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 and L. 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.
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References
Accinelli C, Abbas HK, Zablotowicz RM, Wilkinson JR (2008) Aspergillus flavus aflatoxin occurrence and expression of aflatoxin biosynthesis genes in soil. Can J Microbiol 54:371–379
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 12:321–326
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/EEC
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
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 64:441–456
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 46–48
Cerdeira AL, Duke SO (2006) The current status and environmental impacts of glyphosate-resistant crops: a review. J Environ Qual 35:1633–1658
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):195–206
Chihaya Y, Matskawa K, Mizushima S, Matsui Y (1988) Ruminant forestomach and abomasal mucormycosis under rumen acidosis. Vet Pathol 25:119–123
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):486–489
Curwin BD, Hein MJ, Sanderson WT, Streiley C, Heederik D (2007) Pesticide dose estimates for children of Iowa farmers and non-farmers. Environ Res 105:307–315
Davies JL, Ngeleka M, Wobeser GA (2010) Systemic infection with Mortierella wolfii following abortion in a cow. Can Vet 51:1391–1393
De Roos AJ, Svec MA, Blair A, Rusiecki JA (2005) Glyphosate results revisited: respond. Environ Health Perspect 113:366–367
Edwards SG (2004) Influence of agricultural practices on Fusarium infection of cereals and subsequent contamination of grain by trichothecene mycotoxins. Toxicol Lett 153:29–35
El-Shenawy NS (2009) Oxidative stress responses of rats exposed to roundup and its active ingredient glyphosate. Environ Toxicol Pharmacol 28:379–385
Fernandez M (2003) Fusarium corrections. New Sci 179:23–35
Hanson KG, Fernandez MR (2003) Saskatchewan Regional Meeting 2002 The Canadian Phytopathological Society. Can J Plant Pathol 25:119–122
Helander M, Saloniemi I, Saikkonen K (2013) Glyphosate in northern ecosystems. TRPLSC 979:1–6
Jensen HE (1994) Systemic bovine aspergillosis and zygomycosis in Denmark with reference to pathogenesis, pathology, and diagnosis. APMIS Suppl 42:1–48
Jensen HE, Olsen SN, Aalbaek B (1994) Gastrointestinal Aspergillosis and Zygomycosis of cattle. Vet Pathol 31:28–36
Johal GS, Huber DM (2009) Glyphosate effects on diseases of plants. Europ J Agron 33:144–152
Kremer RJ, Means NE (2009) Glyphosate and glyphosate-resistant crop interactions with rhizosphere microorganisms. Europ J Agron 31:153–161
Krüger M, Shehata AA, Grosse-Herrenthey A, Ständer N, Schrödl W (2014) Relationship between gastrointestinal dysbiosis and Clostridium botulinum in dairy cows. Anaerobe 27:100–105
Krüger M, Shehata AA, Schrödl W, Rodloff A (2013) Glyphosate suppresses the antagonistic effect of Enterococcus spp. on Clostridium botulinum. Anaerobe 20:74–78
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
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 33:354–360
Lund A (1974) Yeast and moulds in the bovine rumen. J Gen Microbiol 81(453–462):1974
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):123–127
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):351–359
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):108–115
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 30:138–140
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 24:1367–1373
Rippon JW (1982) Mucormycosis. Medical Mycology: the Pathogenic Fungi and the Pathogenic Actinomycetes, 2nd edn. WB Saunders, Philadelphia, pp 615–640
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
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):419–427
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):350–358
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): 47
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 190:43–125
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 68:4322–4327
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 17:1421–1428
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Schrödl, W., Krüger, S., Konstantinova-Müller, T. et al. Possible Effects of Glyphosate on Mucorales Abundance in the Rumen of Dairy Cows in Germany. Curr Microbiol 69, 817–823 (2014). https://doi.org/10.1007/s00284-014-0656-y
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DOI: https://doi.org/10.1007/s00284-014-0656-y