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

Abstract

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.

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

References

  1. 1.

    Barja BC, Herszage J, Afonso MD (2001) Iron(III)–phosphonate complexes. Polyhedron 20:1821–1830

    Article  CAS  Google Scholar 

  2. 2.

    Barry G, Padgette SR (1992) Glyphosate tolerant 5-enolpyruvylshikimate-3-phosphate synthases. World Patent, WO 92/04449

  3. 3.

    Baums CG, Schotte U, Amtsberg G, Goethe R (2004) Diagnostic multiplex PCR for toxin genotyping of Clostridium perfringens isolates. Vet Microbiol 20:11–16

    Article  Google 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 22:97–105

    PubMed  Article  CAS  Google 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 53:126–133

    PubMed  Article  CAS  Google 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 153:227–232

    PubMed  Article  CAS  Google 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 19:501–504

    PubMed  Article  CAS  Google Scholar 

  8. 8.

    Bezkorovainy A (2001) Probiotics: determinants of survival and growth in the gut. Am J Clin Nutr 73:399–405

    Google 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 22:78–91

    PubMed  Article  CAS  Google Scholar 

  10. 10.

    Bradshaw LD, Padgette SR, Kimball SL et al (1997) Perspectives on glyphosate resistance. Weed Technol 11:189–198

    CAS  Google Scholar 

  11. 11.

    Burr DH, Sugiyama H, Jarvis G (1982) Susceptibility to enteric botulinum colonization of antibiotic treated adult mice. Infect Immun 36:103–106

    PubMed  CAS  Google Scholar 

  12. 12.

    Cerdeira AL, Duke SO (2006) The current status and environmental impacts of glyphosate-resistant crops: a review. J Environ Qual 35:1633–1658

    PubMed  Article  CAS  Google 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 64:486–491

    PubMed  Article  CAS  Google 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

    Article  Google Scholar 

  15. 15.

    De Roos AJ, Svec MA, Blair A, Rusiecki JA et al (2005) Glyphosate results revisited: respond. Environ Health Perspect 113:366–367

    Article  Google 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 223:1–320

    Google 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 216:129–135

    PubMed  Article  CAS  Google Scholar 

  19. 19.

    FAO (2005) Pesticide residues in food. http://www.fao.org/docrep/009/a0209e/a0209e0d.htm. 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 262:184–191

    PubMed  Article  CAS  Google 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 208:1–7

    PubMed  Article  CAS  Google 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 171–192

    Google 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 68:724–730

    PubMed  Article  CAS  Google Scholar 

  24. 24.

    Houf K, Stephan R (2007) Isolation and characterization of the emerging foodborne pathogen Arcobacter from human stool. J Microbiol Methods 68:408–413

    PubMed  Article  CAS  Google Scholar 

  25. 25.

    IFEN (2006) Report on pesticides in waters. Data 2003–2004

  26. 26.

    Isolauri E, Sutas Y, Kankaanpaa P et al (2001) Probiotics: effects on immunity. Am J Clin Nutr 73:444–450

    Google Scholar 

  27. 27.

    Kishore GM, Shah DM (1988) Amino acid biosynthesis inhibitors as herbicides. Annu Rev Biochem 57:627–663

    PubMed  Article  CAS  Google Scholar 

  28. 28.

    Klaenhammer TR (1993) Genetics of bacteriocins produced by lactic acid bacteria. FEMS Microbiol Rev 12:39–86

    PubMed  CAS  Google 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 66:2171–2175

    PubMed  CAS  Google 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):221–223

    Article  Google 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 74:3626–3633

    PubMed  Article  CAS  Google 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 66:59–64

    PubMed  Article  CAS  Google 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 13:675–678

    CAS  Google 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):125–164

    Google 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 55:66–71

    PubMed  Article  CAS  Google Scholar 

  36. 36.

    Moore JE, Corcoran D, Dooley JSG, Fanning S, Lucey B et al (2005) Campylobacter. Vet Res 36:351–382

    PubMed  Article  CAS  Google Scholar 

  37. 37.

    Motekaitis RJ, Martell AE (1985) Metal chelate formation by N-phosphonomethylglycine and related ligands. J Coord Chem 14:139–149

    Article  CAS  Google 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 187–207

    Google 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 23:182–191

    PubMed  Article  CAS  Google 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 23:1586–1595

    PubMed  Article  CAS  Google Scholar 

  41. 41.

    Parente E, Hill C (1992) Characterization of enterocin 1146, a bacteriocin from Enterococcus faecium inhibitory to Listeria monocytogenes. J Food Protect 55:497–502

    CAS  Google 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 55:503–508

    CAS  Google 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 0269-7491

    Google 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 672:95–102

    PubMed  Article  CAS  Google 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 579:728–732

    PubMed  Article  CAS  Google Scholar 

  46. 46.

    Relyea RA (2005) The impact of insecticides and herbicides on the biodiversity and productivity of aquatic communities. Ecol Appl 15:618–627

    Article  Google 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):2335–2345

    PubMed  Article  Google Scholar 

  48. 48.

    Schmatz DM, Crane MS, Murray PK (1984) Purification of Eimeria sporozoites by DE-52 anion exchange chromatography. J Protozool 31(1):181–183

    PubMed  CAS  Google 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 181–182

  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)

  51. 51.

    Smith GR, Milligan RA (1979) Clostridium botulinum in soil on the site of the former Metropolitan (Caledonian) cattle market. J Hyg Camb 83:241–273

    Google 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 190:43–125

    PubMed  Article  CAS  Google 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 260:4724–4728

    PubMed  CAS  Google 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 1:179–192

    Article  Google 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 23:20–23

    PubMed  Article  Google Scholar 

  56. 56.

    Tomley F (1997) Techniques for isolation and characterization of apical organelles from Eimeria tenella sporozoites. Methods 13:171–176

    PubMed  Article  CAS  Google 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 46:715–719

    PubMed  CAS  Google Scholar 

  58. 58.

    WHO (1994) Glyphosate, Environmental Health Criteria 159 http://www.inchem.org/documents/ehc/ehc/ehc159.htm#SubSectionNumber:4.1.6. 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 30:513–534

    PubMed  Article  CAS  Google Scholar 

Download references

Author information

Affiliations

Authors

Corresponding author

Correspondence to Awad A. Shehata.

Rights and permissions

Reprints and Permissions

About this article

Cite this article

Shehata, A.A., Schrödl, W., Aldin, A.A. et al. The Effect of Glyphosate on Potential Pathogens and Beneficial Members of Poultry Microbiota In Vitro. Curr Microbiol 66, 350–358 (2013). https://doi.org/10.1007/s00284-012-0277-2

Download citation

Keywords

  • Minimal Inhibitory Concentration
  • Glyphosate
  • Clostridium Botulinum
  • Beneficial Bacterium
  • Bifidobacterium Longum