Bacteria, phages and pigs: The effects of in-feed antibiotics on the microbiome at different gut locations

ISME Journal

Volumn 8, Issue 8, 2014, Pages 1566-1576

  Looft, Torey ^a   Allen, Heather K ^a   Cantarel, Brandi L ^b   Levine, Uri Y ^a,e   Bayles, Darrell O ^a   Alt, David P ^a   Henrissat, Bernard ^c,d   Stanton, Thaddeus B ^a  

^a NATIONAL ANIMAL DISEASE CENTER   (United States)

^b BAYLOR INSTITUTE FOR IMMUNOLOGY RESEARCH   (United States)

^c AIX MARSEILLE UNIVERSITY   (France)

^d UNIVERSITY OF COPENHAGEN   (Denmark)

^e Novozymes Biotech Inc   (United States)

Author keywords

antibiotics; CAZy; gut ecology; metagenomics; microbiota; swine

Indexed keywords

ANTIINFECTIVE AGENT;

ANIMAL; ANIMAL FOOD; BACTERIOPHAGE; BACTERIUM; CLASSIFICATION; DRUG EFFECTS; FEMALE; GENETICS; INTESTINE; ISOLATION AND PURIFICATION; LARGE INTESTINE; MALE; MICROBIOLOGY; MICROFLORA; PIG; SMALL INTESTINE;

ANIMAL FEED; ANIMALS; ANTI-BACTERIAL AGENTS; BACTERIA; BACTERIOPHAGES; FEMALE; INTESTINE, LARGE; INTESTINE, SMALL; INTESTINES; MALE; MICROBIOTA; SWINE;

EID: 84904999639     PISSN: 17517362     EISSN: 17517370     Source Type: Journal    
DOI: 10.1038/ismej.2014.12     Document Type: Article

References (60)

1. Abedon ST. (2009). Phage evolution and ecology. Adv Appl Microbiol 67: 1-45.
2. Allen HK, Looft T, Bayles DO, Humphrey S, Levine UY, Alt D et al. (2011). Antibiotics in feed induce prophages in swine fecal microbiomes. MBio 2: e00260-11.
3. Allison MJ, Robinson IM, Bucklin JA, Booth GD. (1979). Comparison of bacterial populations of the pig cecum and colon based upon enumeration with specific energy sources. Appl Environ Microbiol 37: 1142-1151.
4. Aristoteli LP, Willcox MD. (2003). Mucin degradation mechanisms by distinct Pseudomonas aeruginosa isolates in vitro. Infect Immun 71: 5565-5575.
5. Ashida H, Ogawa M, Kim M, Mimuro H, Sasakawa C. (2012). Bacteria and host interactions in the gut epithelial barrier. Nat Chem Biol 8: 36-45.
6. Azcarate-Peril MA, Foster DM, Cadenas MB, Stone MR, Jacobi SK, Stauffer SH et al. (2011). Acute necrotizing enterocolitis of preterm piglets is characterized by dysbiosis of ileal mucosa-associated bacteria. Gut Microbes 2: 234-243.
7. Bird AR, Conlon MA, Christophersen CT, Topping DL. (2010). Resistant starch, large bowel fermentation and a broader perspective of prebiotics and probiotics. Benef Microbes 1: 423-431.
8. Booijink CC, El-Aidy S, Rajilic-Stojanovic M, Heilig HG, Troost FJ, Smidt H et al. (2010). High temporal and inter-individual variation detected in the human ileal microbiota. Environ Microbiol 12: 3213-3227.
9. Bunge J. (2011). Estimating the number of species with CatchAll. Pac Symp Biocomput 11: 121-130.
10. Cantarel BL, Coutinho PM, Rancurel C, Bernard T, Lombard V, Henrissat B. (2009). The Carbohydrate-Active EnZymes database (CAZy): an expert resource for glycogenomics. Nucleic Acids Res 37: D233-D238.
11. Cantarel BL, Lombard V, Henrissat B. (2012). Complex carbohydrate utilization by the healthy human micro-biome. PLoS One 7: e28742.
12. Chichlowski M, Croom WJ, Edens FW, McBride BW, Qiu R, Chiang CC et al. (2007). Microarchitecture and spatial relationship between bacteria and ileal, cecal, and colonic epithelium in chicks fed a direct-fed microbial, PrimaLac, and salinomycin. Poult Sci 86: 1121-1132.
13. Cole JR, Wang Q, Cardenas E, Fish J, Chai B, Farris RJ et al. (2009). The Ribosomal Database Project: improved alignments and new tools for rRNA analysis. Nucleic Acids Res 37: D141-D145.
14. Cromwell GL. (2002). Why and how antibiotics are used in swine production. Anim Biotechnol 13: 7-27.
15. Cuiv PO, Klaassens ES, Durkin AS, Harkins DM, Foster L, McCorrison J et al. (2011). Draft genome sequence of Turicibacter sanguinis PC909, isolated from human feces. J Bacteriol 193: 1288-1289.
16. Dibner JJ, Richards JD. (2005). Antibiotic growth promoters in agriculture: history and mode of action. Poult Sci 84: 634-643.
17. Edgar RC, Haas BJ, Clemente JC, Quince C, Knight R. (2011). UCHIME improves sensitivity and speed of chimera detection. Bioinformatics 27: 2194-2200.
18. Gomez-Alvarez V, Teal TK, Schmidt TM. (2009). Systematic artifacts in metagenomes from complex microbial communities. ISME J 3: 1314-1317.
19. Green GL, Brostoff J, Hudspith B, Michael M, Mylonaki M, Rayment N et al. (2006). Molecular characterization of the bacteria adherent to human colorectal mucosa. J Appl Microbiol 100: 460-469.
20. Hamady M, Walker JJ, Harris JK, Gold NJ, Knight R. (2008). Error-correcting barcoded primers for pyrosequencing hundreds of samples in multiplex. Nat Methods 5: 235-237.
21. Hammer Ø, Harper DAT, Ryan PD. (2001). PAST: paleon-tological statistics software package for education and data analysis. Palaeontol Electron 4: 9.
22. Hao WL, Lee YK. (2004). Microflora of the gastrointestinal tract: a review. Method Mol Biol 268: 491-502.
23. Heilig HG, Zoetendal EG, Vaughan EE, Marteau P, Akkermans AD, de Vos WM. (2002). Molecular diversity of Lactobacillus spp. and other lactic acid bacteria in the human intestine as determined by specific amplification of 16S ribosomal DNA. Appl Environ Microbiol 68: 114-123.
24. Hill DA, Hoffmann C, Abt MC, Du Y, Kobuley D, Kirn TJ et al. (2010). Metagenomic analyses reveal antibiotic-induced temporal and spatial changes in intestinal microbiota with associated alterations in immune cell homeostasis. Mucosal Immunol 3: 148-158.
25. Hillman K, Whyte AL, Stewart CS. (1993). Dissolved oxygen in the porcine gastrointestinal tract. Lett Appl Microbiol 16: 299-302.
26. Kim HB, Borewicz K, White BA, Singer RS, Sreevatsan S, Tu Z J et al. (2012). Microbial shifts in the swine distal gut in response to the treatment with antimicrobial growth promoter, tylosin. Proc Natl Acad Sci USA 109: 15485-15490.
27. Lamendella R, Domingo JW, Ghosh S, Martinson J, Oerther DB. (2011). Comparative fecal metagenomics unveils unique functional capacity of the swine gut. BMC Microbiol 11: 103.
28. Lee SM, Donaldson GP, Mikulski Z, Boyajian S, Ley K, Mazmanian SK. (2013). Bacterial colonization factors control specificity and stability of the gut microbiota. Nature 501: 426-429.
29. Leser TD, Amenuvor JZ, Jensen TK, Lindecrona RH, Boye M, Moller K. (2002). Culture-independent analysis of gut bacteria: the pig gastrointestinal tract microbiota revisited. Appl Environ Microbiol 68: 673-690.
30. Levine UV, Looft T, Allen HK, Stanton TB. (2013). Butyrate-producing bacteria, including mucin degra-ders, from the swine intestinal tract. Appl Environ Microbiol 79: 3879-3881.
31. Liu B, Pop M. (2009). ARDB-Antibiotic Resistance Genes Database. Nucleic Acids Res 37: D443-D447.
32. Looft T, Johnson TA, Allen HK, Bayles DO, Alt DP, Stedtfeld RD et al. (2012). In-feed antibiotic effects on the swine intestinal microbiome. Proc Natl Acad Sci USA 109: 1691-1696.
33. Mahowald MA, Rey FE, Seedorf H, Turnbaugh PJ, Fulton RS, Wollam A et al. (2009). Characterizing a model human gut microbiota composed of members of its two dominant bacterial phyla. Proc Natl Acad Sci USA 106: 5859-5864.
34. McAllister TA, Beauchemin KA, Alazzeh AY, Baah J, Teather RM, Stanford K. (2011). Review: the use of direct fed microbials to mitigate pathogens and enhance production in cattle. Can J Anim Sci 91: 193-211.
35. Muyzer G, de Waal EC, Uitterlinden AG. (1993). Profiling of complex microbial populations by denaturing gradient gel electrophoresis analysis of polymerase chain reaction-amplified genes coding for 16S rRNA. Appl Environ Microbiol 59: 695-700.
36. Nava GM, Friedrichsen HJ, Stappenbeck TS. (2011). Spatial organization of intestinal microbiota in the mouse ascending colon. ISME J 5: 627-638.
37. Ng KM, Ferreyra JA, Higginbottom SK, Lynch JB, Kashyap PC, Gopinath S et al. (2013). Microbiota-liberated host sugars facilitate post-antibiotic expansion of enteric pathogens. Nature 502: 96-99.
38. On SL. (1996). Identification methods for campylobacters, helicobacters, and related organisms. Clin Microbiol Rev 9: 405-422.
39. Parks DH, Beiko RG. (2010). Identifying biologically relevant differences between metagenomic communities. Bioinformatics 26: 715-721.
40. Pryde SE, Richardson AJ, Stewart CS, Flint HJ. (1999). Molecular analysis of the microbial diversity present in the colonic wall, colonic lumen, and cecal lumen of a pig. Appl Environ Microbiol 65: 5372-5377.
41. Qin J, Li R, Raes J, Arumugam M, Burgdorf KS, Manichanh C et al. (2010). A human gut microbial gene catalogue established by metagenomic sequencing. Nature 464: 59-65.
42. Quince C, Lanzen A, Davenport R, Turnbaugh P. (2011). Removing noise from pyrosequenced amplicons. BMC Bioinformatics 12: 38.
43. Ripp S, Miller RV. (1997). The role of pseudolysogeny in bacteriophage-host interactions in a natural freshwater environment. Microbiology 143: 2065-2070.
44. Rosengren LB, Waldner CL, Reid-Smith RJ, Dowling PM, Harding JC. (2007). Associations between feed and water antimicrobial use in farrow-to-finish swine herds and antimicrobial resistance of fecal Escherichia coli from grow-finish pigs. Microb Drug Resist 13: 261-269.
45. Savage DC. (1987). Microorganisms associated with epithelial surfaces and stability of the indigenous gastrointestinal microflora. Nahrung 31: 383-395.
46. Schloss PD, Westcott SL, Ryabin T, Hall JR, Hartmann M, Hollister EB et al. (2009). Introducing mothur: open-source, platform-independent, community-supported software for describing and comparing microbial communities. Appl Environ Microbiol 75: 7537-7541.
47. Schloss PD, Gevers D, Westcott SL. (2011). Reducing the effects of PCR amplification and sequencing artifacts on 16S rRNA-based studies. PLoS One 6: e27310.
48. Seshadri R, Kravitz SA, Smarr L, Gilna P, Frazier M. (2007). CAMERA: a community resource for metage-nomics. PLoS Biol 5: e75.
49. Shinohara K, Ohashi Y, Kawasumi K, Terada A, Fujisawa T. (2010). Effect of apple intake on fecal microbiota and metabolites in humans. Anaerobe 16: 510-515.
50. Siunov AV, Nikitin DV, Suzina NE, Dmitriev VV, Kuzmin NP, Duda VI. (1999). Phylogenetic status of Anaerobacter polyendosporus, an anaerobic, polysporogenic bacterium. Int J Syst Bacteriol 49: 1119-1124.
51. Suchodolski JS, Ruaux CG, Steiner JM, Fetz K, Williams DA. (2005). Assessment of the qualitative variation in bacterial microflora among compartments of the intestinal tract of dogs by use of a molecular fingerprinting technique. Am J Vet Res 66: 1556-1562.
52. Takahashi T, Sakaguchi E. (2006). Transport of bacteria across and along the large intestinal lumen of guinea pigs. J Comp Physiol B 176: 173-178.
53. Tsang KW, Rutman A, Tanaka E, Lund V, Dewar A, Cole PJ et al. (1994). Interaction of Pseudomonas aeruginosa with human respiratory mucosa in vitro. Eur Respir J 7: 1746-1753.
54. Weisburg WG, Barns SM, Pelletier DA, Lane DJ. (1991). 16S ribosomal DNA amplification for phylogenetic study. J Bacteriol 173: 697-703.
55. White JR, Nagarajan N, Pop M. (2009). Statistical methods for detecting differentially abundant features in clinical metagenomic samples. PLoS Comput Biol 5: e1000352.
56. Whitman WB, Coleman DC, Wiebe WJ. (1998). Prokaryotes: the unseen majority. Proc Natl Acad Sci USA 95: 6578-6583.
57. Williams BL, Hornig M, Buie T, Bauman ML, Cho Paik M, Wick I et al. (2011). Impaired carbohydrate digestion and transport and mucosal dysbiosis in the intestines of children with autism and gastrointestinal disturbances. PLoS One 6: e24585.
58. Zhang Z, Geng J, Tang X, Fan H, Xu J, Wen X et al. (2014). Spatial heterogeneity and co-occurrence patterns of human mucosal-associated intestinal microbiota. ISME J 8: 881-893.
59. Zoetendal EG, von Wright A, Vilpponen-Salmela T, Ben-Amor K, Akkermans AD, de Vos WM. (2002). Mucosa-associated bacteria in the human gastrointestinal tract are uniformly distributed along the colon and differ from the community recovered from feces. Appl Environ Microbiol 68: 3401-3407.
60. Zoetendal EG, Raes J, van den Bogert B, Arumugam M, Booijink CC, Troost FJ et al. (2012). The human small intestinal microbiota is driven by rapid uptake and conversion of simple carbohydrates. ISME J 6: 1415-1426.