Current Microbiology

, Volume 69, Issue 6, pp 817–823 | Cite as

Possible Effects of Glyphosate on Mucorales Abundance in the Rumen of Dairy Cows in Germany

  • Wieland Schrödl
  • Susanne Krüger
  • Theodora Konstantinova-Müller
  • Awad A. Shehata
  • Ramon Rulff
  • Monika Krüger
Article

Abstract

Glyphosate (N-phosphonomethyl glycine) is registered as a herbicide for many food and non-food crops, as well as non-crop areas where total vegetation control is desired. Glyphosate influences the soil mycobiota; however, the possible effect of glyphosate residues in animal feed (soybean, corn, etc.) on animal mycobiota is almost unknown. Accordingly, the present study was initiated to investigate the mycological characteristics of dairy cows in relationship to glyphosate concentrations in urine. A total of 258 dairy cows on 14 dairy farms in Germany were examined. Glyphosate was detected in urine using ELISA. The fungal profile was analyzed in rumen fluid samples using conventional microbiological culture techniques and differentiated by MALDI-TOF mass spectrometry. LPS-binding protein (LBP) and antibodies (IgG1, IgG2, IgA, and IgM) against fungi were determined in blood using ELISA. Different populations of Lichtheimia corymbifera, Lichtheimia ramosa, Mucor, and Rhizopus were detected. L. corymbifera andL. ramosa were significantly more abundant in animals containing high glyphosate (>40 ng/ml) concentrations in urine. There were no significant changes in IgG1 and IgG2 antibodies toward isolated fungi that were related to glyphosate concentration in urine; however, IgA antibodies against L. corymbifera and L. ramosa were significantly lower in the higher glyphosate groups. Moreover, a negative correlation between IgM antibodies against L. corymbifera,L. ramosa, and Rhizopus relative to glyphosate concentration in urine was observed. LBP also was significantly decreased in animals with higher concentrations of glyphosate in their urine. In conclusion, glyphosate appears to modulate the fungal community. The reduction of IgM antibodies and LBP indicates an influence on the innate immune system of animals.

References

  1. 1.
    Accinelli C, Abbas HK, Zablotowicz RM, Wilkinson JR (2008) Aspergillus flavus aflatoxin occurrence and expression of aflatoxin biosynthesis genes in soil. Can J Microbiol 54:371–379PubMedCrossRefGoogle Scholar
  2. 2.
    Acquavella JF, Alexander BH, Mandel JS, Gustin C, Baker B (2004) Glyphosate biomonitoring for farmers and their families: results from the farm family exposure study. Environ Health Perspect 12:321–326Google Scholar
  3. 3.
    Anonymous (2001) Commission working document. Review report for the active substance glyphosate. Finalized in the Standing Committee on Plant Health at its meeting on 29 June 2001 in view of the inclusion of glyphosate in Annex I of Directive 91/414/EECGoogle Scholar
  4. 4.
    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
  5. 5.
    Borggard OK, Gimsing AL (2008) Fate of glyphosate in soil and the possibility of leaching to ground and surface waters: a review. Pest Manag Sci 64:441–456CrossRefGoogle Scholar
  6. 6.
    Brown CC, Baker DC, Barker Ik (2007) Rumenitis and acidosis caused by overeating on grain. Jubb, Kennedy and Palmer´s Pathology of Domestic Animals, 5th edn. Elsevier Saunders, Philadelphia, pp 46–48Google Scholar
  7. 7.
    Cerdeira AL, Duke SO (2006) The current status and environmental impacts of glyphosate-resistant crops: a review. J Environ Qual 35:1633–1658PubMedCrossRefGoogle Scholar
  8. 8.
    Chihaya Y, Matsukawa K, Ohshima K, Matsui Y, Ogasa K, Furusawa Y, Okada H (1992) A pathological study of bovine alimentary mycosis. J Comp Pathol 107(2):195–206PubMedCrossRefGoogle Scholar
  9. 9.
    Chihaya Y, Matskawa K, Mizushima S, Matsui Y (1988) Ruminant forestomach and abomasal mucormycosis under rumen acidosis. Vet Pathol 25:119–123PubMedCrossRefGoogle Scholar
  10. 10.
    Clair E, Linn L, Travert C, Amiel C, Séralini GE, Panoff JM (2012) Effects of Roundup® and glyphosate on three food microorganisms: Geotrichum candidum, Lactococcus lactis subsp. cremoris and Lactobacillus delbrueckii subsp. Bulgaricus. Curr Microbiol 64(5):486–489PubMedCrossRefGoogle Scholar
  11. 11.
    Curwin BD, Hein MJ, Sanderson WT, Streiley C, Heederik D (2007) Pesticide dose estimates for children of Iowa farmers and non-farmers. Environ Res 105:307–315PubMedCrossRefGoogle Scholar
  12. 12.
    Davies JL, Ngeleka M, Wobeser GA (2010) Systemic infection with Mortierella wolfii following abortion in a cow. Can Vet 51:1391–1393Google Scholar
  13. 13.
    De Roos AJ, Svec MA, Blair A, Rusiecki JA (2005) Glyphosate results revisited: respond. Environ Health Perspect 113:366–367CrossRefGoogle Scholar
  14. 14.
    Edwards SG (2004) Influence of agricultural practices on Fusarium infection of cereals and subsequent contamination of grain by trichothecene mycotoxins. Toxicol Lett 153:29–35PubMedCrossRefGoogle Scholar
  15. 15.
    El-Shenawy NS (2009) Oxidative stress responses of rats exposed to roundup and its active ingredient glyphosate. Environ Toxicol Pharmacol 28:379–385PubMedCrossRefGoogle Scholar
  16. 16.
    Fernandez M (2003) Fusarium corrections. New Sci 179:23–35Google Scholar
  17. 17.
    Hanson KG, Fernandez MR (2003) Saskatchewan Regional Meeting 2002 The Canadian Phytopathological Society. Can J Plant Pathol 25:119–122CrossRefGoogle Scholar
  18. 18.
    Helander M, Saloniemi I, Saikkonen K (2013) Glyphosate in northern ecosystems. TRPLSC 979:1–6Google Scholar
  19. 19.
    Jensen HE (1994) Systemic bovine aspergillosis and zygomycosis in Denmark with reference to pathogenesis, pathology, and diagnosis. APMIS Suppl 42:1–48PubMedGoogle Scholar
  20. 20.
    Jensen HE, Olsen SN, Aalbaek B (1994) Gastrointestinal Aspergillosis and Zygomycosis of cattle. Vet Pathol 31:28–36PubMedCrossRefGoogle Scholar
  21. 21.
    Johal GS, Huber DM (2009) Glyphosate effects on diseases of plants. Europ J Agron 33:144–152CrossRefGoogle Scholar
  22. 22.
    Kremer RJ, Means NE (2009) Glyphosate and glyphosate-resistant crop interactions with rhizosphere microorganisms. Europ J Agron 31:153–161CrossRefGoogle Scholar
  23. 23.
    Krüger M, Shehata AA, Grosse-Herrenthey A, Ständer N, Schrödl W (2014) Relationship between gastrointestinal dysbiosis and Clostridium botulinum in dairy cows. Anaerobe 27:100–105PubMedCrossRefGoogle Scholar
  24. 24.
    Krüger M, Shehata AA, Schrödl W, Rodloff A (2013) Glyphosate suppresses the antagonistic effect of Enterococcus spp. on Clostridium botulinum. Anaerobe 20:74–78PubMedCrossRefGoogle Scholar
  25. 25.
    Krüger M, Schrödl W, Neuhaus J, Shehata AA (2013b) Field investigations of glyphosate in urine of Danish dairy cows. J Environ Anal Toxicol 3: (186) doi:10.4172/2161-0525.1000186
  26. 26.
    Levesque CA, Rahe JE, Eaves DM (1987) Effects of glyphosate on Fusarium spp.: its influence on root colonization of weeds, propagule density in the soil, and crop emergence. Can J Microbiol 33:354–360CrossRefGoogle Scholar
  27. 27.
    Lund A (1974) Yeast and moulds in the bovine rumen. J Gen Microbiol 81(453–462):1974Google Scholar
  28. 28.
    Nishimura M, Toyota Y, Ishida Y, Nakaya H, Kameyama K, Nishikawa Y, Miyahara K, Inokuma H, Furuoka H (2014) Zygomycotic mediastinal lymphadenitis in beef cattle with rumenal tympany. J Vet Med Sci 76(1):123–127PubMedCrossRefPubMedCentralGoogle Scholar
  29. 29.
    Ostermann C, Schroedl W, Schubert E, Sachse K, Reinhold P (2013) Dose-dependent effects of Chlamydia psittaci infection on pulmonary gas exchange, innate immunity and acute-phase reaction in a bovine respiratory model. Vet J 196(3):351–359PubMedCrossRefGoogle Scholar
  30. 30.
    Ortega J, Uzal FA, Walker R, Kinde H, Diab SS, Shahriar F, Pamma R, Eigenheer A, Read DH (2010) Zygomycotic lymphadenitis in slaughtered feedlot cattle. Vet Pathol 47(1):108–115PubMedCrossRefGoogle Scholar
  31. 31.
    Piancastelli C, Ghidini F, Donofrio G, Jottini S, Taddei S, Cavirani S, Cabassi CS (2009) Isolation and characterization of a strain of Lichtheimia corymbifera (ex Absidia corymbifera) from a case of bovine abortion. Reprod Biol Endocrinol 30:138–140CrossRefGoogle Scholar
  32. 32.
    Reddy KN, Abbas HK, Zablotowicz RM, Abel CA, Koger CH (2007) Mycotoxin occurrence and Aspergillus flavus soil propagules in a corn and cotton glyphosate-resistant cropping system. Food Addit Contam 24:1367–1373PubMedCrossRefGoogle Scholar
  33. 33.
    Rippon JW (1982) Mucormycosis. Medical Mycology: the Pathogenic Fungi and the Pathogenic Actinomycetes, 2nd edn. WB Saunders, Philadelphia, pp 615–640Google Scholar
  34. 34.
    Samsel A, Seneff S (2013) Glyphosate’s suppression of cytochrome P450 enzymes and amino acid biosynthesis by the gut microbiome: Pathways to modern diseases. Entropy 15:1416–1463. doi:10.3390/e140x000x.2013 CrossRefGoogle Scholar
  35. 35.
    Schrödl W, Heydel T, Schwartze VU, Hoffmann K, Grosse-Herrenthey A, Walther G, Alastruey-Izquierdo A, Rodriguez-Tudela JL, Olias P, Jacobsen ID, de Hoog GS, Voigt K (2012) Direct analysis and identification of pathogenic Lichtheimia species by matrix-assisted laser desorption ionization-time of flight analyzer-mediated mass spectrometry. J Clin Microbiol 50(2):419–427PubMedCrossRefPubMedCentralGoogle Scholar
  36. 36.
    Shehata AA, Schrödl W, Aldin AA, Hafez HM, Krüger M (2013) The effect of glyphosate on potential pathogens and beneficial members of poultry microbiota in vitro. Curr Microbiol 66(4):350–358PubMedCrossRefGoogle Scholar
  37. 37.
    Shehata, AA, Schrödl W, Neuhaus J, Krüger M (2013b) Antagonistic effect of different bacteria on Clostridium botulinum types A, B, C, D and E in vitro. Vet Rec 12; 172(2): 47Google Scholar
  38. 38.
    Solomon KR, Anadón A, Carrasquilla G (2007) Coca and poppy eradication in Colombia: environmental and human health assessment of aerially applied glyphosate. Rev Environ Contam Toxicol 190:43–125PubMedGoogle Scholar
  39. 39.
    Ström K, Sjögren J, Broberg A, Schnürer J (2002) Lactobacillus plantarum MiLAB 393 produces the antifungal cyclic dipeptides Cyclo(L-Phe–L-Pro) and cyclo(L-Phe–trans-4-OH-L-Pro) and 3-phenyllactic acid. Appl Environ Microbiol 68:4322–4327PubMedCrossRefPubMedCentralGoogle Scholar
  40. 40.
    Wan MT, Rahe JE, Watts RG (1998) New technique for determinating the sublethal toxicity of pesticides to the vesicular-arbuscular mycirrhizal fungus Glomus intraradices. Environ Toxic Chem 17:1421–1428Google Scholar

Copyright information

© Springer Science+Business Media New York 2014

Authors and Affiliations

  • Wieland Schrödl
    • 1
  • Susanne Krüger
    • 1
  • Theodora Konstantinova-Müller
    • 1
  • Awad A. Shehata
    • 1
    • 2
  • Ramon Rulff
    • 1
  • Monika Krüger
    • 1
  1. 1.Institute of Bacteriology and Mycology, Faculty of Veterinary MedicineLeipzig UniversityLeipzigGermany
  2. 2.Avian and Rabbit Diseases Department, Faculty of Veterinary MedicineSadat City UniversitySadat CityEgypt

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