Hostname: page-component-cd9895bd7-mkpzs Total loading time: 0 Render date: 2024-12-22T11:54:00.310Z Has data issue: false hasContentIssue false
  • English
  • Français

The intestinal microbiome of the pig

Published online by Cambridge University Press:  04 July 2012

Richard Isaacson  and
Hyeun Bum Kim
Richard Isaacson*
Affiliation:
Department of Veterinary and Biomedical Sciences, College of Veterinary Medicine, University of Minnesota, 1971 Commonwealth Ave., St. Paul, Minnesota 55108, USA
Hyeun Bum Kim
Affiliation:
Department of Veterinary and Biomedical Sciences, College of Veterinary Medicine, University of Minnesota, 1971 Commonwealth Ave., St. Paul, Minnesota 55108, USA
*
*Corresponding author. E-mail: [email protected]
Get access Rights & Permissions [Opens in a new window]

Abstract

The intestinal microbiome has been the subject of study for many decades because of its importance in the health and well being of animals. The bacterial components of the intestinal microbiome have closely evolved as animals have and in so doing contribute to the overall development and metabolic needs of the animal. The microbiome of the pig has been the subject of many investigations using culture-dependent methods and more recently using culture-independent techniques. A review of the literature is consistent with many of the ecologic principles put forth by Rene Dubos. Animals develop an intestinal microbiome over time and space. During the growth and development of the pig, the microbiome changes in composition in a process known as the microbial succession. There are clear and distinct differences in the composition of the pig intestinal microbiome moving from the proximal end of the intestinal tract to the distal end. The majority (>90%) of the bacteria in the pig intestinal microbiome are from two Phyla: Firmicutes and Bacteroidetes. However, the ileum has a high percentage of bacteria in the phylum Proteobacterium (up to 40%). Perturbations to the microbiome occur in response to many factors including stresses, treatment with antibiotics, and diet.

Keywords

Pig intestinesmicrofloramicrobial community structuretaxonomy
Type
Review Article
Information
Animal Health Research Reviews , Volume 13 , Issue 1 , June 2012 , pp. 100 - 109
Copyright
Copyright © Cambridge University Press 2012

Access options

Get access to the full version of this content by using one of the access options below. (Log in options will check for institutional or personal access. Content may require purchase if you do not have access.)

References

Allen, HK, Looft, T, Bayles, DO, Humphrey, S, Levine, UY, Alt, D and Stanton, TB (2011). Antibiotics in feed induce prophages in swine fecal microbiomes. mBio 2.Google Scholar
Allison, MJ, Robinson, IM, Bucklin, JA and Booth, GD (1979). Comparison of bacterial populations of the pig cecum and colon based upon enumeration with specific energy sources. Applied and Environmental Microbiology 37: 1142–1151.CrossRefGoogle ScholarPubMed
Backhed, F, Ley, RE, Sonnenburg, JL, Peterson, DA and Gordon, JI (2005). Host–bacterial mutualism in the human intestine. Science 307: 1915–1920.Google Scholar
Berg, RD (1996). The indigenous gastrointestinal microflora. Trends in Microbiology 4: 430–435.CrossRefGoogle ScholarPubMed
Brogden, KA, Guthmiller, JM and Taylor, CE (2005). Human polymicrobial infections. Lancet 365: 253–255.Google Scholar
Bryant, MP (1972). Commentary on the Hungate technique for culture of anaerobic bacteria. American Journal of Clinical Nutrition 25: 1324–1328.CrossRefGoogle ScholarPubMed
Collier, CT, Smiricky-Tjardes, MR, Albin, DM, Wubben, JE, Gabert, VM, Deplancke, B, Bane, D, Anderson, DB and Gaskins, HR (2003). Molecular ecological analysis of porcine ileal microbiota responses to antimicrobial growth promoters. Journal of Animal Science 81: 3035–3045.CrossRefGoogle ScholarPubMed
Dethlefsen, L, Huse, S, Sogin, ML and Relman, DA (2008). The pervasive effects of an antibiotic on the human gut microbiota, as revealed by deep 16S rRNA sequencing. PLoS Biology 6: e280.CrossRefGoogle ScholarPubMed
Dowd, SE, Callaway, TR and Morrow-Tesch, J (2007). Handling may cause increased shedding of Escherichia coli and total coliforms in pigs. Foodborne Pathogens and Disease 4: 99–102.Google Scholar
Dowd, SE, Sun, Y, Wolcott, RD, Domingo, A and Carroll, JA (2008). Bacterial tag-encoded FLX amplicon pyrosequencing (bTEFAP) for microbiome studies: bacterial diversity in the ileum of newly weaned Salmonella-infected pigs. Foodborne Pathogens and Disease 5: 459–472.Google Scholar
Dubos, R, Schaedler, RW, Costello, R and Hoet, P (1965). Indigenous, normal, and autochthonous flora of the gastrointestinal tract. Journal of Experimental Medicine 122: 67–76.Google Scholar
Fox, G, Stackebrandt, E, Hespell, R, Gibson, J, Maniloff, J, Dyer, TA, Wolfe, RS, Balch, WE, Tanner, RS, Magrum, LJ, Zablen, LB, Blakemore, R, Gupta, R, Bonen, L, Lewis, BJ, Stahl, DA, Luehrsen, KR, Chen, KN and Woese, CR (1980). The phylogeny of prokaryotes. Science 209: 457–463.CrossRefGoogle ScholarPubMed
Gilliland, SE and Speck, ML (1977). Deconjugation of bile acids by intestinal lactobacilli. Applied and Environmental Microbiology 33: 15–18.Google Scholar
International Human Genome Sequencing Consortium (2004). Finishing the euchromatic sequence of the human genome. Nature 431: 931–945.Google Scholar
Isaacson, R, Borewicz, K, Kim, HB, Vannucci, F, Gebhart, C, Singer, R, Sreevatsan, S and Johnson, T (2011). Lawsonia interacellularis increases Salmonella enterica levels in the intestines of pigs. In Conference of Research Workers in Animal Diseases, Chicago, Illinois, abstract #107.Google Scholar
Isaacson, RE, Firkins, LD, Weigel, RM, Zuckermann, FA and DiPietro, JA (1999). Effect of transportation and feed withdrawal on shedding of Salmonella Typhimurium among experimentally infected pigs. American Journal of Veterinary Research 60: 1155–1158.CrossRefGoogle ScholarPubMed
Janczyk, P, Pieper, R, Smidt, H and Souffrant, WB (2007). Changes in the diversity of pig ileal lactobacilli around weaning determined by means of 16S rRNA gene amplification and denaturing gradient gel electrophoresis. FEMS Microbiology Ecology 61: 132–140.CrossRefGoogle ScholarPubMed
Kim, HB, Borewicz, K, White, BA, Singer, RS, Sreevatsan, S, Tu, ZJ and Isaacson, RE (2011). Longitudinal investigation of the age-related bacterial diversity in the feces of commercial pigs. Veterinary Microbiology 153: 124–133.Google Scholar
Lamendella, R, Domingo, JW, Ghosh, S, Martinson, J and Oerther, DB (2011). Comparative fecal metagenomics unveils unique functional capacity of the swine gut. BMC Microbiology 11: 103.Google Scholar
Lederberg, J and McCray, AT (2001). ‘Ome sweet’ omics – a genealogical treasury of words. The Scientist 15: 8.Google Scholar
Leser, TD, Amenuvor, JZ, Jensen, TK, Lindecrona, RH, Boye, M and Moller, K (2002). Culture-independent analysis of gut bacteria: the pig gastrointestinal tract microbiota revisited. Applied and Environmental Microbiology 68: 673–690.CrossRefGoogle ScholarPubMed
Leser, TD, Lindecrona, RH, Jensen, TK, Jensen, BB and Moller, K (2000). Changes in bacterial community structure in the colon of pigs fed different experimental diets and after infection with Brachyspira hyodysenteriae. Applied and Environmental Microbiology 66: 3290–3296.CrossRefGoogle ScholarPubMed
Leslie, M (2012). Immunology. Gut microbes keep rare immune cells in line. Science 335: 1428.Google Scholar
Looft, T, Johnson, TA, Allen, HK, Bayles, DO, Alt, DP, Stedtfeld, RD, Chai, B, Cole, JR, Hashsham, SA, Tiedje, JM and Stanton, TB (2012). In-feed antibiotic effects on the swine intestinal microbiome. Proceedings of the National Academy of Sciences, USA 109: 1691–1696.CrossRefGoogle ScholarPubMed
Luckey, TD (1972). Introduction to intestinal microecology. American Journal of Clinical Nutrition 25: 1292–1294.CrossRefGoogle ScholarPubMed
Mazmanian, SK, Liu, CH, Tzianabos, AO and Kasper, DL (2005). An immunomodulatory molecule of symbiotic bacteria directs maturation of the host immune system. Cell 122: 107–118.Google Scholar
Nocker, A, Burr, M and Camper, AK (2007). Genotypic microbial community profiling: a critical technical review. Microbial Ecology 54: 276–289.Google Scholar
Olsen, GJ and Woese, CR (1993). Ribosomal RNA: a key to phylogeny. FASEB Journal 7: 113–123.Google Scholar
Peterson, J, Garges, S, Giovanni, M, McInnes, P, Wang, L, Schloss, JA, Bonazzi, V, McEwen, JE, Wetterstrand, KA, Deal, C, Baker, CC, Di Francesco, V, Howcroft, TK, Karp, RW, Lunsford, RD, Wellington, CR, Belachew, T, Wright, M, Giblin, C, David, H, Mills, M, Salomon, R, Mullins, C, Akolkar, B, Begg, L, Davis, C, Grandison, L, Humble, M, Khalsa, J, Little, AR, Peavy, H, Pontzer, C, Portnoy, M, Sayre, MH, Starke-Reed, P, Zakhari, S, Read, J, Watson, B and Guyer, M (2009). The NIH Human Microbiome Project. Genome Research 19: 2317–2323.Google Scholar
Phillips, I, Casewell, M, Cox, T, De Groot, B, Friis, C, Jones, R, Nightingale, C, Preston, R and Waddell, J (2004). Does the use of antibiotics in food animals pose a risk to human health? A critical review of published data. Journal of Antimicrobial Chemotherapy 53: 28–52.CrossRefGoogle Scholar
Pieper, R, Janczyk, P, Urubschurov, V, Korn, U, Pieper, B and Souffrant, WB (2009). Effect of a single oral administration of Lactobacillus plantarum DSMZ 8862/8866 before and at the time point of weaning on intestinal microbial communities in piglets. International Journal of Food Microbiology 130: 227–232.Google Scholar
Pryde, SE, Richardson, AJ, Stewart, CS and Flint, HJ (1999). Molecular analysis of the microbial diversity present in the colonic wall, colonic lumen, and cecal lumen of a pig. Applied and Environmental Microbiology 65: 5372–5377.Google Scholar
Qin, J, Li, R, Raes, J, Arumugam, M, Burgdorf, KS, Manichanh, C, Nielsen, T, Pons, N, Levenez, F, Yamada, T, Mende, DR, Li, J, Xu, J, Li, S, Li, D, Cao, J, Wang, B, Liang, H, Zheng, H, Xie, Y, Tap, J, Lepage, P, Bertalan, M, Batto, JM, Hansen, T, Le Paslier, D, Linneberg, A, Nielsen, HB, Pelletier, E, Renault, P, Sicheritz-Ponten, T, Turner, K, Zhu, H, Yu, C, Li, S, Jian, M, Zhou, Y, Li, Y, Zhang, X, Li, S, Qin, N, Yang, H, Wang, J, Brunak, S, Doré, J, Guarner, F, Kristiansen, K, Pedersen, O, Parkhill, J, Weissenbach, J; MetaHIT Consortium, Bork, P, Ehrlich, SD and Wang, J (2010). A human gut microbial gene catalogue established by metagenomic sequencing. Nature 464: 59–65.Google Scholar
Rakoff-Nahoum, S, Paglino, J, Eslami-Varzaneh, F, Edberg, S and Medzhitov, R (2004). Recognition of commensal microflora by toll-like receptors is required for intestinal homeostasis. Cell 118: 229–241.CrossRefGoogle ScholarPubMed
Ramotar, K, Conly, JM, Chubb, H and Louie, TJ (1984). Production of menaquinones by intestinal anaerobes. Journal of Infectious Diseases 150: 213–218.Google Scholar
Rettedal, E, Vilain, S, Lindblom, S, Lehnert, K, Scofield, C, George, S, Clay, S, Kaushik, RS, Rosa, AJ, Francis, D and Brözel, VS (2009). Alteration of the ileal microbiota of weanling piglets by the growth-promoting antibiotic chlortetracycline. Applied and Environmental Microbiology 75: 5489–5495.Google Scholar
Robinson, IM, Allison, MJ and Bucklin, JA (1981). Characterization of the cecal bacteria of normal pigs. Applied and Environmental Microbiology 41: 950–955.Google Scholar
Robinson, IM, Whipp, SC, Bucklin, JA and Allison, MJ (1984). Characterization of predominant bacteria from the colons of normal and dysenteric pigs. Applied and Environmental Microbiology 48: 964–969.Google Scholar
Roediger, WE (1980). Role of anaerobic bacteria in the metabolic welfare of the colonic mucosa in man. Gut 21: 793–798.CrossRefGoogle ScholarPubMed
Russell, EG (1979). Types and distribution of anaerobic bacteria in the large intestine of pigs. Applied and Environmental Microbiology 37: 187–193.CrossRefGoogle ScholarPubMed
Savage, DC (1977). Microbial ecology of the gastrointestinal tract. Annual Reviews in Microbiology 31: 107–133.Google Scholar
Schloss, PD and Handelsman, J (2005). Introducing DOTUR, a computer program for defining operational taxonomic units and estimating species richness. Applied and Environmental Microbiology 71: 1501–1506.CrossRefGoogle ScholarPubMed
Schuster, SC (2008). Next-generation sequencing transforms today's biology. Nature Methods 5: 16–18.CrossRefGoogle ScholarPubMed
Sellon, RK, Tonkonogy, S, Schultz, M, Dieleman, LA, Grenther, W, Balish, E, Rennick, DM and Sartor, RB (1998). Resident enteric bacteria are necessary for development of spontaneous colitis and immune system activation in interleukin-10-deficient mice. Infection and Immunity 66: 5224–5231.CrossRefGoogle ScholarPubMed
Shan, T, Li, L, Simmonds, P, Wang, C, Moeser, A and Delwart, E (2011). The fecal virome of pigs on a high-density farm. Journal of Virology 85: 11697–11708.CrossRefGoogle ScholarPubMed
Shimada, K, Bricknell, KS and Finegold, SM (1969). Deconjugation of bile acids by intestinal bacteria: review of literature and additional studies. Journal of Infectious Diseases 119: 273–281.CrossRefGoogle ScholarPubMed
Simpson, JM, Kocherginskaya, S, Aminov, RI, Skerlos, LT, Bradley, TM, Mackie, RI and White, BA (2002). Comparative microbial diversity in the gastrointestinal tracts of food animal species. Integrative and Comparative Biology 42: 327–331.Google Scholar
Simpson, JM, McCracken, VJ, White, BA, Gaskins, HR and Mackie, RI (1999). Application of denaturant gradient gel electrophoresis for the analysis of the porcine gastrointestinal microbiota. Journal of Microbiological Methods 36: 167.CrossRefGoogle ScholarPubMed
Turnbaugh, PJ and Gordon, JI (2008). An invitation to the marriage of metagenomics and metabolomics. Cell 134: 708–713.Google Scholar
Urubschurov, V, Janczyk, P, Souffrant, WB, Freyer, G and Zeyner, A (2011). Establishment of intestinal microbiota with focus on yeasts of unweaned and weaned piglets kept under different farm conditions. FEMS Microbiology Ecology 77: 493–502.Google Scholar
Vahjen, W, Pieper, R and Zentek, J (2010). Bar-coded pyrosequencing of 16S rRNA gene amplicons reveals changes in ileal porcine bacterial communities due to high dietary zinc intake. Applied and Environmental Microbiology 76: 6689–6691.Google Scholar
Varel, VH, Robinson, IM and Jung, HJ (1987). Influence of dietary fiber on xylanolytic and cellulolytic bacteria of adult pigs. Applied and Environmental Microbiology 53: 22–26.Google Scholar
Woese, CR and Fox, GE (1977). Phylogenetic structure of the prokaryotic domain: the primary kingdoms. Proceedings of the National Academy of Sciences, USA 74: 5088–5090.Google Scholar
Yolton, D and Savage, DC (1976). Influence of certain indigenous gastrointestinal microorganisms on duodenal alkaline phosphatase of mice. Applied and Environmental Microbiology 31: 880–888.Google Scholar
Zhu, WY, Williams, BA, Konstantinov, SR, Tamminga, S, De Vos, WM and Akkermans, AD (2003). Analysis of 16S rDNA reveals bacterial shift during in vitro fermentation of fermentable carbohydrate using piglet faeces as inoculum. Anaerobe 9: 175–180.Google Scholar