Increased dietary zinc oxide changes the bacterial core and enterobacterial composition in the ileum of piglets

Journal of Animal Science

Volumn 89, Issue 8, 2011, Pages 2430-2439

  Vahjen, W ^a   Pieper, R ^a   Zentek, J ^a  

^a FREIE UNIVERSITÄT BERLIN   (Germany)

Author keywords

Bacterial core; Microbiota; Piglet; Pyrosequencing; Zinc oxide

Indexed keywords

ZINC OXIDE;

ANIMAL; ANIMAL DISEASE; ANIMAL FOOD; ARTICLE; CLASSIFICATION; CLINICAL TRIAL; CONTROLLED CLINICAL TRIAL; CONTROLLED STUDY; DIET; DOSE RESPONSE; DRUG EFFECT; ENTEROBACTERIACEAE; GENETICS; ILEUM; MICROBIOLOGY; PHYLOGENY; SWINE;

ANIMAL FEED; ANIMAL NUTRITIONAL PHYSIOLOGICAL PHENOMENA; ANIMALS; DIET; DOSE-RESPONSE RELATIONSHIP, DRUG; ENTEROBACTERIACEAE; ILEUM; PHYLOGENY; SWINE; ZINC OXIDE;

BACTERIA (MICROORGANISMS); ENTEROBACTERIACEAE; LACTOBACILLUS REUTERI; LEUCONOSTOC CITREUM; SARCINA VENTRICULI; STREPTOCOCCUS EQUINUS; WEISSELLA CIBARIA;

EID: 80052583902     PISSN: 00218812     EISSN: 15253163     Source Type: Journal    
DOI: 10.2527/jas.2010-3270     Document Type: Article

References (55)

1. Aarestrup, F. M., and H. Hasman. 2004. Susceptibility of different bacterial species isolated from food animals to copper sulphate, zinc chloride and antimicrobial substances used for disinfection. Vet. Microbiol. 100:83-89.
2. Amezcua, R., M. Friendship, and C. E. Dewey. 2008. An investigation of the presence of Escherichia coli O149:K91:F4 on pig farms in southern Ontario and the use of antimicrobials and risk factors associated with the presence of this serogroup. Can. Vet. J. 49:39-45.
3. Armougom, F., and D. Raoult. 2008. Use of pyrosequencing and DNA barcodes to monitor variations in Firmicutes and Bacteroidetes communities in the gut microbiota of obese humans. BMC Genomics 9:576-588.
4. Baker, G. C., J. J. Smith, and D. A. Cowan. 2003. Review and reanalysis of domain-specific 16S primers. J. Microbiol. Methods 55:541-555.
5. Broom, L. J., H. M. Miller, K. G. Kerr, and J. S. Knapp. 2006. Effects of zinc oxide and Enterococcus faecium SF68 dietary supplementation on the performance, intestinal microbiota and immune status of weaned piglets. Res. Vet. Sci. 80:45-54.
6. Carlson, D., J. Sehested, Z. Feng, and H. D. Poulson. 2008. Serosal zinc attenuate serotonin and vasoactive intestinal peptide induced secretion in piglet small intestinal epithelium in vitro. Comp. Biochem. Physiol. A Mol. Integr. Physiol. 149:51-58.
7. Chen, Y. Y., C. W. Feng, C. F. Chiu, and R. A. Burne. 2008. cadDX operon of Streptococcus salivarius 57.I. Appl. Environ. Microbiol. 74:1642-1645.
8. Choudhury, R., and S. Srivastava. 2001. Zinc resistance mechanisms in bacteria. Curr. Sci. 81:768-775.
9. Cleusix, V., C. Lacroix, S. Vollenweider, M. Duboux, and G. Le Blay. 2007. Inhibitory activity spectrum of reuterin produced by Lactobacillus reuteri against intestinal bacteria. BMC Microbiol. 7:101-110.
10. Crowther, J. S. 1971. Sarcina ventriculi in human faeces. J. Med. Microbiol. 4:343-350.
11. Dintzis, F. R., J. A. Laszlo, T. C. Nelsen, F. L. Baker, and C. C. Calvert. 1995. Free and total ion concentrations in pig digesta. J. Anim. Sci. 73:1138-1146.
12. Dowd, S. E., Y. Sun, R. D. Wolcott, A. Domingo, and J. A. Carroll. 2008. Bacterial tag-encoded FLX amplicon pyrosequencing (bTEFAP) for microbiome studies: Bacterial diversity in the ileum of newly weaned Salmonella-infected pigs. Foodborne Pathog. Dis. 5:459-472.
13. Fairbrother, J. M., E. Nadeau, and C. L. Gyles. 2005. Escherichia coli in postweaning diarrhea in pigs; an update on bacterial types, pathogenesis, and prevention strategies. Anim. Health Res. Rev. 6:17-39.
14. Gill, S. R., M. Pop, R. T. Deboy, P. B. Eckburg, P. J. Turnbaugh, B. S. Samuel, J. L. Gordon, D. A. Relman, C. M. Fraser-Liggett, and K. E. Nelson. 2006. Metagenomic analysis of the human distal gut microbiome. Science 312:1355-1359.
15. Hamady, M., J. J. Walker, J. K. Harris, N. J. Gold, and R. Knight. 2008. Error-correcting barcoded primers for pyrosequencing hundreds of samples in multiplex. Nat. Methods 5:235-237.
16. Hedemann, M. S., B. B. Jensen, and H. D. Poulsen. 2006. Influence of dietary zinc and copper on digestive enzyme activity and intestinal morphology in weaned pigs. J. Anim. Sci. 84:3310-3320.
17. Hill, J. E., S. M. Hemmingsen, B. G. Goldade, T. J. Dumonceaux, J. Klassen, R. T. Zijlstra, S. H. Goh, and A. G. Van Kessel. 2005. Comparison of ileum microflora of pigs fed corn-, wheat-, or barley-based diets by chaperonin-60 sequencing and quantitative PCR. Appl. Environ. Microbiol. 71:867-875.
18. Hojberg, O., N. Canibe, H. D. Poulsen, M. S. Hedemann, and B. B. Jensen. 2005. Influence of dietary zinc oxide and copper sulfate on the gastrointestinal ecosystem in newly weaned piglets. Appl. Environ. Microbiol. 71:2267-2277.
19. Hollis, G. R., S. D. Carter, T. R. Cline, T. D. Crenshaw, G. L. Cromwell, G. M. Hill, S. W. Kim, A. J. Lewis, D. C. Mahan, P. S. Miller, H. H. Stein, and T. L. Veum. 2005. Effects of replacing pharmacological levels of dietary zinc oxide with lower dietary levels of various organic zinc sources for weanling pigs. J. Anim. Sci. 83:2123-2129.
20. Holm, A. 1988. Escherichia coli-associated post-weaning diarrhoea in piglets. Zinc oxide added to feed as an antibacterial agent? Dansk Veterinaertidsskrift 71:1118-1126.
21. Holmgren, N. 1994. Prophylactic effects of zinc oxide or olaquindox against weaning diarrhoea in pigs. Svensk Veterinartidning 46:217-222.
22. Huse, S. M., J. A. Huber, H. G. Morrison, M. L. Sogin, and D. M. Welch. 2007. Accuracy and quality of massively parallel DNA pyrosequencing. Genome Biol. 8:R143.2-143.9.
23. Husted, L., T. K. Jensen, S. N. Olsen, and L. Molbak. 2010. Examination of equine glandular stomach lesions for bacteria, including Helicobacter spp. by fluorescence in situ hybridisation. BMC Microbiol. 10:84-91.
24. Jacob, M. E., J. T. Fox, T. G. Nagaraja, J. S. Drouillard, R. G. Amachawadi, and S. K. Narayanan. 2010. Effects of feeding elevated concentrations of copper and zinc on the antimicrobial susceptibilities of fecal bacteria in feedlot cattle. Foodborne Pathog. Dis. 7:643-648.
25. Katouli, M., L. Melin, M. Jensen-Waern, P. Wallgren, and R. Mollby. 1999. The effect of zinc oxide supplementation on the stability of the intestinal flora with special reference to composition of coliforms in weaned pigs. J. Appl. Microbiol. 87:564-573.
26. Kunin, V., A. Engelbrektson, H. Ochman, and P. Hugenholtz. 2010. Wrinkles in the rare biosphere: Pyrosequencing errors lead to artificial inflation of diversity estimates. Environ. Microbiol. 12:118-123.
27. Kwak, T. J., and J. T. Peterson. 2007. Community indices, parameters, and comparisons. Pages 677-763 in Analysis and Interpretation of Freshwater Fisheries Data. C. S. Guy and M. L. Brown, ed. American Fisheries Society, Bethesda, MD.
28. Ludwig, W., O. Strunk, R. Westram, L. Richter, H. Meier, A. Buchner, T. Lai, S. Steppi, G. Jobb, W. Forster, I. Brettske, S. Gerber, A. W. Ginhart, O. Gross, S. Grumann, S. Hermann, R. Jost, A. Konig, T. Liss, R. Lusmann, M. May, B. Nonhoff, B. Reichel, R. Strehlow, A. Stamatakis, N. Stuckmann, A. Vilbig, M. Lenke, T. Ludwig, A. Bode, and K.-H. Schleifer. 2004. ARB: A software environment for sequence data. Nucleic Acids Res. 32:1363-1371.
29. Meyer, F., D. Paarmann, M. D'Souza, R. Olson, E. M. Glass, M. Kubal, T. Paczian, A. Rodriguez, R. Stevens, A. Wilke, J. Wilkening, and R. A. Edwards. 2008. The Metagenomics RAST server-A public resource for the automatic phylogenetic and functional analysis of metagenomes. BMC Bioinformatics 9:386.
30. Mores, N., J. Christani, I. A. Piffer, W. Barioni, and G. M. M. Lima. 1998. Effects of zinc oxide on postweaning diarrhea control in pigs experimentally infected with E. coli. Arq. Brasil Med. Vet. Zootec. 50:513-523.
31. Morita, H., T. Kuwahara, K. Ohshima, H. Sasamoto, K. Itoh, M. Hattori, T. Hayashi, and H. Takami. 2007. An improved DNA isolation method for metagenomic analysis of the microbial flora of the human intestine. Microbes Environ. 22:214-222.
32. Nechvatal, J. M., J. L. Ram, M. D. Basson, P. Namprachan, S. R. Niec, K. Z. Badsha, L. H. Matherly, A. P. Majumdar, and I. Kato. 2008. Fecal collection ambient preservation and DNA extraction for PCR amplification of bacterial and human markers from human feces. J. Microbiol. Methods 72:124-132.
33. Nies, D. H. 1992. Resistance to cadmium, cobalt, zinc, and nickel in microbes. Plasmid 27:17-28.
34. Nies, D. H., and S. Silver. 1995. Ion efflux systems involved in bacterial metal resistances. J. Ind. Microbiol. 14:186-199.
35. Overbeek, R., T. Begley, R. M. Butler, J. V. Choudhuri, H. Y. Chuang, M. de Cohoon, V. Crecy-Lagard, N. Diaz, T. Disz, R. Edwards, M. Fonstein, E. D. Frank, S. Gerdes, E. M. Glass, A. Goesmann, A. Hanson, D. Iwata-Reuyl, R. Jensen, N. Jamshidi, L. Krause, M. Kubal, N. Larsen, B. Linke, A. C. McHardy, F. Meyer, H. Neuweger, G. Olsen, R. Olson, A. Osterman, V. Portnoy, G. D. Pusch, D. A. Rodionov, C. Ruckert, J. Steiner, R. Stevens, I. Thiele, O. Vassieva, Y. Ye, O. Zagnitko, and V. Vonstein. 2005. The subsystems approach to genome annotation and its use in the project to annotate 1000 genomes. Nucleic Acids Res. 33:5691-5702.
36. Owaki, K., R. E. Hungate, L. Lotter, R. R. Hofmann, and G. Maloiy. 1974. Stomach fermentation in East African Colobus monkeys in their natural state. Appl. Microbiol. 27:713-723.
37. Papathanasopoulos, M. A., F. Krier, A. M. Revol-Junelles, G. Lefebvre, J. P. Le Caer, A. von Holy, and J. W. Hastings. 1997. Multiple bacteriocin production by Leuconostoc mesenteroides TA33a and other Leuconostoc/Weissella strains. Curr. Microbiol. 35:331-335.
38. Pieper, R., P. Janczyk, A. Zeyner, H. Smidt, V. Guiard, and W. B. Souffrant. 2008. Ecophysiology of the developing total bacterial and lactobacillus communities in the terminal small intestine of weaning piglets. Microb. Ecol. 56:474-483.
39. Poulsen, H. D. 1995. Zinc oxide for weanling piglets. Acta Agric. Scand. Anim. Sci. 45:159-167.
40. Pruesse, E., C. Quast, K. Knittel, B. Fuchs, W. Ludwig, J. Peplies, and F. O. Glockner. 2007. SILVA: A comprehensive online resource for quality checked and aligned ribosomal RNA sequence data compatible with ARB. Nucleic Acids Res. 35:7188-7196.
41. Salminen, S., A. von Wright, and A. C. Ouwehand. 2004. Lactic Acid Bacteria: Microbiological and Functional Aspects. 3rd ed. Page 11 in Classification and Physiology. S. Salminen, A. von Wright, A. C. Ouwehand, and S. Lahtinen, ed. Marcel Dekker Inc., New York, NY.
42. Salonen, A., J. Nikkila, J. Jalanka-Tuovinen, O. Immonen, M. Rajilic-Stojanovic, R. A. Kekkonen, A. Palva, and W. M. de Vos. 2010. Comparative analysis of fecal DNA extraction methods with phylogenetic microarray: Effective recovery of bacterial and archaeal DNA using mechanical cell lysis. J. Microbiol. Methods 81:127-134.
43. Sawai, J., H. Igarashi, A. Hashimoto, T. Kokugan, and M. Shimizu. 1996. Effect of particle size and heating temperature of ceramic powders on antibacterial activity of their slurries. J. Chem. Eng. Jpn. 29:251-256.
44. Schmalenberger, A., F. Schwieger, and C. C. Tebbe. 2001. Effect of primers hybridizing to different evolutionarily conserved regions of the small-subunit rRNA gene in PCR-based microbial community analyses and genetic profiling. Appl. Environ. Microbiol. 67:3557-3563.
45. Sghir, A., D. Antonopoulos, and R. I. Mackie. 1998. Design and evaluation of a Lactobacillus group-specific ribosomal RNA-targeted hybridization probe and its application to the study of intestinal microecology in pigs. Syst. Appl. Microbiol. 21:291-296.
46. Silver, S. 1996. Bacterial heavy metal resistance. New surprises. Annu. Rev. Microbiol. 50:753-789.
47. Silver, S., and M. Walderhaug. 1992. Gene regulation of plasmidand chromosome-determined inorganic ion transport in bacteria. Microbiol. Rev. 56:195-228.
48. Sipos, R., A. J. Szekely, M. Palatinszky, S. Revesz, K. Marialigeti, and M. Nikolausz. 2007. Effect of primer mismatch annealing temperature and PCR cycle number on 16S rRNA gene-targeting bacterial community analysis. FEMS Microbiol. Ecol. 60:341-350.
49. Smith, D. C. 1991. Dental cements. Curr. Opin. Dent. 1:228-234.
50. Snyder, L. A., N. Loman, M. J. Pallen, and C. W. Penn. 2009. Nextgeneration sequencing-The promise and perils of charting the great microbial unknown. Microb. Ecol. 57:1-3.
51. Srionnual, S., F. Yanagida, L. H. Lin, K. N. Hsiao, and Y. S. Chen. 2007. Weissellicin 110, a newly discovered bacteriocin from Weissella cibaria 110, isolated from plaa-som, a fermented fish product from Thailand. Appl. Environ. Microbiol. 73:2247-2250.
52. Thanantong, N., S. Edwards, and O. A. Sparagano. 2006. Characterization of lactic acid bacteria and other gut bacteria in pigs by a macroarraying method. Ann. N. Y. Acad. Sci. 1081:276-279.
53. Vatn, S., G. Gunnes, K. Nybo, and H. M. Juul. 2000. Possible involvement of Sarcina ventriculi in canine and equine acute gastric dilatation. Acta Vet. Scand. 41:333-337.
54. Wang, X., D. Ou, J. Yin, G. Wu, and J. Wang. 2009. Proteomic analysis reveals altered expression of proteins related to glutathione metabolism and apoptosis in the small intestine of zinc oxide-supplemented piglets. Amino Acids 37:209-218.
55. Yin, J., X. Li, D. Li, T. Yue, Q. Fang, J. Ni, X. Zhou, and G. Wu. 2009. Dietary supplementation with zinc oxide stimulates ghrelin secretion from the stomach of young pigs. J. Nutr. Biochem. 20:783-790.