After ban of antibiotics growth promoters (AGP) in Europe in 2006, use of non-medicated gut microbiota regulators as feed additives has dramatically increased. This study aimed at describing the effects of a copper-exchanged zeolite on broiler growth performance, small intestine morphology and microbiota composition. Illumina Sequencing of the V3-V4 region of the 16S rRNA gene was employed to study the small intestine microbiota. This microbiota with copper-exchanged zeolite treated-chickens was significantly less diverse with an almost exclusive presence of Lactobacillus johnsonii and Lactobacillus reuteri. These Lactobacilli are correlated with increased diameter, length and weight of the three segments of the small intestine and decreased viscosity of the intestinal content, suggesting probiotic action. The tested copper-exchanged zeolite would act as a prebiotic, selecting a “favorable” flora for the healthy broilers development.
Hooper, L.V., Midtvedt, T. and Gordon, J.I. (2002) How Host-Microbial Interactions Shape the Nutrient Environment of the Mammalian Intestine. Annual Review of Nutrition, 22, 283-307. https://doi.org/10.1146/annurev.nutr.22.011602.092259
Waite, D.W. and Taylor, M.W. (2015) Exploring the Avian Gut Microbiota: Current Trends and Future Directions. Frontiers in Microbiology, 6, 673. https://doi.org/10.3389/fmicb.2015.00673
Jukes, T.H. and Williams, W.L. (1953) Nutritional Effects of Antibiotics. Pharmacological Reviews, 5, 381-420.
Coates, M.E., Fuller, R., Harrison, G.F., Lev, M. and Suffolk, S.F. (1963) A Comparison of the Growth of Chicks in the Gustafsson Germ-Free Apparatus and in a Conventional Environment, with and without Dietary Supplements of Penicillin. British Journal of Nutrition, 17, 141-150. https://doi.org/10.1079/BJN19630015
Gaskins, H.R., Collier, C.T. and Anderson, D.B. (2002) Antibiotics as Growth Promotants: Mode of Action. Animal Biotechnology, 13, 29-42. https://doi.org/10.1081/ABIO-120005768
Niewold, T.A. (2007) The Nonantibiotic Anti-Inflammatory Effect of Antimicrobial Growth Promoters, the Real Mode of Action? A Hypothesis. Poultry Science, 86, 605-609. https://doi.org/10.1093/ps/86.4.605
Samanidou, V.F. and Evaggelopoulou, E.N. (2008) Chromatographic Analysis of Banned Antibacterial Growth Promoters in Animal Feed. Journal of Separation Science, 31, 2091-2112. https://doi.org/10.1002/jssc.200800075
Mai, V. and Morris, J.G.J. (2004) Colonic Bacterial Flora: Changing Understandings in the Molecular Age. Journal of Nutrition, 134, 459-464.
Stokstad, E.L., Jukes, T.H., et al. (1949) The Multiple Nature of the Animal Protein Factor. The Journal of Biological Chemistry, 180, 647-654.
Libby, D.A. and Schaible, P.J. (1955) Observations on Growth Responses to Antibiotics and Arsonic Acids in Poultry Feeds. Science, 121, 733-734.
Gustafson, R.H. and Bowen, R.E. (1997) Antibiotic Use in Animal Agriculture. Journal of Applied Microbiology, 83, 531-541. https://doi.org/10.1046/j.1365-2672.1997.00280.x
Johnston, A.M. (2001) Animals and Antibiotics. International Journal of Antimicrobial Agents, 18, 291-294. https://doi.org/10.1016/S0924-8579(01)00379-X
Barton, M.D. (2000) Antibiotic Use in Animal Feed and Its Impact on Human Healt. Nutrition Research Reviews, 13, 279-299. https://doi.org/10.1079/095442200108729106
Hinton, M., Kaukas, A., Lim, S.K. and Linton, A.H. (1986) Preliminary Observations on the Influence of Antibiotics on the Ecology of Escherichia Coli and the Enterococci in the Faecal Flora of Healthy Young Chickens. Journal of Antimicrobial Chemotherapy, 18, 165-173.
Hinton, M., Kaukas, A. and Linton, A.H. (1986) The Ecology of Drug Resistance in Enteric Bacteria. Society for Applied Bacteriology Symposium Series, 15, 77S-92S.
Diarra, M.S. and Malouin, F. (2014) Antibiotics in Canadian Poultry Productions and Anticipated Alternatives. Frontiers in Microbiology, 5, 282. https://doi.org/10.3389/fmicb.2014.00282
Smith, J.M. (2014) A Review of Avian Probiotics. Journal of Avian Medicine and Surgery, 28, 87-94. https://doi.org/10.1647/2012-031
Patterson, J.A. and Burkholder, K.M. (2003) Application of Prebiotics and Probiotics in Poultry Production. Poultry Science, 82, 627-631. https://doi.org/10.1093/ps/82.4.627
Ricke, S.C. (2015) Potential of Fructooligosaccharide Prebiotics in Alternative and Nonconventional Poultry Production Systems. Poultry Science, 94, 1411-1418. https://doi.org/10.3382/ps/pev049
Michalak, I., Chojnacka, K., Dobrzanski, Z., Gorecki, H., Zielinska, A., Korczynski, M. and Opalinski, S. (2011) Effect of Macroalgae Enriched with Microelements on Egg Quality Parameters and Mineral Content of Eggs, Eggshell, Blood, Feathers and Droppings. Journal of Animal Physiology and Animal Nutrition, 95, 374-387. https://doi.org/10.1111/j.1439-0396.2010.01065.x
Gheisari, A.A., Sanei, A., Samie, A., Gheisari, M.M. and Toghyani, M. (2011) Effect of Diets Supplemented with Different Levels of Manganese, Zinc, and Copper from Their Organic or Inorganic Sources on Egg Production and Quality Characteristics in Laying Hens. Biological Trace Element Research, 142, 557-571. https://doi.org/10.1007/s12011-010-8779-x
Sornlake, W., Matetaviparee, P., Rattanaphan, N., Tanapongpipat, S. and Eurwilaichitr, L. (2013) Beta-Mannanase Production by Aspergillus niger BCC4525 and Its Efficacy on Broiler Performance. Journal of the Science of Food and Agriculture, 93, 3345-3351. https://doi.org/10.1002/jsfa.6183
Amerah, A.M., Mathis, G. and Hofacre, C.L. (2012) Effect of Xylanase and a Blend of Essential Oils on Performance and Salmonella Colonization of Broiler Chickens Challenged with Salmonella Heidelberg. Poultry Science, 91, 943-947. https://doi.org/10.3382/ps.2011-01922
Pirgozliev, V., Bravo, D., Mirza, M.W. and Rose, S.P. (2015) Growth Performance and Endogenous Losses of Broilers Fed Wheat-Based Diets with and without Essential Oils and Xylanase Supplementation. Poultry Science, 94, 1227-1232. https://doi.org/10.3382/ps/peu017
Bozkurt, M., Giannenas, I., Kucukyilmaz, K., Christaki, E. and Florou-Paneri, P. (2013) An Update on Approaches to Controlling Coccidia in Poultry Using Botanical Extracts. British Poultry Science, 54, 713-727. https://doi.org/10.1080/00071668.2013.849795
Wallace, R.J., Oleszek, W., Franz, C., Hahn, I., Baser, K.H., Mathe, A. and Teichmann, K. (2010) Dietary Plant Bioactives for Poultry Health and Productivity. British Poultry Science, 51, 461-487. https://doi.org/10.1080/00071668.2010.506908
Almeida, J.A., Ponnuraj, N.P., Lee, J.J., Utterback, P., Gaskins, H.R., Dilger, R.N. and Pettigrew, J.E. (2014) Effects of Dietary Clays on Performance and Intestinal Mucus Barrier of Broiler Chicks Challenged with Salmonella enterica Serovar Typhimurium and on Goblet Cell Function in Vitro. Poultry Science, 93, 839-847. https://doi.org/10.3382/ps.2013-03587
Magnoli, A.P., Texeira, M., Rosa, C.A., Miazzo, R.D., Cavaglieri, L.R., Magnoli, C.E., Dalcero, A.M. and Chiacchiera, S.M. (2011) Sodium Bentonite and Monensin under Chronic Aflatoxicosis in Broiler Chickens. Poultry Science, 90, 352-357. https://doi.org/10.3382/ps.2010-00834
Cabanero, A.I., Madrid, Y. and Camara, C. (2005) Effect of Animal Feed Enriched with Se and Clays on Hg Bioaccumulation in Chickens: In Vivo Experimental Study. Journal of Agricultural and Food Chemistry, 53, 2125-2132. https://doi.org/10.1021/jf048267v
Xia, M.S., Hu, C.H. and Xu, Z.R. (2004) Effects of Copper-Bearing Montmorillonite on Growth Performance, Digestive Enzyme Activities, and Intestinal Microflora and Morphology of Male Broilers. Poultry Science, 83, 1868-1875. https://doi.org/10.1093/ps/83.11.1868
Tang, Z.G., Wen, C., Wang, L.C., Wang, T. and Zhou, Y.M. (2014) Effects of Zinc-Bearing Clinoptilolite on Growth Performance, Cecal Microflora and Intestinal Mucosal Function of Broiler Chickens. Animal Feed Science and Technology, 189, 98-106. https://doi.org/10.1016/j.anifeedsci.2013.12.014
Song, J., Li, Y.L. and Hu, C.H. (2013) Effects of Copper-Exchanged Montmorillonite, as Alternative to Antibiotic, on Diarrhea, Intestinal Permeability and Proinflammatory Cytokine of Weanling Pigs. Applied Clay Science, 77-78, 52-55. https://doi.org/10.1016/j.clay.2013.01.016
Hasselbacher, P. (1976) Measuring Synovial Fluid Viscosity with a White Blood Cell Diluting Pipette. A Simple, Rapid, and Reproducible Method. Arthritis & Rheumatology, 19, 1358-1362. https://doi.org/10.1002/art.1780190620
Huse, S.M., Mark Welch, D.B., Voorhis, A., Shipunova, A., Morrison, H.G., Eren, A.M. and Sogin, M.L. (2014) VAMPS: A Website for Visualization and Analysis of Microbial Population Structures. BMC Bioinformatics, 15, 41. https://doi.org/10.1186/1471-2105-15-41
Meyer, F., Paarmann, D., D’Souza, M., Olson, R., Glass, E.M., Kubal, M., Paczian, T., Rodriguez, A., Stevens, R., Wilke, A., Wilkening, J. and Edwards, R.A. (2008) The Metagenomics RAST Server—A Public Resource for the Automatic Phylogenetic and Functional Analysis of Metagenomes. BMC Bioinformatics, 9, 386. https://doi.org/10.1186/1471-2105-9-386
Chao, A.L.S. (1992) Estimating the Number of Classes via Sample Coverage. Journal of the American Statistical Association, 87, 210-217. https://doi.org/10.1080/01621459.1992.10475194
Chao, A. (1984) Non-Parametric Estimation of the Number of Classes in a Population. Scandinavian Journal of Statistics, 11, 265-270.
Simpson, E.H. (1949) Measurement of Diversity. Nature, 163, 688. https://doi.org/10.1038/163688a0
Shannon, C.E. (1948) A Mathematical Theory of Communication. The Bell System Technical Journal, 27, 379-423, 623-656.
Lozupone, C.A., Hamady, M., Kelley, S.T. and Knight, R. (2007) Quantitative and Qualitative Beta Diversity Measures Lead to Different Insights into Factors That Structure Microbial Communities. Applied and Environmental Microbiology, 73, 1576-1585. https://doi.org/10.1128/AEM.01996-06
Vazquez-Baeza, Y., Pirrung, M., Gonzalez, A. and Knight, R. (2013) EMPeror: A Tool for Visualizing High-Throughput Microbial Community Data. Gigascience, 2, 16.
Quast, C., Pruesse, E., Yilmaz, P., Gerken, J., Schweer, T., Yarza, P., Peplies, J. and Glockner, F.O. (2013) The SILVA Ribosomal RNA Gene Database Project: Improved Data Processing and Web-Based Tools. Nucleic Acids Research, 41, D590-D596. https://doi.org/10.1093/nar/gks1219
Cole, J.R., Chai, B., Farris, R.J., Wang, Q., Kulam-Syed-Mohideen, A.S., McGarrell, D.M., Bandela, A.M., Cardenas, E., Garrity, G.M. and Tiedje, J.M. (2007) The Ribosomal Database Project (RDP-II): Introducing myRDP Space and Quality Controlled Public Data. Nucleic Acids Research, 35, D169-D172. https://doi.org/10.1093/nar/gkl889
DeSantis, T.Z., Hugenholtz, P., Larsen, N., Rojas, M., Brodie, E.L., Keller, K., Huber, T., Dalevi, D., Hu, P. and Andersen, G.L. (2006) Greengenes, a Chimera-Checked 16S rRNA Gene Database and Workbench Compatible with ARB. Applied and Environmental Microbiology, 72, 5069-5072. https://doi.org/10.1128/AEM.03006-05
Gao, X.Y., Zhi, X.Y., Li, H.W., Klenk, H.P. and Li, W.J. (2014) Comparative Genomics of the Bacterial Genus Streptococcus Illuminates Evolutionary Implications of Species Groups. PLoS ONE, 9, e101229. https://doi.org/10.1371/journal.pone.0101229
Yang, H.M., Wang W., Wang, Z.Y., Wang, J., Cao, Y.J. and Chen, Y.H. (2013) Comparative Study of Intestine Length, Weight and Digestibility on Different Body Weight Chickens. African Journal of Biotechnology, 12, 5097-5100. https://doi.org/10.5897/AJB11.4014
Jamroz, D. (2005) Comparative Characteristic of Gastrointestinal Tract Development and Digestibility of Nutrients in Young Chickens, Ducks and Geese. Proceedings of the 15th European Symposium on Poultry Nutrition, Balatonfüred, 25-29 September 2005, 74-85.
Bedford, M.R. and Schulze, H. (1998) Exogenous Enzymes for Pigs and Poultry. Nutrition Research Reviews, 11, 91-114. https://doi.org/10.1079/NRR19980007
Choct, M. and Annison, G. (1992) Anti-Nutritive Effect of Wheat Pentosans in Broiler Chickens: Roles of Viscosity and Gut Microflora. British Poultry Science, 33, 821-834. https://doi.org/10.1080/00071669208417524
Choct, M., Hughes, R.J. and Bedford, M.R. (1999) Effects of a Xylanase on Individual Bird Variation, Starch Digestion throughout the Intestine, and Ileal and Caecal Volatile Fatty Acid Production in Chickens Fed Wheat. British Poultry Science, 40, 419-422. https://doi.org/10.1080/00071669987548
Wang, Z.R., Qiao, S.Y., Lu, W.Q. and Li, D.F. (2005) Effects of Enzyme Supplementation on Performance, Nutrient Digestibility, Gastrointestinal Morphology, and Volatile Fatty Acid Profiles in the Hindgut of Broilers Fed Wheat-Based Diets. Poultry Science, 84, 875-881. https://doi.org/10.1093/ps/84.6.875
Ravindran, V., Selle, P.H. and Bryden, W.L. (1999) Effects of Phytase Supplementation, Individually and in Combination, with Glycanase, on the Nutritive Value of Wheat and Barley. Poultry Science, 78, 1588-1595. https://doi.org/10.1093/ps/78.11.1588
Petersen, S.T., Wiseman, J. and Bedford, M.R. (1999) Effects of Age and Diet on the Viscosity of Intestinal Contents in Broiler Chicks. British Poultry Science, 40, 364-370. https://doi.org/10.1080/00071669987467
Pourabedin, M., Guan, L. and Zhao, X. (2015) Xylo-Oligosaccharides and Virginiamycin Differentially Modulate Gut Microbial Composition in Chickens. Microbiome, 3, 15.
Wei, S., Morrison, M. and Yu, Z. (2013) Bacterial Census of Poultry Intestinal Microbiome. Poultry Science, 92, 671-683. https://doi.org/10.3382/ps.2012-02822
Nishiyama, K., Nakazato, A., Ueno, S., Seto, Y., Kakuda, T., Takai, S., Yamamoto, Y. and Mukai, T. (2015) Cell Surface-Associated Aggregation-Promoting Factor from Lactobacillus gasseri SBT2055 Facilitates Host Colonization and Competitive Exclusion of Campylobacter jejuni. Molecular Microbiology, 98, 712-726. https://doi.org/10.1111/mmi.13153
Garriga, M., Pascual, M., Monfort, J.M. and Hugas, M. (1998) Selection of Lactobacilli for Chicken Probiotic Adjuncts. Journal of Applied Microbiology, 84, 125-132. https://doi.org/10.1046/j.1365-2672.1997.00329.x
Ehrmann, M.A., Kurzak, P., Bauer, J. and Vogel, R.F. (2002) Characterization of Lactobacilli towards Their Use as Probiotic Adjuncts in Poultry. Journal of Applied Microbiology, 92, 966-975. https://doi.org/10.1046/j.1365-2672.2002.01608.x
Brisbin, J.T., Davidge, L., Roshdieh, A. and Sharif, S. (2015) Characterization of the Effects of Three Lactobacillus Species on the Function of Chicken Macrophages. Research in Veterinary Science, 100, 39-44. https://doi.org/10.1016/j.rvsc.2015.03.003
Brisbin, J.T., Gong, J., Orouji, S., Esufali, J., Mallick, A.I., Parvizi, P., Shewen, P.E. and Sharif, S. (2011) Oral Treatment of Chickens with Lactobacilli Influences Elicitation of Immune Responses. Clinical and Vaccine Immunology, 18, 1447-1455. https://doi.org/10.1128/CVI.05100-11
Montiel, R., Martin-Cabrejas, I., Langa, S., El Aouad, N., Arques, J.L., Reyes, F. and Medina, M. (2014) Antimicrobial Activity of Reuterin Produced by Lactobacillus reuteri on Listeria monocytogenes in Cold-Smoked Salmon. Food Microbiology, 44, 1-5. https://doi.org/10.1016/j.fm.2014.05.006
Pandey, N., Malik, R.K., Kaushik, J.K. and Singroha, G. (2013) Gassericin A: A Circular Bacteriocin Produced by Lactic Acid Bacteria Lactobacillus gasseri. World Journal of Microbiology and Biotechnology, 29, 1977-1987. https://doi.org/10.1007/s11274-013-1368-3
Abee, T., Klaenhammer, T.R. and Letellier, L. (1994) Kinetic Studies of the Action of Lactacin F, a Bacteriocin Produced by Lactobacillus Johnsonii That Forms Poration Complexes in the Cytoplasmic Membrane. Applied and Environmental Microbiology, 60, 1006-1013.
Karczewski, J., Troost, F.J., Konings, I., Dekker, J., Kleerebezem, M., Brummer, R.J. and Wells, J.M. (2010) Regulation of Human Epithelial Tight Junction Proteins by Lactobacillus Plantarum in Vivo and Protective Effects on the Epithelial Barrier. American Journal of Physiology—Gastrointestinal and Liver Physiology, 298, G851-G859. https://doi.org/10.1152/ajpgi.00327.2009
Gong, J., Si, W., Forster, R.J., Huang, R., Yu, H., Yin, Y., Yang, C. and Han, Y. (2007) 16S rRNA Gene-Based Analysis of Mucosa-Associated Bacterial Community and Phylogeny in the Chicken Gastrointestinal Tracts: From Crops to Ceca. FEMS Microbiology Ecology, 59, 147-157. https://doi.org/10.1111/j.1574-6941.2006.00193.x
Phillips, I. (1999) The Use of Bacitracin as a Growth Promoter in Animals Produces No Risk to Human Health. Journal of Antimicrobial Chemotherapy, 44, 725-728. https://doi.org/10.1093/jac/44.6.725
Fox, G.E., Wisotzkey, J.D. and Jurtshuk, P.J. (1992) How Close Is Close: 16S rRNA Sequence Identity May Not Be Sufficient to Guarantee Species Identity. International Journal of Systematic Bacteriology, 42, 166-170. https://doi.org/10.1099/00207713-42-1-166
Vancanneyt, M., Snauwaert, C., Cleenwerck, I., Baele, M., Descheemaeker, P., Goossens, H., Pot, B., Vandamme, P., Swings, J., Haesebrouck, F. and Devriese, L.A. (2001) Enterococcus villorum sp. nov., an Enteroadherent Bacterium Associated with Diarrhoea in Piglets. International Journal of Systematic and Evolutionary Microbiology, 51, 393-400. https://doi.org/10.1099/00207713-51-2-393
Teixeira, L.M., Carvalho, M.G., Espinola, M.M., Steigerwalt, A.G., Douglas, M.P., Brenner, D.J. and Facklam, R.R. (2001) Enterococcus porcinus sp. nov. and Enterococcus ratti sp. nov., Associated with Enteric Disorders in Animals. International Journal of Systematic and Evolutionary Microbiology, 51, 1737-1743. https://doi.org/10.1099/00207713-51-5-1737
Chadfield, M.S., Christensen, J.P., Juhl-Hansen, J., Christensen, H. and Bisgaard, M. (2005) Characterization of Enterococcus hirae Outbreaks in Broiler Flocks Demonstrating Increased Mortality Because of Septicemia and Endocarditis and/or Altered Production Parameters. Avian Diseases, 49, 16-23. https://doi.org/10.1637/7205-050604
Devriese, L.A., Hommez, J., Wijfels, R. and Haesebrouck, F. (1991) Composition of the Enterococcal and Streptococcal Intestinal Flora of Poultry. Journal of Applied Bacteriology, 1, 46-50.
Tremblay, C.L., Letellier, A., Quessy, S., Boulianne, M., Daignault, D. and Archambault, M. (2011) Multiple-Antibiotic Resistance of Enterococcus faecalis and Enterococcus faecium from Cecal Contents in Broiler Chicken and Turkey Flocks Slaughtered in Canada and Plasmid Colocalization of tetO and ermB Genes. Journal of Food Protection, 74, 1639-1648. https://doi.org/10.4315/0362-028X.JFP-10-451
Manson, J.M., Smith, J.M. and Cook, G.M. (2004) Persistence of Vancomycin-Resistant Enterococci in New Zealand Broilers after Discontinuation of Avoparcin Use. Applied and Environmental Microbiology, 70, 5764-5768. https://doi.org/10.1128/AEM.70.10.5764-5768.2004
Frei, A., Goldenberger, D. and Teuber, M. (2001) Antimicrobial Susceptibility of Intestinal Bacteria from Swiss Poultry Flocks before the Ban of Antimicrobial Growth Promoters. Systematic and Applied Microbiology, 24, 116-121. https://doi.org/10.1078/0723-2020-00004
Gong, J., Yu, H., Liu, T., Gill, J.J., Chambers, J.R., Wheatcroft, R. and Sabour, P.M. (2008) Effects of Zinc Bacitracin, Bird Age and Access to Range on Bacterial Microbiota in the Ileum and Caeca of Broiler Chickens. Journal of Applied Microbiology, 104, 1372-1382. https://doi.org/10.1111/j.1365-2672.2007.03699.x
Schlegel, L., Grimont, F., Ageron, E., Grimont, P.A. and Bouvet, A. (2003) Reappraisal of the Taxonomy of the Streptococcus bovis/Streptococcus equinus Complex and Related Species: Description of Streptococcus gallolyticus subsp. Gallolyticus subsp. nov., S. Gallolyticus subsp. Macedonicus subsp. nov. and S. Gallolyticus subsp. Pasteurianus subsp. nov. International Journal of Systematic and Evolutionary Microbiology, 53, 631-645. https://doi.org/10.1099/ijs.0.02361-0
Papadimitriou, K., Ferreira, S., Papandreou, N.C., Mavrogonatou, E., Supply, P., Pot, B. and Tsakalidou, E. (2012) Complete Genome Sequence of the Dairy Isolate Streptococcus macedonicus ACA-DC 198. Journal of Bacteriology, 194, 1838-1839. https://doi.org/10.1128/JB.06804-11
Punpanich, W., Munsrichoom, A. and Dejsirilert, S. (2012) Streptococcus gallolyticus Subspecies Pasteurianus meningitis in an Infant: A Case Report and Literature Review. Journal of the Medical Association of Thailand, 95, 1606-1612.
Jans, C., Follador, R., Hochstrasser, M., Lacroix, C., Meile, L. and Stevens, M.J. (2013) Comparative Genome Analysis of Streptococcus Infantarius Subsp. Infantarius CJ18, an African Fermented Camel Milk Isolate with Adaptations to Dairy Environment. BMC Genomics, 14, 200. https://doi.org/10.1186/1471-2164-14-200