How Benthic Sediment Microbial Communities Respond to Glyphosate and Its Metabolite: a Microcosm Experiment.
AMPA
Glyphosate
Microcosms
Microorganisms
Sediments
Wetlands
Journal
Microbial ecology
ISSN: 1432-184X
Titre abrégé: Microb Ecol
Pays: United States
ID NLM: 7500663
Informations de publication
Date de publication:
Nov 2023
Nov 2023
Historique:
received:
03
05
2023
accepted:
28
08
2023
medline:
13
11
2023
pubmed:
7
9
2023
entrez:
6
9
2023
Statut:
ppublish
Résumé
Glyphosate is the most commonly used agricultural herbicide in the world. In aquatic ecosystems, glyphosate often adsorbs to benthic substrates or is metabolized and degraded by microorganisms. The effects of glyphosate on microbial communities vary widely as microorganisms respond differently to exposure. To help understand the impacts of glyphosate on the sediment microbiome, we conducted a microcosm experiment examining the responses of benthic sediment microbial communities to herbicide treatments. Sediments from a prairie pothole wetland were collected, and 16S rRNA gene sequencing was used to analyze community composition 2-h and 14-days after a single treatment of low (0.07 ppm), medium (0.7 ppm), or high (7 ppm) glyphosate, aminomethylphosphonic acid (glyphosate metabolite), or a glyphosate-based commercial formula. We found no significant differences in microbial community composition across treatments, concentration levels, or day of sampling. These findings suggest that microbial species in the Prairie Pothole Region of North America may be tolerant to glyphosate exposure.
Identifiants
pubmed: 37674014
doi: 10.1007/s00248-023-02296-6
pii: 10.1007/s00248-023-02296-6
doi:
Substances chimiques
RNA, Ribosomal, 16S
0
Water Pollutants, Chemical
0
Herbicides
0
Types de publication
Journal Article
Langues
eng
Sous-ensembles de citation
IM
Pagination
2949-2958Informations de copyright
© 2023. The Author(s), under exclusive licence to Springer Science+Business Media, LLC, part of Springer Nature.
Références
Benbrook CM (2016) Trends in glyphosate herbicide use in the United States and globally. Environ Sci Eur 28:3. https://doi.org/10.1186/s12302-016-0070-0
doi: 10.1186/s12302-016-0070-0
pubmed: 27752438
pmcid: 5044953
Coupe RH, Kalkhoff SJ, Capel PD, Gregoire C (2012) Fate and transport of glyphosate and aminomethylphosphonic acid in surface waters of agricultural basins. Pest Manag Sci 68:16–30. https://doi.org/10.1002/ps.2212
doi: 10.1002/ps.2212
pubmed: 21681915
Belden JB, Hanson BR, McMurry ST et al (2012) Assessment of the effects of farming and conservation programs on pesticide deposition in high plains wetlands. Environ Sci Technol 46:3424–3432. https://doi.org/10.1021/es300316q
doi: 10.1021/es300316q
pubmed: 22356096
Warren N, Allan IJ, Carter JE et al (2003) Pesticides and other micro-organic contaminants in freshwater sedimentary environments—a review. Appl Geochem 18:159–194. https://doi.org/10.1016/S0883-2927(02)00159-2
doi: 10.1016/S0883-2927(02)00159-2
Battaglin WA, Meyer MT, Kuivila KM, Dietze JE (2014) Glyphosate and its degradation product AMPA occur frequently and widely in U.S. soils, surface water, groundwater, and precipitation. J Am Water Resour Assoc 50:275–290. https://doi.org/10.1111/jawr.12159
doi: 10.1111/jawr.12159
Zhan H, Feng Y, Fan X, Chen S (2018) Recent advances in glyphosate biodegradation. Appl Microbiol Biotechnol 102:5033–5043. https://doi.org/10.1007/s00253-018-9035-0
doi: 10.1007/s00253-018-9035-0
pubmed: 29705962
Cobb AH, Reade JPH (2010) Herbicides and plant physiology: Cobb/Herbicides and Plant Physiology. Wiley-Blackwell, Oxford, UK
doi: 10.1002/9781444327793
Herrmann KM, Weaver LM (1999) The shikimate pathway. Annu Rev Plant Physiol Plant Mol Biol 50:473–503. https://doi.org/10.1146/annurev.arplant.50.1.473
doi: 10.1146/annurev.arplant.50.1.473
pubmed: 15012217
Leino L, Tall T, Helander M et al (2021) Classification of the glyphosate target enzyme (5-enolpyruvylshikimate-3-phosphate synthase) for assessing sensitivity of organisms to the herbicide. J Hazard Mater 408:124556. https://doi.org/10.1016/j.jhazmat.2020.124556
doi: 10.1016/j.jhazmat.2020.124556
pubmed: 33243645
Pérez GL, Torremorell A, Mugni H et al (2007) Effects of the herbicide roundup on freshwater microbial communities: a mesocosm study. Ecol Appl 17:2310–2322. https://doi.org/10.1890/07-0499.1
doi: 10.1890/07-0499.1
pubmed: 18213971
Lu T, Xu N, Zhang Q et al (2020) Understanding the influence of glyphosate on the structure and function of freshwater microbial community in a microcosm. Environ Pollut 260:114012. https://doi.org/10.1016/j.envpol.2020.114012
doi: 10.1016/j.envpol.2020.114012
pubmed: 31995771
Forlani G, Pavan M, Gramek M et al (2008) Biochemical bases for a widespread tolerance of cyanobacteria to the phosphonate herbicide glyphosate. Plant Cell Physiol 49:443–456. https://doi.org/10.1093/pcp/pcn021
doi: 10.1093/pcp/pcn021
pubmed: 18263622
Shushkova TV, Vasilieva GK, Ermakova IT, Leontievsky AA (2009) Sorption and microbial degradation of glyphosate in soil suspensions. Appl Biochem Microbiol 45:599–603. https://doi.org/10.1134/S0003683809060040
doi: 10.1134/S0003683809060040
Grandcoin A, Piel S, Baurès E (2017) Aminomethylphosphonic acid (AMPA) in natural waters: its sources, behavior and environmental fate. Water Res 117:187–197. https://doi.org/10.1016/j.watres.2017.03.055
doi: 10.1016/j.watres.2017.03.055
pubmed: 28391123
Blake R, Pallett K (2018) The environmental fate and ecotoxicity of glyphosate. Outlook Pest Man 29:266–269. https://doi.org/10.1564/v29_dec_08
doi: 10.1564/v29_dec_08
Degenhardt D, Humphries D, Cessna AJ et al (2012) Dissipation of glyphosate and aminomethylphosphonic acid in water and sediment of two Canadian prairie wetlands. J Environ Sci Health, Part B 47:631–639. https://doi.org/10.1080/03601234.2012.668459
doi: 10.1080/03601234.2012.668459
Kjaer J, Olsen P, Ullum M, Grant R (2005) Leaching of glyphosate and amino-methylphosphonic acid from Danish agricultural field sites. J Environ Qual 34:608–620. https://doi.org/10.2134/jeq2005.0608
doi: 10.2134/jeq2005.0608
pubmed: 15758114
Reddy KN, Rimando AM, Duke SO, Nandula VK (2008) Aminomethylphosphonic acid accumulation in plant species treated with glyphosate. J Agric Food Chem 56:2125–2130. https://doi.org/10.1021/jf072954f
doi: 10.1021/jf072954f
pubmed: 18298069
Bai SH, Ogbourne SM (2016) Glyphosate: environmental contamination, toxicity and potential risks to human health via food contamination. Environ Sci Pollut Res 23:18988–19001. https://doi.org/10.1007/s11356-016-7425-3
doi: 10.1007/s11356-016-7425-3
Beecraft L, Rooney R (2021) Bioconcentration of glyphosate in wetland biofilms. Sci Total Environ 756:143993. https://doi.org/10.1016/j.scitotenv.2020.143993
doi: 10.1016/j.scitotenv.2020.143993
pubmed: 33310222
Malaj E, Liber K, Morrissey CA (2020) Spatial distribution of agricultural pesticide use and predicted wetland exposure in the Canadian Prairie Pothole Region. Sci Total Environ 718:134765. https://doi.org/10.1016/j.scitotenv.2019.134765
doi: 10.1016/j.scitotenv.2019.134765
pubmed: 31843311
Okada E, Costa JL, Bedmar F (2016) Adsorption and mobility of glyphosate in different soils under no-till and conventional tillage. Geoderma 263:78–85. https://doi.org/10.1016/j.geoderma.2015.09.009
doi: 10.1016/j.geoderma.2015.09.009
Dahl TE (2014) Status and trends of prairie wetlands in the United States 1997 to 2009. U.S. Department of the Interior, Fish and Wildlife Service, Ecological Services, Washington, D.C.
McMurry ST, Belden JB, Smith LM et al (2016) Land use effects on pesticides in sediments of prairie pothole wetlands in North and South Dakota. Sci Total Environ 565:682–689. https://doi.org/10.1016/j.scitotenv.2016.04.209
doi: 10.1016/j.scitotenv.2016.04.209
pubmed: 27219502
Holloway JM, Goldhaber MB, Mills CT (2011) Carbon and nitrogen biogeochemistry of a prairie pothole wetland, Stutsman County, North Dakota, USA. Appl Geochem 26:S44–S47. https://doi.org/10.1016/j.apgeochem.2011.03.025
doi: 10.1016/j.apgeochem.2011.03.025
Dalcin Martins P, Hoyt DW, Bansal S et al (2017) Abundant carbon substrates drive extremely high sulfate reduction rates and methane fluxes in prairie pothole wetlands. Glob Change Biol 23:3107–3120. https://doi.org/10.1111/gcb.13633
doi: 10.1111/gcb.13633
Winter TC (2003) Hydrological, chemical, and biological characteristics of a prairie pothole wetland complex under highly variable climate conditions: the Cottonwood Lake area, east-central North Dakota. U.S. Dept. of the Interior, U.S. Geological Survey : U.S. Geological Survey, Information Services [distributor], Denver, CO
Maestri S, Cosentino E, Paterno M et al (2019) A rapid and accurate MinION-based workflow for tracking species biodiversity in the field. Genes 10:468. https://doi.org/10.3390/genes10060468
doi: 10.3390/genes10060468
pubmed: 31226847
pmcid: 6627956
Pruesse E, Quast C, Knittel K et al (2007) SILVA: a comprehensive online resource for quality checked and aligned ribosomal RNA sequence data compatible with ARB. Nucleic Acids Res 35:7188–7196. https://doi.org/10.1093/nar/gkm864
doi: 10.1093/nar/gkm864
pubmed: 17947321
pmcid: 2175337
Quast C, Pruesse E, Yilmaz P et al (2012) The SILVA ribosomal RNA gene database project: improved data processing and web-based tools. Nucleic Acids Res 41:D590–D596. https://doi.org/10.1093/nar/gks1219
doi: 10.1093/nar/gks1219
pubmed: 23193283
pmcid: 3531112
McMurdie PJ, Paulson JN (2015) Biomformat: an interface package for the BIOM file format. http://biom-format.org/
Oksanen J, Simpson G, Blanchet F et al (2017) Vegan: community ecology package. R package version 2.6-4. https://CRAN.R-project.org/package=vegan
R Core Team (2022) R: A language and environment for statistical computing. R Foundation for Statistical Computing, Vienna, Austria. https://www.R-project.org/
Gill JPK, Sethi N, Mohan A (2017) Analysis of the glyphosate herbicide in water, soil and food using derivatising agents. Environ Chem Lett 15:85–100. https://doi.org/10.1007/s10311-016-0585-z
doi: 10.1007/s10311-016-0585-z
Tang FHM, Jeffries TC, Vervoort RW et al (2019) Microcosm experiments and kinetic modeling of glyphosate biodegradation in soils and sediments. Sci Total Environ 658:105–115. https://doi.org/10.1016/j.scitotenv.2018.12.179
doi: 10.1016/j.scitotenv.2018.12.179
pubmed: 30572210
Pesce S, Batisson I, Bardot C et al (2009) Response of spring and summer riverine microbial communities following glyphosate exposure. Ecotoxicol Environ Saf 72:1905–1912. https://doi.org/10.1016/j.ecoenv.2009.07.004
doi: 10.1016/j.ecoenv.2009.07.004
pubmed: 19646758
Lane M, Lorenz N, Saxena J et al (2012) The effect of glyphosate on soil microbial activity, microbial community structure, and soil potassium. Pedobiologia 55:335–342. https://doi.org/10.1016/j.pedobi.2012.08.001
doi: 10.1016/j.pedobi.2012.08.001
Muturi EJ, Donthu RK, Fields CJ et al (2017) Effect of pesticides on microbial communities in container aquatic habitats. Sci Rep 7:44565. https://doi.org/10.1038/srep44565
doi: 10.1038/srep44565
pubmed: 28300212
pmcid: 5353589
Dennis PG, Kukulies T, Forstner C et al (2018) The effects of glyphosate, glufosinate, paraquat and paraquat-diquat on soil microbial activity and bacterial, archaeal and nematode diversity. Sci Rep 8:2119. https://doi.org/10.1038/s41598-018-20589-6
doi: 10.1038/s41598-018-20589-6
pubmed: 29391493
pmcid: 5794862
Widenfalk A, Bertilsson S, Sundh I, Goedkoop W (2008) Effects of pesticides on community composition and activity of sediment microbes – responses at various levels of microbial community organization. Environ Pollut 152:576–584. https://doi.org/10.1016/j.envpol.2007.07.003
doi: 10.1016/j.envpol.2007.07.003
pubmed: 17822816
Sura S, Waiser M, Tumber V et al (2012) Effects of glyphosate and two herbicide mixtures on microbial communities in prairie wetland ecosystems: a mesocosm approach. J Environ Qual 41:732–743. https://doi.org/10.2134/jeq2011.0376
doi: 10.2134/jeq2011.0376
pubmed: 22565255
Priestman MA, Funke T, Singh IM et al (2005) 5-Enolpyruvylshikimate-3-phosphate synthase from Staphylococcus aureus is insensitive to glyphosate. FEBS Lett 579:728–732. https://doi.org/10.1016/j.febslet.2004.12.057
doi: 10.1016/j.febslet.2004.12.057
pubmed: 15670836
Firdous S, Iqbal S, Anwar S, Jabeen H (2018) Identification and analysis of 5-enolpyruvylshikimate-3-phosphate synthase (EPSPS) gene from glyphosate-resistant Ochrobactrum intermedium Sq20: identification of EPSPS from Ochrobactrum intermedium Sq20. Pest Manag Sci 74:1184–1196. https://doi.org/10.1002/ps.4624
doi: 10.1002/ps.4624
pubmed: 28544077
Padgette SR, Kolacz KH, Delannay X et al (1995) Development, identification, and characterization of a glyphosate-tolerant soybean line. Crop Sci 35:1451–1461. https://doi.org/10.2135/cropsci1995.0011183X003500050032x
doi: 10.2135/cropsci1995.0011183X003500050032x
Hertel R, Gibhardt J, Martienssen M et al (2021) Molecular mechanisms underlying glyphosate resistance in bacteria. Environ Microbiol 23:2891–2905. https://doi.org/10.1111/1462-2920.15534
doi: 10.1111/1462-2920.15534
pubmed: 33876549
Allegrini M, Zabaloy MC, Gómez EDV (2015) Ecotoxicological assessment of soil microbial community tolerance to glyphosate. Sci Total Environ 533:60–68. https://doi.org/10.1016/j.scitotenv.2015.06.096
doi: 10.1016/j.scitotenv.2015.06.096
pubmed: 26150308
Dion HM, Harsh JB, Hill Jr HH (2001) Competitive sorption between glyphosate and inorganic phosphate on clay minerals and low organic matter soils. J Radioanal Nucl Chem 249:385–390. https://doi.org/10.1023/A:1013222704311
doi: 10.1023/A:1013222704311
de Jonge H, de Jonge LW, Jacobsen OH et al (2001) Glyphosate sorption in soils of different pH and phosphorus content. Soil Sci 166:230–238. https://doi.org/10.1097/00010694-200104000-00002
doi: 10.1097/00010694-200104000-00002
Guijarro KH, Aparicio V, De Gerónimo E et al (2018) Soil microbial communities and glyphosate decay in soils with different herbicide application history. Sci Total Environ 634:974–982. https://doi.org/10.1016/j.scitotenv.2018.03.393
doi: 10.1016/j.scitotenv.2018.03.393
pubmed: 29660891
Helander M, Saloniemi I, Saikkonen K (2012) Glyphosate in northern ecosystems. Trends Plant Sci 17:569–574. https://doi.org/10.1016/j.tplants.2012.05.008
doi: 10.1016/j.tplants.2012.05.008
pubmed: 22677798
Muskus AM, Miltner A, Hamer U, Nowak KM (2022) Microbial community composition and glyphosate degraders of two soils under the influence of temperature, total organic carbon and pH. Environ Pollut 297:118790. https://doi.org/10.1016/j.envpol.2022.118790
doi: 10.1016/j.envpol.2022.118790
pubmed: 35016983