Phylogenetic and functional alterations in bacterial community compositions in broiler ceca as a result of mannan oligosaccharide supplementation

Applied and Environmental Microbiology

Volumn 81, Issue 10, 2015, Pages 3460-3470

  Corrigan, A ^a   De Leeuw, Marcel ^b   Penaud Frézet, Stéphanie ^c   Dimova, Diliana ^c   Murphya, R A ^a  

^a ALLTECH INC   (United States)

^b GeneCreek   (France)

^c BECKMAN COULTER INC   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

BACTERIA; BACTERIOLOGY; OLIGOSACCHARIDES;

BACTERIAL COMMUNITY; BACTERIAL COMMUNITY COMPOSITION; BACTERIAL COMMUNITY STRUCTURE; COMMERCIAL PRODUCTIONS; DIETARY SUPPLEMENTATION; FUNCTION PREDICTION; FUNCTIONAL CAPABILITIES; PROTEOBACTERIA;

DIETARY SUPPLEMENTS;

COMMERCIAL SPECIES; COMMUNITY COMPOSITION; DIET; FUNCTIONAL CHANGE; HATCHERY; MICROBIAL COMMUNITY; NUCLEIC ACID ANALYSIS; PHYLOGENETICS; POLYMER; POULTRY;

ACTINOBACTERIA; AVES; BACTERIA (MICROORGANISMS); BACTEROIDETES; FIRMICUTES; MOLLICUTES; PROTEOBACTERIA;

MANNAN; OLIGOSACCHARIDE; PREBIOTIC AGENT;

ANALYSIS; ANIMAL; ANIMAL FOOD; BACTERIUM; BIODIVERSITY; CECUM; CHICKEN; CLASSIFICATION; DIETARY SUPPLEMENT; FEMALE; GENETICS; ISOLATION AND PURIFICATION; MALE; METABOLISM; MICROBIOLOGY; PHYLOGENY; UTILIZATION;

ANIMAL FEED; ANIMALS; BACTERIA; BIODIVERSITY; CECUM; CHICKENS; DIETARY SUPPLEMENTS; FEMALE; MALE; MANNANS; OLIGOSACCHARIDES; PHYLOGENY; PREBIOTICS;

EID: 84930035045     PISSN: 00992240     EISSN: 10985336     Source Type: Journal    
DOI: 10.1128/AEM.04194-14     Document Type: Article

References (62)

1. Yeoman CJ, White BA. 2014. Gastrointestinal tract microbiota and probiotics in production animals. Annu Rev Anim Biosci 2:469-486. http://dx.doi.org/10.1146/annurev-animal-022513-114149.
2. Sugiharto S. 12 June 2014. Role of nutraceuticals in gut health and growth performance of poultry. J Saudi Soc Agric Sci doi:http://dx.doi.org/10.1016/j.jssas.2014.06.001.
3. Rinttilä T, Apajalahti J. 2013. Intestinal microbiota and metabolites-implications for broiler chicken health and performance. J Appl Poult Res 22:647-658. http://dx.doi.org/10.3382/japr.2013-00742.
4. Yegani M, Korver DR. 2008. Factors affecting intestinal health in poultry. Poult Sci 87:2052-2063. http://dx.doi.org/10.3382/ps.2008-00091.
5. Mead G, Lammerding AM, Cox N, Doyle MP, Humbert F, Kulikovskiy A, Panin A, do Nascimento VP, Wierup M. 2010. Scientific and technical factors affecting the setting of Salmonella criteria for raw poultry: a global perspective. J Food Prot 73:1566-1590.
6. Marshall BM, Levy SB. 2011. Food animals and antimicrobials: impacts on human health. Clin Microbiol Rev 24:718-733. http://dx.doi.org/10.1128/CMR.00002-11.
7. Maron DF, Smith TJS, Nachman KE. 2013. Restrictions on antimicrobial use in food animal production: an international regulatory and economic survey. Globalization and Health 9:48-48. http://dx.doi.org/10.1186/1744-8603-9-48.
8. Sofos JN. 2008. Challenges to meat safety in the 21st century. Meat Sci 78:3-13. http://dx.doi.org/10.1016/j.meatsci.2007.07.027.
9. Yang Y, Iji PA, Choct M. 2009. Dietary modulation of gut microflora in broiler chickens: a review of the role of six kinds of alternatives to in-feed antibiotics. World Poult Sci J 65:97-114. http://dx.doi.org/10.1017/S0043933909000087.
10. Spring P, Wenk C, Dawson KA, Newman KE. 2000. The effects of dietary mannaoligosaccharides on cecal parameters and the concentrations of enteric bacteria in the ceca of salmonella-challenged broiler chicks. Poult Sci 79:205-211. http://dx.doi.org/10.1093/ps/79.2.205.
11. Connolly DM, Ha A. 2011. Meta-analysis summary of broiler chicken trials with dietary actigen (2009 -2011). Int J Poul Sci 10:819-824. http://dx.doi.org/10.3923/ijps.2011.819.824.
12. Langille MGI, Zaneveld J, Caporaso JG, McDonald D, Knights D, Reyes JA, Clemente JC, Burkepile DE, Vega Thurber RL, Knight R, Beiko RG, Huttenhower C. 2013. Predictive functional profiling of microbial communities using 16S rRNA marker gene sequences. Nat Biotechnol 31:814-821. http://dx.doi.org/10.1038/nbt.2676.
13. Corrigan A, Horgan K, Clipson N, Murphy RA. 2011. Effect of dietary supplementation with a Saccharomyces cerevisiae mannan oligosaccharide on the bacterial community structure of broiler cecal contents. Appl Environ Microbiol 77:6653-6662. http://dx.doi.org/10.1128/AEM.05028-11.
14. Mitra S, Stark M, Huson DH. 2011. Analysis of 16S rRNA environmental sequences using MEGAN. BMC Genomics 12(Suppl 3):S17. http://dx.doi .org/10.1186/1471-2164-12-S3-S17.
15. Chen J, Bittinger K, Charlson ES, Hoffmann C, Lewis J, Wu GD, Collman RG, Bushman FD, Li H. 2012. Associating microbiome composition with environmental covariates using generalized UniFrac distances. Bioinformatics 28:2106-2113. http://dx.doi.org/10.1093/bioinformatics/bts342.
16. McDonald D, Price MN, Goodrich J, Nawrocki EP, DeSantis TZ, Probst A, Andersen GL, Knight R, Hugenholtz P. 2012. An improved Greengenes taxonomy with explicit ranks for ecological and evolutionary analyses of bacteria and archaea. ISME J 6:610-618. http://dx.doi.org/10.1038/ismej.2011.139.
17. Caporaso JG, Kuczynski J, Stombaugh J, Bittinger K, Bushman FD, Costello EK, Fierer N, Pena AG, Goodrich JK, Gordon JI, Huttley GA, Kelley ST, Knights D, Koenig JE, Ley RE, Lozupone CA, McDonald D, Muegge BD, Pirrung M, Reeder J, Sevinsky JR, Turnbaugh PJ, Walters WA, Widmann J, Yatsunenko T, Zaneveld J, Knight R. 2010. QIIME allows analysis of high-throughput community sequencing data. Nat Methods 7:335-336. http://dx.doi.org/10.1038/nmeth.f.303.
18. Kanehisa M, Goto S, Sato Y, Kawashima M, Furumichi M, Tanabe M. 2014. Data, information, knowledge and principle: back to metabolism in KEGG. Nucleic Acids Res 42:D199-D205. http://dx.doi.org/10.1093/nar /gkt1076.
19. Kanehisa M, Goto S, Sato Y, Furumichi M, Tanabe M. 2012. KEGG for integration and interpretation of large-scale molecular data sets. Nucleic Acids Res 40:D109-D114. http://dx.doi.org/10.1093/nar/gkr988.
20. Aggrey S, Karnuah A, Sebastian B, Anthony N. 2010. Genetic properties of feed efficiency parameters in meat-type chickens. Genet Sel Evol 42:25. http://dx.doi.org/10.1186/1297-9686-42-25.
21. Lu J, Idris U, Harmon B, Hofacre C, Maurer JJ, Lee MD. 2003. Diversity and succession of the intestinal bacterial community of the maturing broiler chicken. Appl Environ Microbiol 69:6816-6824. http://dx.doi.org /10.1128/AEM.69.11.6816-6824.2003.
22. Torok VA, Hughes RJ, Ophel-Keller K, Ali M, MacAlpine R. 2009. Influence of different litter materials on cecal microbiota colonization in broiler chickens. Poult Sci 88:2474-2481. http://dx.doi.org/10.3382/ps .2008-00381.
23. Torok VA, Ophel-Keller K, Loo M, Hughes RJ. 2008. Application of methods for identifying broiler chicken gut bacterial species linked with increased energy metabolism. Appl Environ Microbiol 74:783-791. http://dx.doi.org/10.1128/AEM.01384-07.
24. Danzeisen JL, Kim HB, Isaacson RE, Tu ZJ, Johnson TJ. 2011. Modulations of the chicken cecal microbiome and metagenome in response to anticoccidial and growth promoter treatment. PLoS One 6:e27949. http://dx.doi.org/10.1371/journal.pone.0027949.
25. Sergeant MJ, Constantinidou C, Cogan TA, Bedford MR, Penn CW, Pallen MJ. 2014. Extensive microbial and functional diversity within the chicken cecal microbiome. PLoS One 9:e91941. http://dx.doi.org/10.1371/journal.pone.0091941.
26. Singh KM, Shah T, Deshpande S, Jakhesara SJ, Koringa PG, Rank DN, Joshi CG. 2012. High throughput 16S rRNA gene-based pyrosequencing analysis of the fecal microbiota of highFCRand lowFCRbroiler growers. Mol Biol Rep 39:10595-10602. http://dx.doi.org/10.1007/s11033-012-1947-7.
27. Stanley D, Geier MS, Hughes RJ, Denman SE, Moore RJ. 2013. Highly variable microbiota development in the chicken gastrointestinal tract. PLoS One 8:e84290. http://dx.doi.org/10.1371/journal.pone.0084290.
28. Singh KM, Shah TM, Reddy B, Deshpande S, Rank DN, Joshi CG. 2014. Taxonomic and gene-centric metagenomics of the fecal microbiome of low and high feed conversion ratio (FCR) broilers. J Appl Genet 55:145-154. http://dx.doi.org/10.1007/s13353-013-0179-4.
29. Torok VA, Allison GE, Percy NJ, Ophel-Keller K, Hughes RJ. 2011. Influence of antimicrobial feed additives on broiler commensal posthatch gut microbiota development and performance. Appl Environ Microbiol 77:3380-3390. http://dx.doi.org/10.1128/AEM.02300-10.
30. Vaahtovuo J, Toivanen P, Eerola E. 2001. Study of murine faecal microflora by cellular fatty acid analysis; effect of age and mouse strain. Antonie Van Leeuwenhoek 80:35-42. http://dx.doi.org/10.1023/A:1012058107731.
31. La Rosa PS, Warner BB, Zhou Y, Weinstock GM, Sodergren E, Hall-Moore CM, Stevens HJ, Bennett WE, Jr, Shaikh N, Linneman LA, Hoffmann JA, Hamvas A, Deych E, Shands BA, Shannon WD, Tarr PI. 2014. Patterned progression of bacterial populations in the premature infant gut. Proc Natl Acad Sci U S A 111:12522-12527. http://dx.doi.org /10.1073/pnas.1409497111.
32. Macfarlane GT, Macfarlane LE. 2009. Acquisition, evolution and maintenance of the normal gut microbiota. Dig Dis 27(Suppl 1):90-98. http://dx.doi.org/10.1159/000268127.
33. van Dongen WF, White J, Brandl H, Moodley Y, Merkling T, Leclaire S, Blanchard P, Danchin E, Hatch S, Wagner R. 2013. Age-related differences in the cloacal microbiota of a wild bird species. BMC Ecol 13:11. http://dx.doi.org/10.1186/1472-6785-13-11.
34. Corrigan A, Horgan K, Clipson N, Murphy RA. 2012. Effect of dietary prebiotic (mannan oligosaccharide) supplementation on the caecal bacterial community structure of turkeys. Microb Ecol 64:826-836. http://dx .doi.org/10.1007/s00248-012-0046-6.
35. Waite D, Taylor M. 2014. Characterising the avian gut microbiota: membership, driving influences, and potential function. Front Microbiol 5:223. http://dx.doi.org/10.3389/fmicb.2014.00223.
36. Wei S, Morrison M, Yu Z. 2013. Bacterial census of poultry intestinal microbiome. Poult Sci 92:671-683. http://dx.doi.org/10.3382/ps.2012-02822.
37. Phillips ML. 2009. Gut reaction: environmental effects on the human microbiota. Environ Health Perspect 117:A198-A205. http://dx.doi.org /10.1289/ehp.117-a198.
38. Wexler HM. 2007. Bacteroides: the good, the bad, and the nitty-gritty. Clin Microbiol Rev 20:593-621. http://dx.doi.org/10.1128/CMR.00008-07.
39. Tu Q, He Z, Li Y, Chen Y, Deng Y, Lin L, Hemme CL, Yuan T, Van Nostrand JD, Wu L, Zhou X, Shi W, Li L, Xu J, Zhou J. 2014. Development of HuMiChip for functional profiling of human microbiomes. PLoS One 9:e90546. http://dx.doi.org/10.1371/journal.pone.0090546.
40. Kotzampassi K, Giamarellos-Bourboulis EJ, Stavrou G. 2014. Obesity as a consequence of gut bacteria and diet interactions. ISRN Obes 2014:651895. http://dx.doi.org/10.1155/2014/651895.
41. Ley RE, Bäckhed F, Turnbaugh P, Lozupone CA, Knight RD, Gordon JI. 2005. Obesity alters gut microbial ecology. Proc Natl Acad Sci U S A 102:11070-11075. http://dx.doi.org/10.1073/pnas.0504978102.
42. Murphy EF, Cotter PD, Healy S, Marques TM, O'Sullivan O, Fouhy F, Clarke SF, O'Toole PW, Quigley EM, Stanton C, Ross PR, O'Doherty RM, Shanahan F. 2010. Composition and energy harvesting capacity of the gut microbiota: relationship to diet, obesity and time in mouse models. Gut 59:1635-1642. http://dx.doi.org/10.1136/gut.2010.215665.
43. Turnbaugh PJ, Ley RE, Mahowald MA, Magrini V, Mardis ER, Gordon JI. 2006. An obesity-associated gut microbiome with increased capacity for energy harvest. Nature 444:1027-1031. http://dx.doi.org/10.1038/nature05414.
44. Tremaroli V, Backhed F. 2012. Functional interactions between the gut microbiota and host metabolism. Nature 489:242-249. http://dx.doi.org /10.1038/nature11552.
45. Henderson B, Pockley AG. 2010. Molecular chaperones and proteinfolding catalysts as intercellular signaling regulators in immunity and inflammation. J Leukoc Biol 88:445-462. http://dx.doi.org/10.1189/jlb .1209779.
46. Xiao R, Power RF, Mallonee D, Routt K, Spangler L, Pescatore AJ, Cantor AH, Ao T, Pierce JL, Dawson KA. 2012. Effects of yeast cell wall-derived mannan-oligosaccharides on jejunal gene expression in young broiler chickens. Poult Sci 91:1660-1669. http://dx.doi.org/10.3382/ps.2011-02035.
47. Che TM, Johnson RW, Kelley KW, Van Alstine WG, Dawson KA, Moran CA, Pettigrew JE. 2011. Mannan oligosaccharide modulates gene expression profile in pigs experimentally infected with porcine reproductive and respiratory syndrome virus. J Anim Sci 89:3016-3029. http://dx .doi.org/10.2527/jas.2010-3366.
48. Baurhoo B, Ferket P, Ashwell CM, de Oliviera J, Zhao X. 2012. Cell walls of Saccharomyces cerevisiae differentially modulated innate immunity and glucose metabolism during late systemic inflammation. PLoS One 7:e30323. http://dx.doi.org/10.1371/journal.pone.0030323.
49. Kogut MH. 2013. The gut microbiota and host innate immunity: regulators of host metabolism and metabolic diseases in poultry? J Appl Poult Res 22:637-646. http://dx.doi.org/10.3382/japr.2013-00741.
50. Lea H, Spring P, Taylor-Pickard J, Burton E. 2012. A natural carbohydrate fraction Actigen from Saccharomyces cerevisiae cell wall: effects on goblet cells, gut morphology and performance of broiler chickens. J Appl Anim Nutr 1:e9. http://dx.doi.org/10.1017/jan.2013.6.
51. Janardhana V, Broadway MM, Bruce MP, Lowenthal JW, Geier MS, Hughes RJ, Bean AGD. 2009. Prebiotics modulate immune responses in the gut-associated lymphoid tissue of chickens. J Nutr 139:1404-1409. http://dx.doi.org/10.3945/jn.109.105007.
52. Svihus B, Choct M, Classen HL. 2013. Function and nutritional roles of the avian caeca: a review. World Poult Sci J 69:249-264. http://dx.doi.org /10.1017/S0043933913000287.
53. Sun Y, O'Riordan MXD. 2013. Regulation of bacterial pathogenesis by intestinal short-chain fatty acids. Adv Appl Microbiol 85:93-118. http://dx.doi.org/10.1016/B978-0-12-407672-3.00003-4.
54. Miller TL, Wolin MJ. 1996. Pathways of acetate, propionate, and butyrate formation by the human fecal microbial flora. Appl Environ Microbiol 62:1589-1592.
55. den Besten G, van Eunen K, Groen AK, Venema K, Reijngoud D-J, Bakker BM. 2013. The role of short-chain fatty acids in the interplay between diet, gut microbiota and host energy metabolism. J Lipid Res 54:2325-2340. http://dx.doi.org/10.1194/jlr.R036012.
56. Paredes CJ, Alsaker KV, Papoutsakis ET. 2005. A comparative genomic view of clostridial sporulation and physiology. Nat Rev Microbiol 3:969-978. http://dx.doi.org/10.1038/nrmicro1288.
57. Veening J-W, Murray H, Errington J. 2009. A mechanism for cell cycle regulation of sporulation initiation in Bacillus subtilis. Genes Dev 23:1959-1970. http://dx.doi.org/10.1101/gad.528209.
58. Sauer U, Santangelo JD, Treuner A, Buchholz M, Dürre P. 1995. Sigma factor and sporulation genes in Clostridium. FEMS Microbiol Rev 17:331-340. http://dx.doi.org/10.1111/j.1574-6976.1995.tb00216.x.
59. Davidson AL, Dassa E, Orelle C, Chen J. 2008. Structure, function, and evolution of bacterial ATP-binding cassette systems. Microbiol Mol Biol Rev 72:317-364. http://dx.doi.org/10.1128/MMBR.00031-07.
60. Rees DC, Johnson E, Lewinson O. 2009. ABC transporters: the power to change. Nat Rev Mol Cell Biol 10:218-227. http://dx.doi.org/10.1038/nrm2646.
61. Vallès Y, Artacho A, Pascual-García A, Ferrús ML, Gosalbes MJ, Abellán JJ, Francino MP. 2014. Microbial succession in the gut: directional trends of taxonomic and functional change in a birth cohort of Spanish infants. PLoS Genet 10:e1004406. http://dx.doi.org/10.1371/journal.pgen .1004406.
62. Turnbaugh PJ, Hamady M, Yatsunenko T, Cantarel BL, Duncan A, Ley RE, Sogin ML, Jones WJ, Roe BA, Affourtit JP, Egholm M, Henrissat B, Heath AC, Knight R, Gordon JI. 2009. A core gut microbiome in obese and lean twins. Nature 457:480 - 484. http://dx .doi.org/10.1038/nature07540.