Investigations on the possible impact of a glyphosate-containing herbicide on ruminal metabolism and bacteria in vitro by means of the ‘Rumen Simulation Technique’

Journal of Applied Microbiology

Volumn 121, Issue 3, 2016, Pages 644-656

  Riede, S ^a   Toboldt, A ^b   Breves, G ^a   Metzner, M ^c   Kohler B ^c   Braunig J ^b   Schafft, H ^b   Lahrssen Wiederholt, M ^b   Niemann, L ^b  

^a UNIVERSITY OF VETERINARY MEDICINE HANNOVER   (Germany)

^b FEDERAL INSTITUTE FOR RISK ASSESSMENT   (Germany)

^c Ripac Labor GmbH   (Germany)

Author keywords

Clostridia; glyphosate; microbial communities; Rumen Simulation Technique; ruminal metabolism

Indexed keywords

AMMONIA; CLOSTRIDIUM; FATTY ACIDS; METABOLISM; WEED CONTROL;

BACTERIAL COMMUNITY; BIOCHEMICAL PARAMETERS; CLOSTRIDIUM SPOROGENES; GLYPHOSATES; IN-VITRO; IN-VITRO MODELS; MICROBIAL COMMUNITIES; RUMEN SIMULATION TECHNIQUE; RUMINAL METABOLISM; SIMULATION TECHNIQUE;

HERBICIDES;

GENOMIC DNA; GLYPHOSATE; HERBICIDE; SHORT CHAIN FATTY ACID; SINGLE STRANDED DNA;

BACTERIUM; CONCENTRATION (COMPOSITION); EXPERIMENTAL STUDY; FATTY ACID; GLYPHOSATE; GROWTH RATE; INOCULATION; METABOLISM; MICROBIAL ACTIVITY; MICROBIAL COMMUNITY; MICROBIAL ECOLOGY; RUMINANT;

ANIMAL TISSUE; ANTIMICROBIAL ACTIVITY; ARTICLE; BACTERIAL GROWTH; BEEF CATTLE; CLOSTRIDIUM SPOROGENES; COLONY FORMING UNIT; CONTROLLED STUDY; DAIRY CATTLE; EFFLUENT; FATTY ACID SYNTHESIS; FERMENTATION; IN VITRO STUDY; METABOLISM; MICROBIAL COMMUNITY; NONHUMAN; NUTRIENT CONTENT; OXIDATION REDUCTION POTENTIAL; PH; PHYLOGENETIC TREE; RUMEN; RUMEN MICROORGANISM; SINGLE STRAND CONFORMATION POLYMORPHISM;

BACTERIA (MICROORGANISMS); BOS; CLOSTRIDIA; CLOSTRIDIUM SPOROGENES;

EID: 84982135412     PISSN: 13645072     EISSN: 13652672     Source Type: Journal    
DOI: 10.1111/jam.13190     Document Type: Article

References (57)

1. Ackermann, W., Coenen, M., Schrödl, W., Shehata, A.A. and Krüger, M. (2015) The Influence of glyphosate on the microbiota and production of botulinum neurotoxin during ruminal fermentation. Curr Microbiol 70, 374–382.
2. Allison, M.J., Bryant, M.P. and Doetsch, R.N. (1962) Studies on the metabolic function of branched-chain volatile fatty acids, growth factors for ruminococci. I. Incorporation of isovalerate into leucine. J Bacteriol 83, 523–532.
3. Anderson, M.J. (2001) A new method for non-parametric multivariate analysis of variance. Austral Ecol 26, 32–46.
4. Anderson, M.J. and Robinson, J. (2003) Generalized discriminant analysis based on distances. Aust N Z J Stat 45, 301–318.
5. Balthazor, T.M. and Hallas, L.E. (1986) Glyphosate-degrading microorganisms from industrial activated sludge. Appl Environ Microbiol 51, 432–434.
6. Beer, J. and Al-Khatib, G. (1968) Zum Nachweis und zur Differenzierung pathogener Clostridien und ihrer Toxine. [Detection and differentiation of pathogenic clostridia and their toxins.]. Monatsh Veterinärmed 23, 709–714.
7. Böhnel, H., Schwagerick, B. and Gessler, F. (2001) Visceral botulism – a new form of bovine Clostridium botulinum intoxication. J Vet Med A Physiol Pathol Clin Med 48, 373–383.
8. Boocock, M.R. and Coggins, J.R. (1983) Kinetics of 5-enolpyruvylshikimate-3-phosphate synthase inhibition by glyphosate. FEBS Lett 154, 127–133.
9. Bottacini, F., Ventura, M., Sinderen, D.V. and Motherway, M.O. (2014) Diversity, ecology and intestinal function of bifidobacteria. Microb Cell Fact 12, S4.
10. Bradbury, M.P., Greenfield, D., Midgley, D., Li, D., Tran-Dinh, N., Vriesekoop, F. and Brown, J.L. (2012) Draft genome sequence of Clostridium sporogenes PA 3679, the common nontoxigenic surrogate for proteolytic Clostridium botulinum. J Bacteriol 194, 1631–1632.
11. Brandt, M. and Rohr, K. (1981) Beiträge zur Quantifizierung der N-Umsetzungen in den Vormägen von Milchkühen. [The quantification of nitrogen metabolism in the forestomachs of dairy cows.]. Z Tierphysiol Tierernahr Futtermittelkd 46, 39–48.
12. Bunesova, V., Vlkova, E., Rada, V., Killer, J. and Musilova, S. (2014) Bifidobacteria from the gastrointestinal tract of animals: differences and similarities. Benef Microbes 5, 377–388.
13. Clair, E., Linn, L., Travert, C., Amiel, C., Seralini, G.E. and Panoff, J.M. (2012) Effects of Roundup((R)) and glyphosate on three food microorganisms: Geotrichum candidum, Lactococcus lactis subsp. cremoris and Lactobacillus delbrueckii subsp. bulgaricus. Curr Microbiol 64, 486–491.
14. Collins, M.D., Lawson, P.A., Willems, A., Cordoba, J.J., Fernandez-Garayzabal, J., Garcia, P., Cai, J., Hippe, H. et al. (1994) The phylogeny of the genus Clostridium: proposal of five new genera and eleven new species combinations. Int J Syst Bacteriol 44, 812–826.
15. Czerkawski, J.W. (1986) An Introduction to Rumen Studies, 1st edn. Oxford: Pergamon Press.
16. Czerkawski, J.W. and Breckenridge, G. (1977) Design and development of a long-term rumen simulation technique (RUSITEC). Br J Nutr 38, 371–384.
17. Dehority, B.A., Scott, H.W. and Kowaluk, P. (1967) Volatile fatty acid requirements of cellulolytic rumen bacteria. J Bacteriol 94, 537–543.
18. Dick, R.E. and Quinn, J.P. (1995) Glyphosate-degrading isolates from environmental samples: occurrence and pathways of degradation. Appl Microbiol Biotechnol 43, 545–550.
19. Dohrmann, A.B., Baumert, S., Klingebiel, L., Weiland, P. and Tebbe, C.C. (2011) Bacterial community structure in experimental methanogenic bioreactors and search for pathogenic clostridia as community members. Appl Microbiol Biotechnol 89, 1991–2004.
20. Duke, S.O. and Powles, S.B. (2008) Glyphosate: a once-in-a-century herbicide. Pest Manag Sci 64, 319–325.
21. Germany (2013) Renewal assessment report (RAR) on the active substance glyphosate prepared by the Rapporteur Member State Germany in the framework of Regulation (EC) No 1107/2009, December 2013. Available at www.efsa.europa.eu.
22. Glass, R.L. (1984) Metal complex formation by glyphosate. J Agric Food Chem 32, 1249–1253.
23. Gürtler, H. (1980) Die Verdauung im Wiederkäuermagen. [Digestion in the stomach of ruminants.] In Lehrbuch der Physiologie der Haustiere, 4th edn, Volume 1 ed. Kolb, E. pp. 213–274. Jena: Gustav Fischer.
24. Hao, C., Morse, D., Morra, F., Zhao, X., Yang, P. and Nunn, B. (2011) Direct aqueous determination of glyphosate and related compounds by liquid chromatography/tandem mass spectrometry using reversed-phase and weak anion-exchange mixed-mode column. J Chromatogr A 1218, 5638–5643.
25. Hungate, R.E. (1966) The Rumen and Its Microbes. New York, NY: Academic Press.
26. Hüther, L., Drebes, S. and Lebzien, P. (2005) Effect of glyphosate contaminated feed on rumen fermentation parameters and in sacco degradation of grass hay and corn grain. Arch Anim Nutr 59, 73–79.
27. Kallow, W., Erhard, M., Shah, H.N., Raptakis, E. and Welker, M. (2010) MALDI-TOF MS and microbial identification: years of experimental development to an established protocol. In Mass Spectrometry for Microbial Proteomics ed. Shah, H.N., Gharbia, S.E. and Encheva, V. pp. 255–276. Chichester, UK: John Wiley & Sons. ISBN 978-0-470-68199-2,.
28. Koch, M., Strobel, E., Tebbe, C.C., Heritage, J., Breves, G. and Huber, K. (2006) Transgenic maize in the presence of ampicillin modifies the metabolic profile and microbial population structure of bovine rumen fluid in vitro. Br J Nutr 96, 820–829.
29. Krüger, M., Shehata, A.A., Schrödl, W. and Rodloff, A. (2013) Glyphosate suppresses the antagonistic effect of Enterococcus spp. on Clostridium botulinum. Anaerobe 20, 74–78.
30. Krüger, M., Schledorn, P., Schrödl, W., Hoppe, H.W., Lutz, W. and Shehata, A.A. (2014) Detection of glyphosate residues in animals and humans. J Environ Anal Toxicol 4, doi: 10.4172/2161-0525.1000210.
31. Lane, D.J. (1991) 16S/23S rRNA sequencing. Nucleic acid techniques in bacterial systematics. J Basic Microbiol 31, 403–480.
32. Le Bourhis, A.G., Saunier, K., Dore, J.J., Carlier, P., Chamba, J.F., Popoff, M.R. and Tholozan, J.L. (2005) Development and validation of PCR primers to assess the diversity of Clostridium spp. in cheese by temporal temperature gradient gel electrophoresis. Appl Environ Microbiol 71, 29–38.
33. Locke, M.A., Zablotowicz, R.M. and Reddy, K.N. (2008) Integrating soil conservation practices and glyphosate-resistant crops: impacts on soil. Pest Manag Sci 64, 457–469.
34. Martínez, M.E., Ranilla, M.J., Tejido, M.L., Ramos, S. and Carro, M.D. (2010) Comparison of fermentation of diets of variable composition and microbial populations in the rumen of sheep and Rusitec fermenters. I. Digestibility, fermentation parameters, and microbial growth. J Dairy Sci 93, 3684–3698.
35. Meer, R.R. and Songer, J.G. (1997) Multiplex polymerase chain reaction assay for genotyping Clostridium perfringens. Am J Vet Res 58, 702–705.
36. Meibaum, B., Riede, S., Schröder, B., Manderscheid, R., Weigel, H.J. and Breves, G. (2012) Elevated CO2 and drought stress effects on the chemical composition of maize plants, their ruminal fermentation and microbial diversity in vitro. Arch Anim Nutr 66, 473–489.
37. Moye, H.A. and Deyrup, C.L. (1984) A simple single-step derivatization method for the gas chromatography analysis of the herbicide glyphosate and its metabolite. J Agric Food Chem 32, 192–195.
38. Owens, F.N. and Zinn, R. (1988) Protein metabolism of ruminant animals. In The Ruminant Animal ed. Church, D.C. Englewood Cliffs, NJ: Prentice Hall.
39. Preidis, G.A. and Versalovic, J. (2009) Targeting the human microbiome with antibiotics, probiotics, and prebiotics: gastroenterology enters the metagenomics era. Gastroenterology 136, 2015–2031.
40. Priestman, M.A., Funke, T., Singh, I.M., Crupper, S.S. and Schönbrunn, E. (2005) 5-Enolpyruvylshikimate-3-phosphate synthase from Staphylococcus aureus is insensitive to glyphosate. FEBS Lett 579, 728–732.
41. Rainey, F.A. and Stackebrandt, E. (1993) 16S rDNA analysis reveals phylogenetic diversity among polysaccharolytic clostridia. FEMS Microbiol Lett 113, 125–128.
42. Ramos, S., Tejido, M.L., Martínez, M.E., Ranilla, M.J. and Carro, M.D. (2009) Microbial protein synthesis, ruminal digestion, microbial populations, and nitrogen balance in sheep fed diets varying in forage-to-concentrate ratio and type of forage. J Anim Sci 87, 2924–2934.
43. Riede, S., Boguhn, J. and Breves, G. (2013) Studies on potential effects of fumaric acid on rumen microbial fermentation, methane production and microbial community. Arch Anim Nutr 67, 368–380.
44. Roberts, F., Roberts, C.W., Johnson, J.J., Kyle, D.E., Krell, T., Coggins, J.R., Coombs, G.H., Milhous, W.K. et al. (1998) Evidence for the shikimate pathway in apicomplexan parasites. Nature 393, 801–805.
45. Rodloff, A.C. and Krüger, M. (2012) Chronic Clostridium botulinum infections in farmers. Anaerobe 18, 226–228.
46. Roslycky, E.B. (1982) Glyphosate and the response of the soil microbiota. Soil Biol Biochem 14, 87–92.
47. Rueppel, M.L., Brightwell, B.B., Schaefer, J. and Marvel, J.T. (1977) Metabolism and degradation of glyphosate in soil and water. J Agric Food Chem 25, 517–528.
48. Schrödl, W., Krüger, S., Konstantinova-Müller, T., Shehata, A.A., Rulff, R. and Krüger, M. (2014) Possible effects of glyphosate on Mucorales abundance in the rumen of dairy cows in Germany. Curr Microbiol 69, 817–823.
49. Schwieger, F. and Tebbe, C.C. (1998) A new approach to utilize PCR-single-strand-conformation polymorphism for 16S rRNA gene-based microbial community analysis. Appl Environ Microbiol 64, 4870–4876.
50. Seyboldt, C., Discher, S., Jordan, E., Neubauer, H., Jensen, K.C., Campe, A., Kreienbrock, L., Scheu, T. et al. (2015) Occurrence of Clostridium botulinum neurotoxin in chronic disease of dairy cows. Vet Microbiol 177, 398–402.
51. Shehata, A.A., Schrödl, W., Aldin, A.A., Hafez, H.M. and Krüger, M. (2013) The effect of glyphosate on potential pathogens and beneficial members of poultry microbiota in vitro. Curr Microbiol 66, 350–358.
52. Sprankle, P., Meggit, W.F. and Penner, D. (1975) Adsorption, mobility and microbial degradation of glyphosate in the soil. Weed Sci 23, 229–234.
53. Stackebrandt, E., Kramer, I., Swiderski, J. and Hippe, H. (1999) Phylogenetic basis for a taxonomic dissection of the genus Clostridium. FEMS Immunol Med Microbiol 24, 253–258.
54. Stewart, C.S. and Bryant, M.P. (1988) The rumen bacteria. In The Rumen Microbial Ecosystem ed. Hobson, P.N. London and New York, NY: Elsevier Science Publications.
55. Trovatelli, L.D. and Matteuzzi, D. (1976) Presence of Bifidobacteria in the rumen of calves fed different rations. Appl Environ Microbiol 32, 470–473.
56. Von Soosten, D., Meyer, U., Hüther, L., Dänicke, S., Lahrssen-Wiederholt, M., Schafft, H., Spolders, M. and Breves, G. (2016) Excretion pathways and ruminal disappearance of glyphosate and its degradation product aminomethylphosphonic acid in dairy cows. J Dairy Sci 99, 1–7.
57. Weisburg, W.G., Barns, S.M., Pelletier, D.A. and Lane, D.J. (1991) 16S ribosomal DNA amplification for phylogenetic study. J Bacteriol 173, 697–703.