Skip to main content
SpringerLink
Log in

Biological Limitations on Glyphosate Biodegradation

  • Chapter
  • First Online:
Green Technologies and Environmental Sustainability

Abstract

Glyphosate is currently considered the most important herbicide of the world due to its broad-spectrum activity, effectiveness, and loss of global patent protection. Its ubiquitous presence in the environment due to anthropogenic activities and recalcitrance has the potential to affect animal behavior and interfere with ecological processes. Despite its important role in the protection of crops, it is important to establish strategies to reduce potential human exposure or decrease its presence in the environment. To date, only one microbial enzyme known as C-P lyase is acknowledged to drive complete glyphosate mineralization. AMPA, the common metabolite product of glyphosate biodegradation, still possesses the unique C-P bond of phosphonates and retains it toxic profile and recalcitrance. Thus, it is important to consider glyphosate and AMPA biodegradation altogether. Nevertheless, the potential to develop a bioremediation process is mainly limited by the genetic regulatory system that governs the expression of the C-P lyase, as it strongly depends on low environmental levels of phosphate. Thus, the complete mineralization of this herbicide by the sole use of microorganisms would remain insufficient until (1) more research on additional genetic control mechanisms of C-P lyase expression are explored, (2) alternative enzymes are studied in detailed, or (3) more complex and elaborated processes are considered. This work explores the available information on glyphosate biodegradation over the course of 40 years of study, the different pathways involving the C-P lyase, the genetic and physiological regulatory system that governs these processes, and the factors limiting the development of glyphosate bioremediation technologies.

This is a preview of subscription content, log in via an institution to check access.

Access this chapter

Log in via an institution
Chapter
USD 29.95
Price excludes VAT (USA)
  • Available as PDF
  • Read on any device
  • Instant download
  • Own it forever
eBook
USD 169.00
Price excludes VAT (USA)
  • Available as EPUB and PDF
  • Read on any device
  • Instant download
  • Own it forever
Softcover Book
USD 219.99
Price excludes VAT (USA)
  • Compact, lightweight edition
  • Dispatched in 3 to 5 business days
  • Free shipping worldwide - see info
Hardcover Book
USD 219.99
Price excludes VAT (USA)
  • Durable hardcover edition
  • Dispatched in 3 to 5 business days
  • Free shipping worldwide - see info

Tax calculation will be finalised at checkout

Purchases are for personal use only

Institutional subscriptions

References

  • Acquavella JF, Alexander BH, Mandel JS, Gustin C, Baker B, Chapman P, Bleeke M (2004) Glyphosate biomonitoring for farmers and their families: results from the Farm Family Exposure Study. Environ Health Perspect 112:321–326

    Article  Google Scholar 

  • Adams WJ, Hallas LE, Heitkamp MA (1990) Microbes and their use to degrade N-phosphonomethylglycine in waste streams. US Pat 5288635:1–4

    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. doi:10.1016/j.jssas.2011.10.001

    Google Scholar 

  • Alexa E, Bragea M, Sumalan R, Lăzureanu A, Negrea M, Iancu S (2009) Dynamic of glyphosate mineralization in different soil types. Rom Agric Res 26:57–60

    Google Scholar 

  • Amemura M, Makino K, Shinagawa H, Nakata A (1990) Cross talk to the phosphate regulon of Escherichia coli by PhoM protein: PhoM is a histidine protein kinase and catalyzes phosphorylation of PhoB and PhoM-open reading frame 2. J Bacteriol 172:6300–3607

    Article  Google Scholar 

  • Aparicio VC, De Gerónimo E, Marino D, Primost J, Carriquiriborde P, Costa JL (2013) Environmental fate of glyphosate and aminomethylphosphonic acid in surface waters and soil of agricultural basins. Chemosphere 93:1866–1873. doi:10.1016/j.chemosphere.2013.06.041

    Article  Google Scholar 

  • Araújo ASF, Monteiro RTR, Abarkeli RB (2003) Effect of glyphosate on the microbial activity of two Brazilian soils. Chemosphere 52:799–804. doi:10.1016/S0045-6535(03)00266-2

    Article  Google Scholar 

  • Arias-Estévez M, López-Periago E, Martínez-Carballo E, Simal-Gándara J, Mejuto J-C, García-Río L (2008) The mobility and degradation of pesticides in soils and the pollution of groundwater resources. Agric Ecosyst Environ 123:247–260. doi:10.1016/j.agee.2007.07.011

    Article  Google Scholar 

  • Arregui MC, Lenardón A, Sanchez D, Maitre MI, Scotta R, Enrique S (2004) Monitoring glyphosate residues in transgenic glyphosate-resistant soybean. Pest Manag Sci 60:163–166. doi:10.1002/ps.775

    Article  Google Scholar 

  • Battaglin WA, Goolsby DA (1999) Are shifts in herbicide use reflected in concentration changes in midwestern rivers? Environ Sci Technol 33:2917–2925

    Article  Google Scholar 

  • Battaglin WA, Kolpin DW, Scribner EA, Kuivila KM, Sandstrom MW (2005) Glyphosate, other herbicides, and transformation products in midwestern streams, 2002. J Am Water Resour Assoc 41:323–332. doi:10.1111/j.1752-1688.2005.tb03738.x

    Article  Google Scholar 

  • 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. doi:10.1111/jawr.12159

    Article  Google Scholar 

  • Bazot S, Lebeau T (2008) Simultaneous mineralization of glyphosate and diuron by a consortium of three bacteria as free- and/or immobilized-cells formulations. Appl Microbiol Biotechnol 77:1351–1358. doi:10.1007/s00253-007-1259-3

    Article  Google Scholar 

  • Benachour N, Séralini G-E (2009) Glyphosate formulations induce apoptosis and necrosis in human umbilical, embryonic, and placental cells. Chem Res Toxicol 22:97–105. doi:10.1021/tx800218n

    Article  Google Scholar 

  • Benachour N, Sipahutar H, Moslemi S, Gasnier C, Travert C, Séralini GE (2007) Time- and dose-dependent effects of roundup on human embryonic and placental cells. Arch Environ Contam Toxicol 53:126–133. doi:10.1007/s00244-006-0154-8

    Article  Google Scholar 

  • Benbrook CM (2016) Trends in glyphosate herbicide use in the United States and globally. Environ Sci Eur 28:3. doi:10.1186/s12302-016-0070-0

    Article  Google Scholar 

  • Bonnet J-L, Bonnemoy F, Dusser M, Bohatier J (2007) Assessment of the potential toxicity of herbicides and their degradation products to nontarget cells using two microorganisms, the bacteria Vibrio fischeri and the ciliate Tetrahymena pyriformis. Environ Toxicol 22:78–91. doi:10.1002/tox.20237

    Article  Google Scholar 

  • Brändli D, Reinacher S (2012) Herbicides found in human urine. Ithaka J 1:270–272

    Google Scholar 

  • Cao G, Liu Y, Zhang S, Yang X, Chen R, Zhang Y, Lu W, Liu Y, Wang J, Lin M, Wang G (2012) A novel 5-enolpyruvylshikimate-3-phosphate synthase shows high glyphosate tolerance in Escherichia coli and tobacco plants. PLoS One 7:e38718. doi:10.1371/journal.pone.0038718

    Article  Google Scholar 

  • Carlisle SM, Trevors JT (1988) Glyphosate in the environment. Water Air Soil Pollut 39:409–420. doi:10.1007/BF00279485

    Google Scholar 

  • Casabé N, Piola L, Fuchs J, Oneto ML, Pamparato L, Basack S, Giménez R, Massaro R, Papa JC, Kesten E (2007) Ecotoxicological assessment of the effects of glyphosate and chlorpyrifos in an Argentine soya field. J Soils Sediments 7:232–239. doi:10.1065/jss2007.04.224

    Article  Google Scholar 

  • Cassigneul A, Benoit P, Bergheaud V, Dumeny V, Etiévant V, Goubard Y, Maylin A, Justes E, Alletto L (2016) Fate of glyphosate and degradates in cover crop residues and underlying soil: a laboratory study. Sci Total Environ 545:582–590. doi:10.1016/j.scitotenv.2015.12.052

    Article  Google Scholar 

  • Cessna AJ, Darwent AL, Townley-Smith L, Harker KN, Kirkland K (2002) Residues of glyphosate and its metabolite AMPA in field pea, barley and flax seed following preharvest applications. Can J Plant Sci 82:485–489. doi:10.4141/P01-094

    Article  Google Scholar 

  • Chaufan G, Coalova I, Ríos de Molina MDC (2014) Glyphosate commercial formulation causes cytotoxicity, oxidative effects, and apoptosis on human cells: differences with its active ingredient. Int J Toxicol 33:29–38. doi:10.1177/1091581813517906

    Article  Google Scholar 

  • Chen CM, Ye QZ, Zhu ZM, Wanner BL, Walsh CT (1990) Molecular biology of carbon-phosphorus bond cleavage. Cloning and sequencing of the phn (psiD) genes involved in alkylphosphonate uptake and C-P lyase activity in Escherichia coli B. J Biol Chem 265:4461–4471

    Google Scholar 

  • Contardo-Jara V, Klingelmann E, Wiegand C (2009) Bioaccumulation of glyphosate and its formulation Roundup Ultra in Lumbriculus variegatus and its effects on biotransformation and antioxidant enzymes. Environ Pollut 157:57–63. doi:10.1016/j.envpol.2008.07.027

    Article  Google Scholar 

  • Correia FV, Moreira JC (2010) Effects of glyphosate and 2,4-D on earthworms (Eisenia foetida) in laboratory tests. Bull Environ Contam Toxicol 85:264–268. doi:10.1007/s00128-010-0089-7

    Article  Google Scholar 

  • Dai P, Hu P, Tang J, Li Y, Li C (2016) Effect of glyphosate on reproductive organs in male rat. Acta Histochem 118:519–526. doi:10.1016/j.acthis.2016.05.009

    Article  Google Scholar 

  • Daruich J, Zirulnik F, Sofía Gimenez M (2001) Effect of the herbicide glyphosate on enzymatic activity in pregnant rats and their fetuses. Environ Res 85:226–231. doi:10.1006/enrs.2000.4229

    Article  Google Scholar 

  • Davis AM, Thorburn PJ, Lewis SE, Bainbridge ZT, Attard SJ, Milla R, Brodie JE (2013) Environmental impacts of irrigated sugarcane production: herbicide run-off dynamics from farms and associated drainage systems. Agric Ecosyst Environ 180:123–135. doi:10.1016/j.agee.2011.06.019

    Article  Google Scholar 

  • Dick RE, Quinn JP (1995) Glyphosate-degrading isolates from environmental samples: occurrence and pathways of degradation. Appl Microbiol Biotechnol 43:545–550. doi:10.1007/BF00218464

    Article  Google Scholar 

  • Dill GM, Sammons RD, Feng PCC, Kohn F, Kretzmer K, Mehrsheikh A, Bleeke M, Honegger JL, Farmer D, Wright D, Haupfear EA (2010) Glyphosate: discovery, development, applications, and properties. In: Glyphosate resistance in crops and weeds: history, development, and management. Wiley, Hoboken, NJ, pp 1–33

    Chapter  Google Scholar 

  • Dollinger J, Dagès C, Voltz M (2015) Glyphosate sorption to soils and sediments predicted by pedotransfer functions. Environ Chem Lett 13:293–307. doi:10.1007/s10311-015-0515-5

    Article  Google Scholar 

  • Duke SO (2011) Glyphosate degradation in glyphosate-resistant and -susceptible crops and weeds. J Agric Food Chem 59:5835–5841. doi:10.1021/jf102704x

    Article  Google Scholar 

  • Duke SO, Lydon J, Koskinen WC, Moorman TB, Chaney RL, Hammerschmidt R (2012) Glyphosate effects on plant mineral nutrition, crop rhizosphere microbiota, and plant disease in glyphosate-resistant crops. J Agric Food Chem 60:10375–10397. doi:10.1021/jf302436u

    Article  Google Scholar 

  • DuPont Pioneer (2016) Glyphosate use for optimum field performance. https://www.pioneer.com/home/site/us/agronomy/glyphosate-optimum-performance

  • Dyhrman S, Ammerman J, Van Mooy B (2007) Microbes and the marine phosphorus cycle. Oceanography 20:110–116. doi:10.5670/oceanog.2007.54

    Article  Google Scholar 

  • Edgerton MD (2009) Increasing crop productivity to meet global needs for feed, food, and fuel. Plant Physiol 149:7–13. doi:10.1104/pp.108.130195

    Article  Google Scholar 

  • Ermakova IT, Kiseleva NI, Shushkova T, Zharikov M, Zharikov GA, Leontievsky AA (2010) Bioremediation of glyphosate-contaminated soils. Appl Microbiol Biotechnol 88:585–594. doi:10.1007/s00253-010-2775-0

    Article  Google Scholar 

  • Evans SC, Shaw EM, Rypstra AL (2010) Exposure to a glyphosate-based herbicide affects agrobiont predatory arthropod behaviour and long-term survival. Ecotoxicology 19:1249–1257. doi:10.1007/s10646-010-0509-9

    Article  Google Scholar 

  • Food and Agriculture Organization of the United Nations (2000) FAO specifications and evaluations for plant protection products: Glyphosate, N-(phosphonomethyl)glycine. http://www.fao.org/fileadmin/templates/agphome/documents/Pests_Pesticides/Specs/glypho01.pdf

  • Food and Agriculture Organization and World Health Organization of the United Nations (2016) Joint FAO/WHO meeting on pesticide residues. http://www.who.int/foodsafety/jmprsummary2016.pdf?ua=1

  • Fu W, Guo Q, Wang J (2010) Solubility of glyphosate in ethanol + water, 1-propanol + water, and 2-propanol + water from (293 to 333) K. J Chem Eng Data 55:3915–3917. doi:10.1021/je901006c

    Article  Google Scholar 

  • Funke T, Yang Y, Han H, Healy-Fried M, Olesen S, Becker A, Schonbrunn E (2009) Structural basis of glyphosate resistance resulting from the double mutation Thr97 -> Ile and Pro101 -> Ser in 5-enolpyruvylshikimate-3-phosphate synthase from Escherichia coli. J Biol Chem 284:9854–9860. doi:10.1074/jbc.M809771200

    Article  Google Scholar 

  • García-Pérez JA, Alarcón-Gutiérrez E, Perroni Y, Barois I (2014) Earthworm communities and soil properties in shaded coffee plantations with and without application of glyphosate. Appl Soil Ecol 83:230–237. doi:10.1016/j.apsoil.2013.09.006

    Article  Google Scholar 

  • Gasnier C, Dumont C, Benachour N, Clair E, Chagnon M-C, Séralini G-E (2009) Glyphosate-based herbicides are toxic and endocrine disruptors in human cell lines. Toxicology 262:184–191. doi:10.1016/j.tox.2009.06.006

    Article  Google Scholar 

  • Gebhard S, Cook GM (2008) Differential regulation of high-affinity phosphate transport systems of Mycobacterium smegmatis: identification of PhnF, a repressor of the phnDCE operon. J Bacteriol 190:1335–1343. doi:10.1128/JB.01764-07

    Article  Google Scholar 

  • Gilland B (2002) World population and food supply: can food production keep pace with population growth in the next half-century? Food Policy 27:47–63. doi:10.1016/S0306-9192(02)00002-7

    Article  Google Scholar 

  • Gimsing AL, Borggaard OK, Jacobsen OS, Aamand J, Sørensen J (2004) Chemical and microbiological soil characteristics controlling glyphosate mineralisation in Danish surface soils. Appl Soil Ecol 27:233–242. doi:10.1016/j.apsoil.2004.05.007

    Article  Google Scholar 

  • Grunewald K, Schmidt W, Unger C, Hanschmann G (2001) Behavior of glyphosate and aminomethylphosphonic acid (AMPA) in soils and water of reservoir Radeburg II catchment (Saxony/Germany). J Plant Nutr Soil Sci 164:65–70. doi:10.1002/1522-2624(200102)164:1<65::AID-JPLN65>3.0.CO;2-G

    Article  Google Scholar 

  • Guyton KZ, Loomis D, Grosse Y, El Ghissassi F, Benbrahim-Tallaa L, Guha N, Scoccianti C, Mattock H, Straif K (2015) Carcinogenicity of tetrachlorvinphos, parathion, malathion, diazinon, and glyphosate. Lancet Oncol 16:490–491. doi:10.1016/S1470-2045(15)70134-8

    Article  Google Scholar 

  • Hallas LE, Adams WJ, Heitkamp MA (1992) Glyphosate degradation by immobilized bacteria: field studies with industrial wastewater effluent. Appl Environ Microbiol 58:1215–1219

    Google Scholar 

  • Heitkamp MA, Adams WJ, Hallas LE (1992) Glyphosate degradation by immobilized bacteria: laboratory studies showing feasibility for glyphosate removal from waste water. Can J Microbiol 38:921–928

    Article  Google Scholar 

  • Hénault-Ethier L (2016) Backgrounder: glyphosate: ubiquitous and worrisome. Canadian Association of Physicians for the Environment, Toronto, pp 1–5

    Google Scholar 

  • Hetherington PR, Reynolds TL, Marshall G, Kirkwood RC (1999) The absorption, translocation and distribution of the herbicide glyphosate in maize expressing the CP-4 transgene. J Exp Bot 50:1567–1576

    Article  Google Scholar 

  • Honeycutt Z, Rowlands H (2014) Glyphosate testing report: findings in American mothers’ breast milk, urine and water. http://www.momsacrossamerica.com/glyphosate_testing_results

  • Hove-Jensen B, Rosenkrantz TJ, Zechel DL, Willemoes M (2010) Accumulation of intermediates of the carbon-phosphorus lyase pathway for phosphonate degradation in phn mutants of Escherichia coli. J Bacteriol 192:370–374. doi:10.1128/JB.01131-09

    Article  Google Scholar 

  • Hove-Jensen B, McSorley FR, Zechel DL (2011) Physiological role of phnP-specified phosphoribosyl cyclic phosphodiesterase in catabolism of organophosphonic acids by the carbon-phosphorus lyase pathway. J Am Chem Soc 133:3617–3624. doi:10.1021/ja1102713

    Article  Google Scholar 

  • Hove-Jensen B, Zechel DL, Jochimsen B (2014) Utilization of glyphosate as phosphate source: biochemistry and genetics of bacterial carbon-phosphorus lyase. Microbiol Mol Biol Rev 78:176–197. doi:10.1128/MMBR.00040-13

    Article  Google Scholar 

  • Huang J, Su Z, Xu Y (2005) The evolution of microbial phosphonate degradative pathways. J Mol Evol 61:682–690. doi:10.1007/s00239-004-0349-4

    Article  Google Scholar 

  • Hulett FM, Lee J, Shi L, Sun G, Chesnut R, Sharkova E, Duggan MF, Kapp N (1994) Sequential action of two-component genetic switches regulates the PHO regulon in Bacillus subtilis. J Bacteriol 176:1348–1358

    Article  Google Scholar 

  • Ilikchyan IN, McKay RML, Zehr JP, Dyhrman ST, Bullerjahn GS (2009) Detection and expression of the phosphonate transporter gene phnD in marine and freshwater picocyanobacteria. Environ Microbiol 11:1314–1324. doi:10.1111/j.1462-2920.2009.01869.x

    Article  Google Scholar 

  • Ilikchyan IN, McKay RML, Kutovaya OA, Condon R, Bullerjahn GS (2010) Seasonal expression of the picocyanobacterial phosphonate transporter gene phnD in the Sargasso Sea. Front Microbiol 1:135. doi:10.3389/fmicb.2010.00135

    Article  Google Scholar 

  • International Agency for Research on Cancer (2015) Some organophosphate insecticides and herbicides: diazinon, glyphosate, malathion, parathion, and tetrachlorvinphos. IARC Monogr Eval Carcinog Risks to Humans 112:1–92

    Google Scholar 

  • Jacob GS, Garbow JR, Hallas LE, Kimack NM, Kishore GM, Schaefer J (1988) Metabolism of glyphosate in Pseudomonas sp. strain LBr. Appl Environ Microbiol 54:2953–2958

    Google Scholar 

  • Jacquel N, Lo CW, Wei YH, Wu HS, Wang SS (2008) Isolation and purification of bacterial poly(3-hydroxyalkanoates). Biochem Eng J 39:15–27. doi:10.1016/j.bej.2007.11.029

    Article  Google Scholar 

  • Jaworska J, Van Genderen-Takken H, Hanstveit A, van de Plassche E, Feijtel T (2002) Environmental risk assessment of phosphonates, used in domestic laundry and cleaning agents in the Netherlands. Chemosphere 47:655–665. doi:10.1016/S0045-6535(01)00328-9

    Article  Google Scholar 

  • Kamat SS, Williams HJ, Dangott LJ, Chakrabarti M, Raushel FM (2013) The catalytic mechanism for aerobic formation of methane by bacteria. Nature 497:132–136. doi:10.1038/nature12061

    Article  Google Scholar 

  • Karl DM, Beversdorf L, Björkman KM, Church MJ, Martinez A, Delong EF (2008) Aerobic production of methane in the sea. Nat Geosci 1:473–478. doi:10.1038/ngeo234

    Article  Google Scholar 

  • Kertesz M, Elgorriaga A, Amrhein N (1991) Evidence for two distinct phosphonate-degrading enzymes (C-P lyases) in Arthrobacter sp. GLP-1. Biodegradation 2:53–59

    Article  Google Scholar 

  • Kertesz MA, Cook AM, Leisinger T (1994) Microbial metabolism of sulfur- and phosphorus-containing xenobiotics. FEMS Microbiol Rev 15:195–215

    Article  Google Scholar 

  • Kishore GM, Jacob GS (1987) Degradation of glyphosate by Pseudomonas sp. PG2982 via a sarcosine intermediate. J Biol Chem 262:12164–12168

    Google Scholar 

  • Kolowith LC, Ingall ED, Benner R (2001) Composition and cycling of marine organic phosphorus. Limnol Oceanogr 46:309–320. doi:10.4319/lo.2001.46.2.0309

    Article  Google Scholar 

  • Kononova SV, Nesmeyanova MA (2002) Phosphonates and their degradation by microorganisms. Biochemistry (Mosc) 67:184–195. doi:10.1023/A:1014409929875

    Article  Google Scholar 

  • Krüger M, Schledorn P, Schrödl W, Hoppe H-W, Lutz W (2014) Detection of glyphosate residues in animals and humans. J Environ Anal Toxocology 4:210. doi:10.4172/2161-0525.1000210

    Google Scholar 

  • Kryuchkova YV, Burygin GL, Gogoleva NE, Gogolev YV, Chernyshova MP, Makarov OE, Fedorov EE, Turkovskaya OV (2014) Isolation and characterization of a glyphosate-degrading rhizosphere strain, Enterobacter cloacae K7. Microbiol Res 169:99–105. doi:10.1016/j.micres.2013.03.002

    Article  Google Scholar 

  • Krzyśko-Łupicka T, Orlik A (1997) The use of glyphosate as the sole source of phosphorus or carbon for the selection of soil-borne fungal strains capable to degrade this herbicide. Chemosphere 34:2601–2605. doi:10.1016/S0045-6535(97)00103-3

    Article  Google Scholar 

  • Kwiatkowska M, Huras B, Bukowska B (2014) The effect of metabolites and impurities of glyphosate on human erythrocytes (in vitro). Pestic Biochem Physiol 109:34–43. doi:10.1016/j.pestbp.2014.01.003

    Article  Google Scholar 

  • Lesueur C, Pfeffer M, Fuerhacker M (2005) Photodegradation of phosphonates in water. Chemosphere 59:685–691. doi:10.1016/j.chemosphere.2004.10.049

    Article  Google Scholar 

  • Liu C-M, McLean PA, Sookdeo CC, Cannon FC (1991) Degradation of the herbicide glyphosate by members of the family Rhizobiaceae. Appl Environ Microbiol 57:1799–1804

    Google Scholar 

  • Ludtke D, Bernstein J, Hamilton C, Torriani A (1984) Identification of the phoM gene product and its regulation in Escherichia coli K-12. J Bacteriol 159:19–25

    Google Scholar 

  • Lund-Høie K, Friestad HO (1986) Photodegradation of the herbicide glyphosate in water. Bull Environ Contam Toxicol 36:723–729. doi:10.1007/BF01623575

    Article  Google Scholar 

  • Makino K, Shinagawa H, Nakata A (1984) Cloning and characterization of the alkaline phosphatase positive regulatory gene (phoM) of Escherichia coli. Mol Gen Genet 195:381–390

    Article  Google Scholar 

  • Makino K, Shinagawa H, Amemura M, Kawamoto T, Yamada M, Nakata A (1989) Signal transduction in the phosphate regulon of Escherichia coli involves phosphotransfer between PhoR and PhoB proteins. J Mol Biol 210:551–559. doi:10.1016/0022-2836(89)90131-9

    Article  Google Scholar 

  • Makino K, Kim SK, Shinagawa H, Amemura M, Nakata A (1991) Molecular analysis of the cryptic and functional phn operons for phosphonate use in Escherichia coli K-12. J Bacteriol 173:2665–2672

    Article  Google Scholar 

  • Mamy L, Barriuso E (2005) Glyphosate adsorption in soils compared to herbicides replaced with the introduction of glyphosate resistant crops. Chemosphere 61:844–855. doi:10.1016/j.chemosphere.2005.04.051

    Article  Google Scholar 

  • Mamy L, Gabrielle B, Barriuso E (2008) Measurement and modelling of glyphosate fate compared with that of herbicides replaced as a result of the introduction of glyphosate-resistant oilseed rape. Pest Manag Sci 64:262–275. doi:10.1002/ps.1519

    Article  Google Scholar 

  • Mamy L, Barriuso E, Gabrielle B (2016) Glyphosate fate in soils when arriving in plant residues. Chemosphere 154:425–433. doi:10.1016/j.chemosphere.2016.03.104

    Article  Google Scholar 

  • McAuliffe KS, Hallas LE, Kulpa CF (1990) Glyphosate degradation by Agrobacterium radiobacter isolated from activated sludge. J Ind Microbiol 6:219–221. doi:10.1007/BF01577700

    Article  Google Scholar 

  • McBride M, Kung K-H (1989) Complexation of glyphosate and related ligands with iron (III). Soil Sci Soc Am J 53:1668. doi:10.2136/sssaj1989.03615995005300060009x

    Article  Google Scholar 

  • McGrath JW, Ternan NG, Quinn JP (1997) Utilization of organophosphonates by environmental micro-organisms. Lett Appl Microbiol 24:69–73. doi:10.1046/j.1472-765X.1997.00350.x

    Article  Google Scholar 

  • McGrath JW, Chin JP, Quinn JP (2013) Organophosphonates revealed: new insights into the microbial metabolism of ancient molecules. Nat Rev Microbiol 11:412–419. doi:10.1038/nrmicro3011

    Article  Google Scholar 

  • Metcalf WW, Wanner BL (1991) Involvement of the Escherichia coli phn (psiD) gene cluster in assimilation of phosphorus in the form of phosphonates, phosphite, Pi esters, and Pi. J Bacteriol 173:587–600

    Article  Google Scholar 

  • Metcalf WW, Wanner BL (1993) Mutational analysis of an Escherichia coli fourteen-gene operon for phosphonate degradation, using TnphoA’ elements. J Bacteriol 175:3430–3442

    Article  Google Scholar 

  • Mink PJ, Mandel JS, Sceurman BK, Lundin JI (2012) Epidemiologic studies of glyphosate and cancer: a review. Regul Toxicol Pharmacol 63:440–452. doi:10.1016/j.yrtph.2012.05.012

    Article  Google Scholar 

  • Moneke AN, Okpala GN, Anyanwu CU (2010) Biodegradation of glyphosate herbicide in vitro using bacterial isolates from four rice fields. African J Biotechnol 9:4067–4074

    Google Scholar 

  • Morowati M (2000) Histochemical and histopathological study of the intestine of the earthworm (Pheretima elongata) exposed to a field dose of the herbicide glyphosate. Environmentalist 20:105–111. doi:10.1023/A:1006704009184

    Article  Google Scholar 

  • Myers JP, Antoniou MN, Blumberg B, Carroll L, Colborn T, Everett LG, Hansen M, Landrigan PJ, Lanphear BP, Mesnage R, Vandenberg LN, vom Saal FS, Welshons W V., Benbrook CM (2016) Concerns over use of glyphosate-based herbicides and risks associated with exposures: a consensus statement. Environ Heal 15:19. doi: 10.1186/s12940-016-0117-0

  • National Pesticide Information Center (2010) Glyphosate General Fact Sheet. http://npic.orst.edu/factsheets/glyphogen.html.

  • Newman MM, Hoilett N, Lorenz N, Dick RP, Liles MR, Ramsier C, Kloepper JW (2016) Glyphosate effects on soil rhizosphere-associated bacterial communities. Sci Total Environ 543:155–160. doi:10.1016/j.scitotenv.2015.11.008

    Article  Google Scholar 

  • Niemann L, Sieke C, Pfeil R, Solecki R (2015) A critical review of glyphosate findings in human urine samples and comparison with the exposure of operators and consumers. J für Verbraucherschutz und Leb 10:3–12. doi:10.1007/s00003-014-0927-3

    Article  Google Scholar 

  • Nourouzi MM, Chuah TG, Choong TSY, Lim CJ (2011) Glyphosate utilization as the source of carbon: isolation and identification of new bacteria. E-Journal Chem 8:1582–1587. doi:10.1155/2011/614109

    Article  Google Scholar 

  • Nowack B (2003) Environmental chemistry of phosphonates. Water Res 37:2533–2546. doi:10.1016/S0043-1354(03)00079-4

    Article  Google Scholar 

  • Oerke E (2006) Crop losses to pests. J Agric Sci 144:31–43. doi:10.1017/S0021859605005708

    Article  Google Scholar 

  • Peruzzo PJ, Porta AA, Ronco AE (2008) Levels of glyphosate in surface waters, sediments and soils associated with direct sowing soybean cultivation in north pampasic region of Argentina. Environ Pollut 156:61–66. doi:10.1016/j.envpol.2008.01.015

    Article  Google Scholar 

  • Pesce S, Fajon C, Bardot C, Bonnemoy F, Portelli C, Bohatier J (2008) Longitudinal changes in microbial planktonic communities of a French river in relation to pesticide and nutrient inputs. Aquat Toxicol 86:352–360. doi:10.1016/j.aquatox.2007.11.016

    Article  Google Scholar 

  • Piccolo A, Celano G (1994) Hydrogen-bonding interactions between the herbicide glyphosate and water-soluble humic substances. Environ Toxicol Chem 13:1737–1741. doi:10.1002/etc.5620131104

    Article  Google Scholar 

  • Pimentel D (2005) Environmental and economic costs of the application of pesticides primarily in the United States. Environ Dev Sustain 7:229–252. doi:10.1007/s10668-005-7314-2

    Article  Google Scholar 

  • Pipke R, Amrhein N (1988) Degradation of the phosphonate herbicide glyphosate by Arthrobacter atrocyaneus ATCC 13752. Appl Environ Microbiol 54:1293–1296

    Google Scholar 

  • Portier CJ, Armstrong BK, Baguley BC, Baur X, Belyaev I, Bellé R, Belpoggi F, Biggeri A, Bosland MC, Bruzzi P, Budnik LT, Bugge MD, Burns K, Calaf GM, Carpenter DO, Carpenter HM, López-Carrillo L, Clapp R, Cocco P, Consonni D, Comba P, Craft E, Dalvie MA, Davis D, Demers PA, De Roos AJ, DeWitt J, Forastiere F, Freedman JH, Fritschi L, Gaus C, Gohlke JM, Goldberg M, Greiser E, Hansen J, Hardell L, Hauptmann M, Huang W, Huff J, James MO, Jameson CW, Kortenkamp A, Kopp-Schneider A, Kromhout H, Larramendy ML, Landrigan PJ, Lash LH, Leszczynski D, Lynch CF, Magnani C, Mandrioli D, Martin FL, Merler E, Michelozzi P, Miligi L, Miller AB, Mirabelli D, Mirer FE, Naidoo S, Perry MJ, Petronio MG, Pirastu R, Portier RJ, Ramos KS, Robertson LW, Rodriguez T, Röösli M, Ross MK, Roy D, Rusyn I, Saldiva P, Sass J, Savolainen K, Scheepers PTJ, Sergi C, Silbergeld EK, Smith MT, Stewart BW, Sutton P, Tateo F, Terracini B, Thielmann HW, Thomas DB, Vainio H, Vena JE, Vineis P, Weiderpass E, Weisenburger DD, Woodruff TJ, Yorifuji T, Yu IJ, Zambon P, Zeeb H, Zhou S-F (2016) Differences in the carcinogenic evaluation of glyphosate between the International Agency for Research on Cancer (IARC) and the European Food Safety Authority (EFSA). J Epidemiol Community Health 70:741–745. doi:10.1136/jech-2015-207005

    Article  Google Scholar 

  • Powles SB, Lorraine-Colwill DF, Dellow JJ, Preston C (1998) Evolved resistance to glyphosate in rigid ryegrass (Lolium rigidum) in Australia. Weed Sci 46:604–607

    Google Scholar 

  • Quinn JP, Kulakova AN, Cooley NA, McGrath JW (2007) New ways to break an old bond: the bacterial carbon-phosphorus hydrolases and their role in biogeochemical phosphorus cycling. Environ Microbiol 9:2392–2400. doi:10.1111/j.1462-2920.2007.01397.x

    Article  Google Scholar 

  • Relyea RA (2005a) The lethal impact of roundup on aquatic and terrestrial amphibians. Ecol Appl 15:1118–1124. doi:10.1890/04-1291

    Article  Google Scholar 

  • Relyea RA (2005b) The impact of insecticides and herbicides on the biodiversity and productivity of aquatic communities. Ecol Appl 15:618–627. doi:10.1890/03-5342

    Article  Google Scholar 

  • Richard S, Moslemi S, Sipahutar H, Benachour N, Seralini G-E (2005) Differential effects of glyphosate and roundup on human placental cells and aromatase. Environ Health Perspect 113:716–720. doi:10.1289/ehp.7728

    Article  Google Scholar 

  • Rittman S, Wrinn KM, Evans SC, Webb AW, Rypstra AL (2013) Glyphosate-based herbicide has contrasting effects on prey capture by two co-occurring wolf spider species. J Chem Ecol 39:1247–1253. doi:10.1007/s10886-013-0353-5

    Article  Google Scholar 

  • Rizk SS, Cuneo MJ, Hellinga HW (2006) Identification of cognate ligands for the Escherichia coli phnD protein product and engineering of a reagentless fluorescent biosensor for phosphonates. Protein Sci 15:1745–1751. doi:10.1110/ps.062135206

    Article  Google Scholar 

  • Rueppel ML, Brightwell BB, Schaefer J, Marvel JT (1977) Metabolism and degradation of glyphosate in soil and water. J Agric Food Chem 25:517–528

    Article  Google Scholar 

  • Sabullah MK, Rahman MF, Ahmad SA, Sulaiman MR, Shukor MS, Shamaan NA, Shukor MY (2016) Isolation and characterization of a molybdenum-reducing and glyphosate-degrading Klebsiella oxytoca strain SAW-5 in soils from Sarawa. AGRIVITA 38:1–13. doi:10.17503/agrivita.v38i1.654

    Google Scholar 

  • Samain J-F, McCombie H (2008) Summer mortality of Pacific oyster Crassostrea gigas the Morest Project. Éditions Quæ

    Google Scholar 

  • Santos-Beneit F (2015) The Pho regulon: a huge regulatory network in bacteria. Front Microbiol 6:402. doi:10.3389/fmicb.2015.00402

    Article  Google Scholar 

  • Seweryn P, Van LB, Kjeldgaard M, Russo CJ, Passmore LA, Hove-Jensen B, Jochimsen B, Brodersen DE (2015) Structural insights into the bacterial carbon-phosphorus lyase machinery. Nature 525:68–72. doi:10.1038/nature14683

    Article  Google Scholar 

  • Shinabarger DL, Braymer HD (1986) Glyphosate catabolism by Pseudomonas sp. strain PG2982. J Bacteriol 168:702–707

    Article  Google Scholar 

  • Shushkova TV, Ermakova IT, Sviridov AV, Leontievsky AA (2012) Biodegradation of glyphosate by soil bacteria: optimization of cultivation and the method for active biomass storage. Microbiology 81:44–50. doi:10.1134/S0026261712010134

    Article  Google Scholar 

  • Skark C, Zullei-seibert N, Schöttler U, Schlett C (1998) The occurrence of glyphosate in surface water. Int J Environ Anal Chem 70:93–104. doi:10.1080/03067319808032607

    Article  Google Scholar 

  • Soltani N, Dille AJ, Burke IC, Everman WJ, VanGessel MJ, Davis VM, Sikkema PH (2016) Potential corn yield losses due to weeds in North America. Weed Technol. doi:10.1614/WT-D-16-00046.1

    Google Scholar 

  • Sprankle P, Meggitt WF, Penner D (1975) Adsorption, mobility, and microbial degradation of glyphosate in the soil. Weed Sci 23:229–234

    Google Scholar 

  • Springett JA, Gray RAJ (1992) Effect of repeated low doses of biocides on the earthworm Aporrectodea caliginosa in laboratory culture. Soil Biol Biochem 24:1739–1744. doi:10.1016/0038-0717(92)90180-6

    Article  Google Scholar 

  • Struger J, Thompson D, Staznik B, Martin P, McDaniel T, Marvin C (2008) Occurrence of glyphosate in surface waters of Southern Ontario. Bull Environ Contam Toxicol 80:378–384. doi:10.1007/s00128-008-9373-1

    Article  Google Scholar 

  • Struger J, Van Stempvoort DR, Brown SJ (2015) Sources of aminomethylphosphonic acid (AMPA) in urban and rural catchments in Ontario, Canada: glyphosate or phosphonates in wastewater? Environ Pollut 204:289–297. doi:10.1016/j.envpol.2015.03.038

    Article  Google Scholar 

  • Sviridov AV, Shushkova TV, Ermakova IT, Ivanova EV, Epiktetov DO, Leontievsky AA (2015) Microbial degradation of glyphosate herbicides (Review). Appl Biochem Microbiol 51:188–195. doi:10.1134/S0003683815020209

    Article  Google Scholar 

  • Tang X, Zhu B, Katou H (2012) A review of rapid transport of pesticides from sloping farmland to surface waters: processes and mitigation strategies. J Environ Sci 24:351–361. doi:10.1016/S1001-0742(11)60753-5

    Article  Google Scholar 

  • Tay B-Y, Lokesh BE, Lee C-Y, Sudesh K (2010) Polyhydroxyalkanoate (PHA) accumulating bacteria from the gut of higher termite Macrotermes carbonarius (Blattodea: Termitidae). World J Microbiol Biotechnol 26:1015–1024. doi:10.1007/s11274-009-0264-3

    Article  Google Scholar 

  • Ternan NG, Quinn JP (1998) Phosphate starvation-independent 2-aminoethylphosphonic acid biodegradation in a newly isolated strain of Pseudomonas putida, NG2. Syst Appl Microbiol 21:346–352. doi:10.1016/S0723-2020(98)80043-X

    Article  Google Scholar 

  • Thongprakaisang S, Thiantanawat A, Rangkadilok N, Suriyo T, Satayavivad J (2013) Glyphosate induces human breast cancer cells growth via estrogen receptors. Food Chem Toxicol 59:129–136. doi:10.1016/j.fct.2013.05.057

    Article  Google Scholar 

  • Tommassen J, de Geus P, Lugtenberg B, Hackett J, Reeves P (1982) Regulation of the pho regulon of Escherichia coli K-12. J Mol Biol 157:265–274. doi:10.1016/0022-2836(82)90233-9

    Article  Google Scholar 

  • Transparency Market Research (2014) Glyphosate industry analysis, share, size, growth, trends and forecast 2013–2019. http://www.prnewswire.com/news-releases/global-glyphosate-market-is-expected-to-reach-usd-879-billion-by-2019-transparency-market-research-244861481.html

  • Tsui MTK, Wang W-X, Chu LM (2005) Influence of glyphosate and its formulation (Roundup®) on the toxicity and bioavailability of metals to Ceriodaphnia dubia. Environ Pollut 138:59–68. doi:10.1016/j.envpol.2005.02.018

    Article  Google Scholar 

  • Van Mooy BAS, Krupke A, Dyhrman ST, Fredricks HF, Frischkorn KR, Ossolinski JE, Repeta DJ, Rouco M, Seewald JD, Sylva SP (2015) Major role of planktonic phosphate reduction in the marine phosphorus redox cycle. Science 348(80):783–785. doi:10.1126/science.aaa8181

    Article  Google Scholar 

  • Van Stempvoort DR, Roy JW, Brown SJ, Bickerton G (2014) Residues of the herbicide glyphosate in riparian groundwater in urban catchments. Chemosphere 95:455–463. doi:10.1016/j.chemosphere.2013.09.095

    Article  Google Scholar 

  • Veiga F, Zapata J, Fernandez MM, Alvarez E (2001) Dynamics of glyphosate and aminomethylphosphonic acid in a forest soil in Galicia, north-west Spain. Sci Total Environ 271:135–144. doi:10.1016/S0048-9697(00)00839-1

    Article  Google Scholar 

  • Verrell P, Van Buskirk E (2004) As the worm turns: Eisenia fetida avoids soil contaminated by a glyphosate-based herbicide. Bull Environ Contam Toxicol 72:219–224. doi:10.1007/s00128-003-9134-0

    Article  Google Scholar 

  • Villarreal-Chiu JF, Quinn JP, McGrath JW (2012) The genes and enzymes of phosphonate metabolism by bacteria, and their distribution in the marine environment. Front Microbiol 3:19. doi:10.3389/fmicb.2012.00019

    Article  Google Scholar 

  • Wanner BL (1994) Molecular genetics of carbon-phosphorus bond cleavage in bacteria. Biodegradation 5:175–184. doi:10.1007/BF00696458

    Article  Google Scholar 

  • Wanner BL (1996) Signal transduction in the control of phosphate-regulated genes of Escherichia coli. Kidney Int 49:964–967. doi:10.1038/ki.1996.136

    Article  Google Scholar 

  • Wanner BL, Wilmes-Riesenberg MR (1992) Involvement of phosphotransacetylase, acetate kinase, and acetyl phosphate synthesis in control of the phosphate regulon in Escherichia coli. J Bacteriol 174:2124–2130

    Article  Google Scholar 

  • White AK, Metcalf WW (2004) Two C-P lyase operons in Pseudomonas stutzeri and their roles in the oxidation of phosphonates, phosphite, and hypophosphite. J Bacteriol 186:4730–4739. doi:10.1128/JB.186.14.4730-4739.2004

    Article  Google Scholar 

  • Williams GM, Kroes R, Munro IC (2000) Safety evaluation and risk assessment of the herbicide roundup and its active ingredient, glyphosate, for humans. Regul Toxicol Pharmacol 31:117–165. doi:10.1006/rtph.1999.1371

    Article  Google Scholar 

  • Yasmin S, D’Souza D (2007) Effect of pesticides on the reproductive output of Eisenia fetida. Bull Environ Contam Toxicol 79:529–532. doi:10.1007/s00128-007-9269-5

    Article  Google Scholar 

  • Yu X, Yu T, Yin G, Dong Q, An M, Wang H, Ai C (2015) Glyphosate biodegradation and potential soil bioremediation by Bacillus subtilis strain Bs-15. Genet Mol Res 14:14717–14730. doi:10.4238/2015.November.18.37

    Article  Google Scholar 

  • Zaller JG, Heigl F, Ruess L, Grabmaier A (2014) Glyphosate herbicide affects belowground interactions between earthworms and symbiotic mycorrhizal fungi in a model ecosystem. Sci Rep 4:519–530. doi:10.1038/srep05634

    Google Scholar 

  • Zhang C, Hu X, Luo J, Wu Z, Wang L, Li B, Wang Y, Sun G (2015) Degradation dynamics of glyphosate in different types of citrus orchard soils in China. Molecules 20:1161–1175. doi:10.3390/molecules20011161

    Article  Google Scholar 

  • Zhou J, Tao B, Messersmith CG (2006) Soil dust reduces glyphosate efficacy. Weed Sci 54:1132–1136. doi:10.1614/WS-06-107R.1

    Article  Google Scholar 

  • Zouaoui K, Dulaurent S, Gaulier JM, Moesch C, Lachâtre G (2013) Determination of glyphosate and AMPA in blood and urine from humans: about 13 cases of acute intoxication. Forensic Sci Int 226:e20–e25. doi:10.1016/j.forsciint.2012.12.010

    Article  Google Scholar 

Download references

Author information

Authors and Affiliations

  1. Facultad de Ciencias Químicas, Laboratorio de Biotecnología, Universidad Autonoma de Nuevo Leon, Av. Universidad s/n, Cd. Universitaria, San Nicolás de los Garza, N.L, 66455, Mexico

    Juan Francisco Villarreal-Chiu & Alejandra Guadalupe Acosta-Cortés

  2. Department of Environmental Science, School of Earth Sciences, Central University of Rajasthan, Ajmer, Rajasthan, 305817, India

    Shardendu Kumar & Garima Kaushik

Authors
  1. Juan Francisco Villarreal-Chiu
    View author publications

    You can also search for this author in PubMed Google Scholar

  2. Alejandra Guadalupe Acosta-Cortés
    View author publications

    You can also search for this author in PubMed Google Scholar

  3. Shardendu Kumar
    View author publications

    You can also search for this author in PubMed Google Scholar

  4. Garima Kaushik
    View author publications

    You can also search for this author in PubMed Google Scholar

Corresponding author

Correspondence to Juan Francisco Villarreal-Chiu .

Editor information

Editors and Affiliations

  1. Department of Environmnetal Science, School of Earth Sciences, Central University of Rajasthan, Ajmer, Rajasthan, India

    Ritu Singh

  2. School for Environmental Science, Babasaheb Bhimrao Ambedkar University, Lucknow, Uttar Pradesh, India

    Sanjeev Kumar

Rights and permissions

Reprints and permissions

Copyright information

© 2017 Springer International Publishing AG

About this chapter

Cite this chapter

Villarreal-Chiu, J.F., Acosta-Cortés, A.G., Kumar, S., Kaushik, G. (2017). Biological Limitations on Glyphosate Biodegradation. In: Singh, R., Kumar, S. (eds) Green Technologies and Environmental Sustainability. Springer, Cham. https://doi.org/10.1007/978-3-319-50654-8_8

Download citation

  • DOI: https://doi.org/10.1007/978-3-319-50654-8_8

  • Published:

  • Publisher Name: Springer, Cham

  • Print ISBN: 978-3-319-50653-1

  • Online ISBN: 978-3-319-50654-8

  • eBook Packages: EnergyEnergy (R0)

Publish with us

Policies and ethics

Search

Navigation