data analysis. Palaeontologia Electronica 4, 1–9.
Jacob, G. S., Garbow, J. R., Hallas, L. E., Kimack, N. M., Kishore, G. M., and Schaefer, J. (1988). Metabolism of glyphosate in Pseudomonas sp. strain LBr. Applied and Environmental Microbiology 54, 2953–2958.
| 3223761PubMed |
Lozupone, C. A., Hamady, M., Kelley, S. T., and Knight, R. (2007). Quantitative and qualitative β diversity measures lead to different insights into factors that structure microbial communities. Applied and Environmental Microbiology 73, 1576–1585.
| Quantitative and qualitative β diversity measures lead to different insights into factors that structure microbial communities.Crossref | GoogleScholarGoogle Scholar | 17220268PubMed |
Marc, J., Le Breton, M., Cormier, P., Morales, J., Bellé, R., and Mulner-Lorillon, O. (2005). A glyphosate-based pesticide impinges on transcription. Toxicology and Applied Pharmacology 203, 1–8.
| A glyphosate-based pesticide impinges on transcription.Crossref | GoogleScholarGoogle Scholar | 15694458PubMed |
Mercurio, P., Flores, F., Mueller, J. F., Carter, S., and Negri, A. P. (2014). Glyphosate persistence in seawater. Marine Pollution Bulletin 85, 385–390.
| Glyphosate persistence in seawater.Crossref | GoogleScholarGoogle Scholar | 24467857PubMed |
Obojska, A., Lejczak, B., and Kubrak, M. (1999). Degradation of phosphonates by streptomycete isolates. Applied Microbiology and Biotechnology 51, 872–876.
| Degradation of phosphonates by streptomycete isolates.Crossref | GoogleScholarGoogle Scholar | 10422232PubMed |
Pérez, G., Torremorell, A., Mugni, H., Rodriguez, P., Vera, M. S., Nascimento, M., Allende, L., Bustingorry, J., Escaray, R., and Ferraro, M. (2007). Effects of the herbicide Roundup on freshwater microbial communities: a mesocosm study. Ecological Applications 17, 2310–2322.
| Effects of the herbicide Roundup on freshwater microbial communities: a mesocosm study.Crossref | GoogleScholarGoogle Scholar | 18213971PubMed |
Pesce, S., Batisson, I., Bardot, C., Fajon, C., Portelli, C., Montuelle, B., and Bohatier, J. (2009). Response of spring and summer riverine microbial communities following glyphosate exposure. Ecotoxicology and Environmental Safety 72, 1905–1912.
| Response of spring and summer riverine microbial communities following glyphosate exposure.Crossref | GoogleScholarGoogle Scholar | 19646758PubMed |
Pipke, R., and Amrhein, N. (1988). Isolation and characterization of a mutant of Arthrobacter sp. strain GLP-1 which utilizes the herbicide glyphosate as its sole source of phosphorus and nitrogen. Applied and Environmental Microbiology 54, 2868–2870.
| 16347784PubMed |
Pizarro, H., Vera, M., Vinocur, A., Pérez, G., Ferraro, M., Helman, R. M., and dos Santos, M. (2016). Glyphosate input modifies microbial community structure in clear and turbid freshwater systems. Environmental Science and Pollution Research International 23, 5143–5153.
| Glyphosate input modifies microbial community structure in clear and turbid freshwater systems.Crossref | GoogleScholarGoogle Scholar | 26552793PubMed |
Porter, K. G., and Feig, Y. S. (1980). The use of DAPI for identifying and counting aquatic microflora. Limnology and Oceanography 25, 943–948.
| The use of DAPI for identifying and counting aquatic microflora.Crossref | GoogleScholarGoogle Scholar |
Ramette, A. (2009). Quantitative community fingerprinting methods for estimating the abundance of operational taxonomic units in natural microbial communities. Applied and Environmental Microbiology 75, 2495–2505.
| Quantitative community fingerprinting methods for estimating the abundance of operational taxonomic units in natural microbial communities.Crossref | GoogleScholarGoogle Scholar | 19201961PubMed |
Ronco, A. E., Marino, D. J. G., Abelandom, M., Almadam, P., and Apartin, C. D. (2016). Water quality of the main tributaries of the Paraná Basin: glyphosate and AMPA in surface water and bottom sediments. Environmental Monitoring and Assessment 188, 458.
| Water quality of the main tributaries of the Paraná Basin: glyphosate and AMPA in surface water and bottom sediments.Crossref | GoogleScholarGoogle Scholar | 27395359PubMed |
Solomon, K., and Thompson, D. (2003). Ecological risk assessment for aquatic organisms from over-water uses of glyphosate. Journal of Toxicology and Environmental Health – B. Critical Reviews 6, 289–324.
| Ecological risk assessment for aquatic organisms from over-water uses of glyphosate.Crossref | GoogleScholarGoogle Scholar | 12746143PubMed |
Sviridov, A. V., Shushkova, T. V., Ermakova, I. T., Ivanova, E. V., Epiktetov, D. O., and Leontievsky, A. A. (2015). Microbial degradation of glyphosate herbicides. Applied Biochemistry and Microbiology 51, 188–195.
| Microbial degradation of glyphosate herbicides.Crossref | GoogleScholarGoogle Scholar |
Ternan, N. G., Mc Grath, J. W., Mc Mullan, G., and Quinn, J. P. (1998). Review: organophosphonates: occurrence, synthesis and biodegradation by microorganisms. World Journal of Microbiology & Biotechnology 14, 635–647.
| Review: organophosphonates: occurrence, synthesis and biodegradation by microorganisms.Crossref | GoogleScholarGoogle Scholar |
Tsui, M. T., and Chu, L. (2003). Aquatic toxicity of glyphosate-based formulations: comparison between different organisms and the effects of environmental factors. Chemosphere 52, 1189–1197.
| Aquatic toxicity of glyphosate-based formulations: comparison between different organisms and the effects of environmental factors.Crossref | GoogleScholarGoogle Scholar | 12821000PubMed |
Veiga, F., Zapata, J. M., Fernandez Marcos, M. L., and Alvarez, E. (2001). Dynamics of glyphosate and aminomethylphosphonic acid in a forest soil in Galicia, north-west Spain. The Science of the Total Environment 271, 135–144.
| Dynamics of glyphosate and aminomethylphosphonic acid in a forest soil in Galicia, north-west Spain.Crossref | GoogleScholarGoogle Scholar | 11346036PubMed |
Vera, M. S., Lagomarsino, L., Sylvester, M., Pérez, G. L., Rodríguez, P., Mugni, H., Sinistro, R., Ferraro, M., Bonetto, C., Zagarese, H., and Pizarro, H. (2010). New evidences of Roundup (glyphosate formulation) impact on the periphyton community and the water quality of freshwater ecosystems. Ecotoxicology 19, 710–721.
| New evidences of Roundup (glyphosate formulation) impact on the periphyton community and the water quality of freshwater ecosystems.Crossref | GoogleScholarGoogle Scholar | 20091117PubMed |
Vera, M. S., Di Fiori, E., Lagomarsino, L., Sinistro, R., Escaray, R., Iummato, M. M., Juárez, A., de Molina, M. R., Tell, G., and Pizarro, H. (2012). Direct and indirect effects of the glyphosate formulation Glifosato Atanor on freshwater microbial communities. Ecotoxicology 21, 1805–1816.
| Direct and indirect effects of the glyphosate formulation Glifosato Atanor on freshwater microbial communities.Crossref | GoogleScholarGoogle Scholar | 22539117PubMed |
Wang, S., Seiwert, B., Kästner, M., Miltner, A., Schäffer, A., Reemtsma, T., Yang, Q., and Nowak, K. M. (2016). (Bio)degradation of glyphosate in water-sediment microcosms – a stable isotope co-labeling approach. Water Research 99, 91–100.
| (Bio)degradation of glyphosate in water-sediment microcosms – a stable isotope co-labeling approach.Crossref | GoogleScholarGoogle Scholar | 27140906PubMed |
Widenfalk, A. (2005). Interactions between pesticides and microorganisms in freshwater sediments. Ph.D. Thesis, Sveriges lantbruksuniv, Uppsala, Sweden. Available at https://pub.epsilon.slu.se/770/1/AWKappa.pdf [Verified 29 October 2019].
Widenfalk, A., Bertilsson, S., Sundh, I., and Goedkoop, W. (2008). Effects of pesticides on community composition and activity of sediment microbes – responses at various levels of microbial community organization. Environmental Pollution 152, 576–584.
| Effects of pesticides on community composition and activity of sediment microbes – responses at various levels of microbial community organization.Crossref | GoogleScholarGoogle Scholar | 17822816PubMed |
Zhan, H., Feng, Y., Fan, X., and Chen, S. (2018). Recent advances in glyphosate biodegradation. Applied Microbiology and Biotechnology 102, 5033–5043.
| Recent advances in glyphosate biodegradation.Crossref | GoogleScholarGoogle Scholar | 29705962PubMed |
Zhou, J., Bruns, M. A., and Tiedje, J. M. (1996). DNA recovery from soils of diverse composition. Applied and Environmental Microbiology 62, 316–322.
| 8593035PubMed |
