Characterization of the Fecal Bacterial Microbiota of Healthy and Diarrheic Dairy Calves

Journal of Veterinary Internal Medicine

Volumn 31, Issue 3, 2017, Pages 928-939

  Gomez, D E ^a   Arroyo, L G ^a   Costa, M C ^b   Viel, L ^a   Weese, J S ^a  

^a UNIVERSITY OF GUELPH   (Canada)

^b UNIVERSITÉ DE MONTRÉAL   (Canada)

Author keywords

Bacterial species; Bifidobacterium; Epidemiology; Escherichia coli; Infectious diseases; LEfSe; Microbiology; PICRUSt

Indexed keywords

AMINO ACID; CHLOROPHYLL; PORPHYRIN; RNA 16S;

ACIDAMINOCOCCACEAE; ARTICLE; BACTERIAL FLORA; BIFIDOBACTERIUM; COLLINSELLA; CONTROLLED STUDY; DAIRY CATTLE; DIARRHEA; DIETZIA; DISCRIMINANT ANALYSIS; ENERGY METABOLISM; ESCHERICHIA; FAECALIBACTERIUM; FECES ANALYSIS; FECES MICROFLORA; GENE SEQUENCE; HIGH THROUGHPUT SEQUENCING; LACHNOSPIRACEAE; LACTOBACILLUS; METABOLISM; METAGENOMICS; MICROBIAL COMMUNITY; MORTALITY RATE; NONHUMAN; PEPTOSTREPTOCOCCUS; PHYLOGENY; POLYMERASE CHAIN REACTION; SEQUENCE ANALYSIS; ANIMAL; BOVINE; CASE CONTROL STUDY; CATTLE DISEASE; FECES; FEMALE; GENETICS; MICROBIOLOGY; MICROFLORA; VETERINARY;

ANIMALS; CASE-CONTROL STUDIES; CATTLE; CATTLE DISEASES; DIARRHEA; FECES; FEMALE; MICROBIOTA; RNA, RIBOSOMAL, 16S;

EID: 85017446973     PISSN: 08916640     EISSN: 19391676     Source Type: Journal    
DOI: 10.1111/jvim.14695     Document Type: Article

References (68)

1. USDA. Dairy 2007, Part I: Reference of Dairy Cattle Health and Management Practices in the United States. Fort Collins CO: USDA-APHIS-VS; 2007.
2. Cho Y-I, Han J-I, Wang C, et al. Case-control study of microbiological etiology associated with calf diarrhea. Vet Microbiol 2013;166:375–385.
3. Bäckhed F, Ley RE, Sonnenburg JL, et al. Host-bacterial mutualism in the human intestine. Science 2005;307:1915–1920.
4. Macpherson AJ, Harris NL. Interactions between commensal intestinal bacteria and the immune system. Nat Rev Immunol 2004;4:478–485.
5. Lei YM, Nair L, Alegre ML. The interplay between the intestinal microbiota and the immune system. Clin Res Hepatol Gastroenterol 2015;39:9–19.
6. Rakoff-Nahoum S, Paglino J, Eslami-Varzaneh F, et al. Recognition of commensal microflora by toll-like receptors is required for intestinal homeostasis. Cell 2004;118:229–241.
7. Warner BB, Deych E, Zhou Y, et al. Gut bacteria dysbiosis and necrotising enterocolitis in very low birthweight infants: A prospective case-control study. Lancet 2016;387:1928–1936.
8. Antharam VC, Li EC, Ishmael A, et al. Intestinal dysbiosis and depletion of butyrogenic bacteria in Clostridium difficile infection and nosocomial diarrhea. J Clin Microbiol 2013;51:2884–2892.
9. Stecher B, Robbiani R, Walker AW, et al. Salmonella enterica serovar typhimurium exploits inflammation to compete with the intestinal microbiota. PLoS Biol 2007;5:2177–2189.
10. Lupp C, Robertson ML, Wickham ME, et al. Host-mediated inflammation disrupts the intestinal microbiota and promotes the overgrowth of Enterobacteriaceae. Cell Host Microbe 2007;2:119–129.
11. van Nood E, Dijkgraaf MG, Keller JJ. Duodenal infusion of feces for recurrent Clostridium difficile. N Engl J Med 2013;368:2143–2145.
12. Oikonomou G, Teixeira AGV, Foditsch C, et al. Fecal microbial diversity in pre-weaned dairy calves as described by pyrosequencing of metagenomic 16S rDNA. Associations of Faecalibacterium species with health and growth. PLoS ONE 2013;8:e63157.
13. McGuirk SM. Disease management of dairy calves and heifers. Vet Clin North Am Food Anim Pract 2008;24:139–153.
14. Klindworth A, Pruesse E, Schweer T, et al. Evaluation of general 16S ribosomal RNA gene PCR primers for classical and next generation sequencing-based diversity studies. Nucleic Acids Res 2013;41:e1.
15. Slifierz MJ, Friendship RM, Weese JS. Longitudinal study of the early-life fecal and nasal microbiotas of the domestic pig. BMC Microbiol 2015;15:184–196.
16. Schloss PD, Westcott SL, Ryabin T, et al. Introducing mothur: Open-source, platform-independent, community-supported software for describing and comparing microbial communities. Appl Environ Microbiol 2009;75:7537–7541.
17. Quast C, Pruesse E, Yilmaz P, et al. The SILVA ribosomal RNA gene database project: Improved data processing and web-based tools. Nucleic Acids Res 2013;41:D590–D596.
18. Edgar RC, Haas BJ, Clemente JC, et al. UCHIME improves sensitivity and speed of chimera detection. Bioinformatics 2011;27:2194–2200.
19. Benjamini Y, Hochberg Y. Controlling the false discovery rate: A practical and powerful approach to multiple testing. J R Stat Soc Methodol 1995;57:289–300.
20. Langille M, Zaneveld J, Caporaso JG, et al. Predictive functional profiling of microbial communities using 16S rRNA marker gene sequences. Nat Biotechnol 2013;31:814–821.
21. DeSantis TZ, Hugenholtz P, Larsen N, et al. Greengenes, a chimera-checked 16S rRNA gene database and workbench compatible with ARB. Appl Environ Microbiol 2006;72:5069–5072.
22. Segata N, Izard J, Waldron L, et al. Metagenomic biomarker discovery and explanation. Genome Biol 2011;12:R60.
23. Li RW, Connor EE, Li C, et al. Characterization of the rumen microbiota of pre-ruminant calves using metagenomic tools. Environ Microbiol 2012;14:129–139.
24. Lukás F, Koppová I, Kudrna V, Kopecný J. Postnatal development of bacterial population in the gastrointestinal tract of calves. Folia Microbiol (Praha) 2007;52:99–104.
25. Smith HW. The development of the flora of the alimentary tract in young animals. J Pathol Bacteriol 1965;90:495–513.
26. Mylrea PJ. The bacterial content of the small intestine of young calves. Res Vet Sci 1969;10:394–395.
27. Klein-Jöbstl D, Schornsteiner E, Mann E, et al. Pyrosequencing reveals diverse fecal microbiota in Simmental calves during early development. Front Microbiol 2014;5:622.
28. Uyeno Y, Sekiguchi Y, Kamagata Y. rRNA-based analysis to monitor succession of faecal bacterial communities in Holstein calves. Lett Appl Microbiol 2010;51:570–577.
29. Edrington TS, Dowd SE, Farrow RF, et al. Development of colonic microflora as assessed by pyrosequencing in dairy calves fed waste milk. J Dairy Sci 2012;95:4519–4525.
30. Malmuthuge N, Li M, Goonewardene LA, et al. Effect of calf starter feeding on gut microbial diversity and expression of genes involved in host immune responses and tight junctions in dairy calves during weaning transition. J Dairy Sci 2013;96:3189–3200.
31. Smith T, Orcutt ML. The bacteriology of the intestinal tract of young calves with special reference to the early diarrhea (“scours”). J Exp Med 1925;41:89–106.
32. Isaacson RE, Moon HW, Schneider RA. Distribution and virulence of Escherichia coli in the small intestines of calves with and without diarrhea. Am J Vet Res 1978;39:1750–1775.
33. Youanes YD, Herdt TH. Changes in small intestinal morphology and flora associated with decreased energy digestibility in calves with naturally occurring diarrhea. Am J Vet Res 1987;48:719–725.
34. Dominguez-Bello MG, Costello EK, Contreras M, et al. Delivery mode shapes the acquisition and structure of the initial microbiota across multiple body habitats in newborns. Proc Natl Acad Sci U S A 2010;107:11971–11975.
35. Malmuthuge N, Chen Y, Liang G, et al. Heat-treated colostrum feeding promotes beneficial bacteria colonization in the small intestine of neonatal calves. J Dairy Sci 2015;98:8044–8053.
36. Pereira RV, Siler JD, Ng JC, et al. Effect of preweaned dairy calf housing system on antimicrobial resistance in commensal Escherichia coli. J Dairy Sci 2014;97:7633–7643.
37. Van Vleck Pereira R, Lima S, Siler JD, et al. Ingestion of milk containing very low concentration of antimicrobials: Longitudinal effect on fecal microbiota composition in preweaned calves. PLoS ONE 2016;11:e0147525.
38. Oultram J, Phipps E, Teixeira AG, et al. Effects of antibiotics (oxytetracycline, florfenicol or tulathromycin) on neonatal calves’ faecal microbial diversity. Vet Rec 2015;177:598–599.
39. Foditsch C, Pereira RV, Ganda EK, et al. Oral Administration of Faecalibacterium prausnitzii Decreased the incidence of severe diarrhea and related mortality rate and increased weight gain in preweaned dairy heifers. PLoS ONE 2015;10:e0145485.
40. Mackie RI, Sghir A, Gaskins HR. Developmental microbial ecology of the neonatal gastrointestinal tract. Am J Clin Nutr 1999;69:1035S–1045S.
41. Jost T, Lacroix C, Braegger CP, et al. New insights in gut microbiota establishment in healthy breast-fed neonates. PLoS ONE 2012;7:e44595.
42. Costa MC, Stämpfli HR, Allen-Vercoe E, et al. Development of the faecal microbiota in foals. Equine Vet J 2016;48:681–688. doi:10.1111/evj.12532.
43. Zivkovic AM, Barile D. Bovine milk as a source of functional oligosaccharides for improving human health. Adv Nutr 2011;2:284–289.
44. Yu ZT, Chen C, Kling DE, et al. The principal fucosylated oligosaccharides of human milk exhibit prebiotic properties on cultured infant microbiota. Glycobiology 2013;23:169–177.
45. Nelson MC, Morrison HG, Benjamino J, et al. Analysis, optimization and verification of Illumina-generated 16S rRNA gene amplicon surveys. PLoS ONE 2014;9:e94249.
46. Singh P, Teal TK, Marsh TL, et al. Intestinal microbial communities associated with acute enteric infections and disease recovery. Microbiome 2015;3:45.
47. Weese JS, Jelinski M. Assessment of the Fecal Microbiota in Beef Calves. J Vet Intern Med 2017;31:176–185. doi:10.1111/jvim.14611.
48. Maharshak N, Packey CD, Ellermann M, et al. Altered enteric microbiota ecology in interleukin 10-deficient mice during development and progression of intestinal inflammation. Gut Microbes 2013;4:316–324.
49. Devkota S, Wang Y, Musch MW, et al. Dietary-fat-induced taurocholic acid promotes pathobiont expansion and colitis in Il10-/- mice. Nature 2012;487:104–108.
50. Shin NR, Whon TW, Bae JW. Proteobacteria: Microbial signature of dysbiosis in gut microbiota. Trends Biotechnol 2015;33:496–503.
51. Stecher B, Chaffron S, Käppeli R, et al. Like will to like: Abundances of closely related species can predict susceptibility to intestinal colonization by pathogenic and commensal bacteria. PLoS Pathog 2010;6:e1000711.
52. Sokol H, Pigneur B, Watterlot L, et al. Faecalibacterium prausnitzii is an anti-inflammatory commensal bacterium identified by gut microbiota analysis of Crohn disease patients. Proc Natl Acad Sci USA 2008;105:16731–19736.
53. Minamoto Y, Otoni CC, Steelman SM, et al. Alteration of the fecal microbiota and serum metabolite profiles in dogs with idiopathic inflammatory bowel disease. Gut Microbes 2015;6:33–47.
54. Suchodolski JS, Foster ML, Sohail MU, et al. The fecal microbiome in cats with diarrhea. PLoS ONE 2015;10:e0127378.
55. Costa MC, Arroyo LG, Allen-Vercoe E, et al. Comparison of the fecal microbiota of healthy horses and horses with colitis by high throughput sequencing of the V3-V5 region of the 16S rRNA gene. PLoS ONE 2012;7:e41484.
56. Sokol H, Seksik P, Furet JP, et al. Low counts of Faecalibacterium prausnitzii in colitis microbiota. Inflamm Bowel Dis 2009;15:1183–1189.
57. Duffy LC, Zielezny MA, Riepenhoff-Talty M, et al. Effectiveness of Bifidobacterium bifidum in mediating the clinical course of murine rotavirus diarrhea. Pediatr Res 1994;35:690–695.
58. Perdigón G, Locascio M, Medici M, et al. Interaction of bifidobacteria with the gut and their influence in the immune function. Biocell 2003;27:1–9.
59. Veiga P, Pons N, Agrawal A, et al. Changes of the human gut microbiome induced by a fermented milk product. Sci Rep 2014;4:6328.
60. Duncan SH, Louis P, Flint HJ. Lactate-utilizing bacteria, isolated from human feces, that produce butyrate as a major fermentation product. Appl Environ Microbiol 2004;70:5810–5817.
61. Furusawa Y, Obata Y, Fukuda S, et al. Commensal microbe-derived butyrate induces the differentiation of colonic regulatory T cells. Nature 2013;504:446–450.
62. Liévin V, Peiffer I, Hudault S, et al. Bifidobacterium strains from resident infant human gastrointestinal microflora exert antimicrobial activity. Gut 2000;47:646–652.
63. Fujiwara S, Hashiba H, Hirota T, Forstner JF. Proteinaceous factor(s) in culture supernatant fluids of bifidobacteria which prevents the binding of enterotoxigenic Escherichia coli to gangliotetraosylceramide. Appl Environ Microbiol 1997;63:506–512.
64. De Simone C, Ciardi A, Grassi A, et al. Effect of Bifidobacterium bifidum and Lactobacillus acidophilus on gut mucosa and peripheral blood B lymphocytes. Immunopharmacol Immunotoxicol 1992;14:331–340.
65. Yasui H, Kiyoshima J, Ushijima H. Passive protection against rotavirus-induced diarrhea of mouse pups born to and nursed by dams fed Bifidobacterium breve YIT4064. J Infect Dis 1995;172:403–409.
66. Abe F, Ishibashi N, Shimamura S. Effect of administration of Bifidobacteria and lactic acid bacteria to newborn calves and piglets. J Dairy Sci 1995;78:2838–2846.
67. Gevers D, Kugathasan S, Denson LA, et al. The treatment-naive microbiome in new-onset Crohn's disease. Cell Host Microbe 2014;15:382–392.
68. Pérez-Urria E, Avalos A. Approach to a comparative study of the metabolism of porphyrins and chlorophylls. J Natural Sci 2015;3:1–16.