Current Microbiology

, Volume 66, Issue 4, pp 350–358 | Cite as

The Effect of Glyphosate on Potential Pathogens and Beneficial Members of Poultry Microbiota In Vitro

  • Awad A. ShehataEmail author
  • Wieland Schrödl
  • Alaa. A. Aldin
  • Hafez M. Hafez
  • Monika Krüger


The use of glyphosate modifies the environment which stresses the living microorganisms. The aim of the present study was to determine the real impact of glyphosate on potential pathogens and beneficial members of poultry microbiota in vitro. The presented results evidence that the highly pathogenic bacteria as Salmonella Entritidis, Salmonella Gallinarum, Salmonella Typhimurium, Clostridium perfringens and Clostridium botulinum are highly resistant to glyphosate. However, most of beneficial bacteria as Enterococcus faecalis, Enterococcus faecium, Bacillus badius, Bifidobacterium adolescentis and Lactobacillus spp. were found to be moderate to highly susceptible. Also Campylobacter spp. were found to be susceptible to glyphosate. A reduction of beneficial bacteria in the gastrointestinal tract microbiota by ingestion of glyphosate could disturb the normal gut bacterial community. Also, the toxicity of glyphosate to the most prevalent Enterococcus spp. could be a significant predisposing factor that is associated with the increase in C. botulinum-mediated diseases by suppressing the antagonistic effect of these bacteria on clostridia.


Minimal Inhibitory Concentration Glyphosate Clostridium Botulinum Beneficial Bacterium Bifidobacterium Longum 
These keywords were added by machine and not by the authors. This process is experimental and the keywords may be updated as the learning algorithm improves.


  1. 1.
    Barja BC, Herszage J, Afonso MD (2001) Iron(III)–phosphonate complexes. Polyhedron 20:1821–1830CrossRefGoogle Scholar
  2. 2.
    Barry G, Padgette SR (1992) Glyphosate tolerant 5-enolpyruvylshikimate-3-phosphate synthases. World Patent, WO 92/04449Google Scholar
  3. 3.
    Baums CG, Schotte U, Amtsberg G, Goethe R (2004) Diagnostic multiplex PCR for toxin genotyping of Clostridium perfringens isolates. Vet Microbiol 20:11–16CrossRefGoogle Scholar
  4. 4.
    Benachour N, Se′ralini GE (2009) Glyphosate formulations induce apoptosis and necrosis in human umbilical, embryonic, and placental cells. Chem Res Toxicol 22:97–105PubMedCrossRefGoogle Scholar
  5. 5.
    Benachour N, Sipahutar H, Moslemi S et al (2007) Time- and dose-dependent effects of Roundup on human embryonic and placental cells. Arch Environ Contam Toxicol 53:126–133PubMedCrossRefGoogle Scholar
  6. 6.
    Benedetti AL, Vituri Cde L, Trentin AG et al (2004) The effects of sub-chronic exposure of Wistar rats to the herbicide Glyphosate-Biocarb. Toxicol Lett 153:227–232PubMedCrossRefGoogle Scholar
  7. 7.
    Beuret CJ, Zirulnik F, Gimenez MS (2005) Effect of the herbicide glyphosate on liver lipoperoxidation in pregnant rats and their fetuses. Reprod Toxicol 19:501–504PubMedCrossRefGoogle Scholar
  8. 8.
    Bezkorovainy A (2001) Probiotics: determinants of survival and growth in the gut. Am J Clin Nutr 73:399–405Google Scholar
  9. 9.
    Bonnet JL, Bonnemoy F, Dusser M et al (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 22:78–91PubMedCrossRefGoogle Scholar
  10. 10.
    Bradshaw LD, Padgette SR, Kimball SL et al (1997) Perspectives on glyphosate resistance. Weed Technol 11:189–198Google Scholar
  11. 11.
    Burr DH, Sugiyama H, Jarvis G (1982) Susceptibility to enteric botulinum colonization of antibiotic treated adult mice. Infect Immun 36:103–106PubMedGoogle Scholar
  12. 12.
    Cerdeira AL, Duke SO (2006) The current status and environmental impacts of glyphosate-resistant crops: a review. J Environ Qual 35:1633–1658PubMedCrossRefGoogle Scholar
  13. 13.
    Clair E, Linn L, Travert C et al (2012) Effects of Roundup and glyphosate on three food microorganisms: Geotrichum candidum, Lactococcus lactis subsp. cremoris and Lactobacillus delbrueckii subsp. bulgaricus. Curr Microbiol 64:486–491PubMedCrossRefGoogle Scholar
  14. 14.
    Coelho Abrantes M, MdF Lopes, Kok J (2011) Impact of manganese, copper and zinc ions on the transcriptome of the nosocomial pathogen Enterococcus faecalis V583. PLoS ONE 6(10):e26519. doi: 10.1371/journal.pone.0026519 CrossRefGoogle Scholar
  15. 15.
    De Roos AJ, Svec MA, Blair A, Rusiecki JA et al (2005) Glyphosate results revisited: respond. Environ Health Perspect 113:366–367CrossRefGoogle Scholar
  16. 16.
    Duke SO, Baerson SR, Rimando AM (2003) Herbicides: glyphosate. In: Plimmer JR, Gammon DW, Ragsdale (eds) Encyclopedia of agrochemicals. http://www.mrw. Accessed June 2012
  17. 17.
    EFSA (2009) The community summary report on trends and sources of zoonoses and zoonotic agents in the European Union in 2007. EFSA J 223:1–320Google Scholar
  18. 18.
    Eschenburg S, Healy ML, Priestman MA et al (2002) How the mutation glycine96 to alanine confers glyphosate insensitivity to 5-enolpyruvyl shikimate-3-phosphate synthase from Escherichia coli. Planta 216:129–135PubMedCrossRefGoogle Scholar
  19. 19.
    FAO (2005) Pesticide residues in food. Accessed June 2012
  20. 20.
    Gasnier C, Dumont C, Benachour N et al (2009) Glyphosate based herbicides are toxic and endocrine disruptors in human cell lines. Toxicology 262:184–191PubMedCrossRefGoogle Scholar
  21. 21.
    Gong J, Forster RJ, Yu H et al (2002) Diversity and phylogenetic analysis of bacteria in the mucosa of chicken ceca and comparison with bacteria in the cecal lumen. FEMS Microbiol Lett 208:1–7PubMedCrossRefGoogle Scholar
  22. 22.
    Havenaar R, Huis JHJ, in’t Veld JHJ (1992) Probiotics: a general view. In: Brian J, Wood B (eds) Lactic acid bacteria. Elsevier Applied Science, London, pp 171–192Google Scholar
  23. 23.
    Hernando MD, De Vettori S, Martinez Bueno MJ et al (2007) Toxicity evaluation with Vibrio fischeri test of organic chemicals used in aquaculture. Chemosphere 68:724–730PubMedCrossRefGoogle Scholar
  24. 24.
    Houf K, Stephan R (2007) Isolation and characterization of the emerging foodborne pathogen Arcobacter from human stool. J Microbiol Methods 68:408–413PubMedCrossRefGoogle Scholar
  25. 25.
    IFEN (2006) Report on pesticides in waters. Data 2003–2004Google Scholar
  26. 26.
    Isolauri E, Sutas Y, Kankaanpaa P et al (2001) Probiotics: effects on immunity. Am J Clin Nutr 73:444–450Google Scholar
  27. 27.
    Kishore GM, Shah DM (1988) Amino acid biosynthesis inhibitors as herbicides. Annu Rev Biochem 57:627–663PubMedCrossRefGoogle Scholar
  28. 28.
    Klaenhammer TR (1993) Genetics of bacteriocins produced by lactic acid bacteria. FEMS Microbiol Rev 12:39–86PubMedGoogle Scholar
  29. 29.
    Kleessen B, Elsayed NAAE, Loehren U et al (2003) Jerusalem artichokes stimulate growth of broiler chickens and protect them against endotoxins and potential cecal pathogens. J Food Prot 66:2171–2175PubMedGoogle Scholar
  30. 30.
    Krüger M, Große-Herrenthy A, Schrödl W et al (2012) Visceral botulism at dairy farms in Schleswig Holstein, Germany—prevalence of Clostridium botulinum in faeces of cows, in animal feeds, in faeces of the farmers, and in house dust. Anaerob 18(2):221–223CrossRefGoogle Scholar
  31. 31.
    Kwan PS, Birtles A, Bolton FJ, French NP, Robinson SE et al (2008) Longitudinal study of the molecular epidemiology of C. jejuni in cattle on dairy farms. Appl Environ Microbiol 74:3626–3633PubMedCrossRefGoogle Scholar
  32. 32.
    Lancaster SH, Hollister EB, Senseman SA, Gentry TJ (2010) Effects of repeated glyphosate applications on soil microbial community composition and the mineralization of glyphosate. Pest Manag Sci 66:59–64PubMedCrossRefGoogle Scholar
  33. 33.
    Lorenzatti E, Maitre MI, Argelia L, Lajmanovich R, Peltzer P, Anglada M (2004) Pesticide residues in immature soybeans of Argentina croplands. Fresenius Environ Bull 13:675–678Google Scholar
  34. 34.
    Meremäe K, Roasto M, Tamme T, Ivanova M, Liisa M et al (2010) In-vitro-Studie über die antimikrobielle Wirkung von ausgewählten Probiotika kombiniert mit Präbiotika auf Campylobacter jejuni. Archiv für Lebensmittelhygiene 61(4):125–164Google Scholar
  35. 35.
    Missous G, Thammavongs B, Dieuleveux V et al (2007) Improvement of the cryopreservation of the fungal starter Geotrichum candidum by artificial nucleation and temperature down shift control. Cryobiology 55:66–71PubMedCrossRefGoogle Scholar
  36. 36.
    Moore JE, Corcoran D, Dooley JSG, Fanning S, Lucey B et al (2005) Campylobacter. Vet Res 36:351–382PubMedCrossRefGoogle Scholar
  37. 37.
    Motekaitis RJ, Martell AE (1985) Metal chelate formation by N-phosphonomethylglycine and related ligands. J Coord Chem 14:139–149CrossRefGoogle Scholar
  38. 38.
    Mulder RWAW, Havenaar R, Huis in’t Veld JHJ (1997) Intervention strategies: the use of probiotics and competitive exclusion microfloras against contamination with pathogens in pigs and poultry. In: Fuller R (ed) Probiotics 2: application and practical aspects. Chapman & Hall, London, pp 187–207Google Scholar
  39. 39.
    Oliveira AG, Telles LF, Hess RA et al (2007) Effects of the herbicide Roundup on the epididymal region of drakes Anas platyrhynchos. Reprod Toxicol 23:182–191PubMedCrossRefGoogle Scholar
  40. 40.
    Paganelli A, Ganso V, Acosta H et al (2010) Glyphosate-based herbicides produce teratogenic effects on vertebrates by impairing retinoic acid signaling. Chem Res Toxicol 23:1586–1595PubMedCrossRefGoogle Scholar
  41. 41.
    Parente E, Hill C (1992) Characterization of enterocin 1146, a bacteriocin from Enterococcus faecium inhibitory to Listeria monocytogenes. J Food Protect 55:497–502Google Scholar
  42. 42.
    Parente E, Hill C (1992) Inhibition of Listeria in buffer, broth, and milk by enterocin 1146, a bacteriocin produced by Enterococcus faecium. J Food Protect 55:503–508Google Scholar
  43. 43.
    Peruzzo P, Porta A, Ronco A (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(1):61-66. ISSN 0269-7491Google Scholar
  44. 44.
    Poletta GL, Larriera A, Kleinsorge E, Mudry MD (2009) Genotoxicity of the herbicide formulation Roundup (glyphosate) in broad-snouted caiman (Caiman latirostris) evidenced by the Comet assay and the micronucleus test. Mutat Res 672:95–102PubMedCrossRefGoogle Scholar
  45. 45.
    Priestman MA, Funke T, Singh IM et al (2005) 5-Enolpyruvylshikimate-3-phosphate synthase from Staphylococcus aureus is insensitive to glyphosate. FEBS Lett 579:728–732PubMedCrossRefGoogle Scholar
  46. 46.
    Relyea RA (2005) The impact of insecticides and herbicides on the biodiversity and productivity of aquatic communities. Ecol Appl 15:618–627CrossRefGoogle Scholar
  47. 47.
    Sanchís J, Kantiani L, Llorca M, Rubio F et al (2012) Determination of glyphosate in groundwater samples using an ultrasensitive immunoassay and confirmation by on-line solid-phase extraction followed by liquid chromatography coupled to tandem mass spectrometry. Anal Bioanal Chem 402(7):2335–2345PubMedCrossRefGoogle Scholar
  48. 48.
    Schmatz DM, Crane MS, Murray PK (1984) Purification of Eimeria sporozoites by DE-52 anion exchange chromatography. J Protozool 31(1):181–183PubMedGoogle Scholar
  49. 49.
    Shehata AA, Schrödl W, Krüger M (2012) Glyphosate suppresses the antagonistic effect of Enterococcus spp. on Clostridium botulinum Anaerobe. In: Tagung der Fachgruppe Bakteriologie und Mykologie, Leipzig, Germany, DVG, pp 181–182Google Scholar
  50. 50.
    Shehata AA, Schrödl W, Neuhaus J, Krüger M (2012) Antagonistic effect of different bacteria on Clostridium botulinum types A, B, C, D and E in vitro. Vet Record J (accepted)Google Scholar
  51. 51.
    Smith GR, Milligan RA (1979) Clostridium botulinum in soil on the site of the former Metropolitan (Caledonian) cattle market. J Hyg Camb 83:241–273Google Scholar
  52. 52.
    Solomon KR, Anadón A, Carrasquilla G et al (2007) Coca and poppy eradication in Colombia: environmental and human health assessment of aerially applied glyphosate. Rev Environ Contam Toxicol 190:43–125PubMedCrossRefGoogle Scholar
  53. 53.
    Stalker DM, Hiatt WR, Comai L (1985) A single amino acid substitution in the enzyme 5-enolpyruvylshikimate-3-phosphate synthase confers resistance to the herbicide glyphosate. J Biol Chem 260:4724–4728PubMedGoogle Scholar
  54. 54.
    Sullivan NM, Mills DC, Riepmann HP et al (1988) Inhibition of growth of Clostridium botulinum by intestinal microflora isolated from healthy infants. Microb Ecol Health Dis 1:179–192CrossRefGoogle Scholar
  55. 55.
    Thammavongs B, Denou E, Missous G et al (2008) Response to environmental stress as a global phenomenon in biology: the example of microorganisms. Microbes Environ 23:20–23PubMedCrossRefGoogle Scholar
  56. 56.
    Tomley F (1997) Techniques for isolation and characterization of apical organelles from Eimeria tenella sporozoites. Methods 13:171–176PubMedCrossRefGoogle Scholar
  57. 57.
    Wang Y, Sugiyama I (1984) Botulism in metronidazole-treated conventional adult mice challenged orogastrically with spores of Clostridium botulinum type A or B. Infect Immun 46:715–719PubMedGoogle Scholar
  58. 58.
    WHO (1994) Glyphosate, Environmental Health Criteria 159 Accessed Nov 2012
  59. 59.
    Yousef MI, Salem MH, Ibrahim HZ et al (1995) Toxic effects of carbofuran and glyphosate on semen characteristics in rabbits. J Environ Sci Health B 30:513–534PubMedCrossRefGoogle Scholar

Copyright information

© Springer Science+Business Media New York 2012

Authors and Affiliations

  • Awad A. Shehata
    • 1
    • 2
    • 3
    Email author
  • Wieland Schrödl
    • 1
  • Alaa. A. Aldin
    • 4
  • Hafez M. Hafez
    • 5
  • Monika Krüger
    • 1
  1. 1.Institute of Bacteriology and Mycology, Faculty of Veterinary MedicineLeipzig UniversityLeipzigGermany
  2. 2.Albrecht Daniel Thaer-Institute of Agronomy, University LeipzigLeipzigGermany
  3. 3.Avian and Rabbit Disease Department, Faculty of Veterinary MedicineMenoufiya UniversitySadat CityEgypt
  4. 4.Institute of Parasitology, Faculty of Veterinary MedicineLeipzig UniversityLeipzigGermany
  5. 5.Institute of Poultry Disease, Free UniversityBerlinGermany

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