Diversity and temporal stability of bacterial communities in a model passerine bird, the zebra finch

Molecular Ecology

Volumn 19, Issue 24, 2010, Pages 5531-5544

  Benskin, Clare McW H ^a   Rhodes, Glenn ^b   Pickup, Roger W ^c   Wilson, Kenneth ^a   Hartley, Ian R ^a  

^a LANCASTER UNIVERSITY   (United Kingdom)

^b CENTRE FOR ECOLOGY AND HYDROLOGY   (United Kingdom)

^c LANCASTER UNIVERSITY   (United Kingdom)

Author keywords

16S rDNA; bacterial diversity and temporal stability; faecal microbial community analysis; passerine; PCR TGGE

Indexed keywords

RNA 16S;

ANIMAL; ARTICLE; DENATURING GRADIENT GEL ELECTROPHORESIS; FEMALE; FINCH; GENETICS; MALE; MICROBIOLOGY; POLYMERASE CHAIN REACTION;

ANIMALS; DENATURING GRADIENT GEL ELECTROPHORESIS; FEMALE; FINCHES; MALE; POLYMERASE CHAIN REACTION; RNA, RIBOSOMAL, 16S;

AVES; BACTERIA (MICROORGANISMS); PASSERIFORMES; TAENIOPYGIA GUTTATA;

EID: 78650100110     PISSN: 09621083     EISSN: 1365294X     Source Type: Journal    
DOI: 10.1111/j.1365-294X.2010.04892.x     Document Type: Article

References (100)

1. Altschul SF, Gish W, Miller W, Myers EW, Lipman DJ, (1990) Basic local alignment search tool. Journal of Molecular Biology, 215, 403-410.
2. Apajalahti JHA, Kettunen A, Bedford MR, Holben WE, (2001) Percent G-C profiling accurately reveals diet-related differences in the gastrointestinal microbial community of broiler chickens. Applied and Environmental Microbiology, 67, 5656-5667.
3. Apajalahti JH, Kettunen A, Graham H, (2004) Characteristics of the gastrointestinal microbial communities, with special reference to the chicken. World's Poultry Science Journal, 60, 223-232.
4. Atlas RM, Bartha R, (1998) Microbial Ecology: Fundamentals and Applications. Benjamin/Cummings Publishing Company Inc., Menlo Park, California.
5. Backhed F, Ley RE, Sonnenburg JL, Peterson DA, Gordon JI, (2005) Host-bacterial mutualism in the human intestine. Science, 307, 1915-1920.
6. Bakker TCM, Pomiankowski A, (1995) The genetic basis of female mate preferences. Journal of Evolutionary Biology, 8, 129-171.
7. Bangert RL, Ward ACS, Stauber EH, Cho BR, Widders PR, (1988a) A survey of the aerobic bacteria in the feces of captive raptors. Avian Diseases, 32, 53-62.
8. Bangert RL, Cho BR, Widders PR, Stauber EH, Ward ACS, (1988b) A survey of aerobic bacteria and fungi in the feces of healthy psittacine birds. Avian Diseases, 32, 46-52.
9. Barbosa TM, Serra CR, Ragione RML, Woodward MJ, Henriques AO, (2005) Screening for Bacillus isolates in the broiler gastrointestinal tract. Applied and Environmental Microbiology, 71, 968-978.
10. Benjamin J, Leaper S, Owen RJ, Skirrow MB, (1983) Description of Campylobacter laridis, a new species comprising the nalidixic acid resistant thermophilic Campylobacter (NARTC) group. Current Microbiology, 8, 231-238.
11. Bennett ATD, Cuthill IC, Partridge JC, Maier EJ, (1996) Ultraviolet vision and mate choice in zebra finches. Nature, 380, 433-435.
12. Benskin CMH, Wilson K, Jones K, Hartley IR, (2009) Bacterial pathogens in wild birds: a review of the frequency and effects of infection. Biological Reviews of the Cambridge Philosophical Society, 84, 349-373.
13. Birkhead TR, Pellatt J, Hunter FM, (1988) Extra-pair copulation and sperm competition in the zebra finch. Nature, 334, 60-62.
14. Birkhead TR, Pellatt EJ, Brekke P, Yeates R, Castillo-Juarez H, (2005) Genetic effects on sperm design in the zebra finch. Nature, 434, 383-387.
15. Bjerrum L, Engberg RM, Leser TD, et al. (2006) Microbial community composition of the ileum and cecum of broiler chickens as revealed by molecular and culture-based techniques. Poultry Science, 85, 1151-1164.
16. Bull SA, Thomas A, Humphrey T, et al. (2008) Flock health indicators and Campylobacter spp. in commercial housed broilers reared in Great Britain. Applied and Environmental Microbiology, 74, 5408-5413.
17. Burley N, (1981) Sex-ratio manipulation and selection for attractiveness. Science, 211, 721-722.
18. Burley NT, Fostera VS, (2006) Variation in female choice of mates: condition influences selectivity. Animal Behaviour, 72, 713-719.
19. Burtt EHJ, Ichida JM, (1999) Occurrence of feather-degrading bacilli in the plumage of birds. The Auk, 116, 364-372.
20. Byrd JA, Hargis BM, Caldwell DJ, et al. (2001) Effect of lactic acid administration in the drinking water during preslaughter feed withdrawal on Salmonella and Campylobacter contamination of broilers. Poultry Science, 80, 278-283.
21. Cartman ST, Ragione RML, Woodward MJ, (2008) Bacillus subtilis spores germinate in the chicken gastrointestinal tract. Applied and Environmental Microbiology, 74, 5254-5258.
22. Collins MD, Wallbanks S, (1992) Comparative sequence analysis of the 16s rRNA genes of Lactobacillus minutus, Lactobacillus rimae and Streptococcus parvulus: proposal for the creation of a new genus Atopobium. FEMS Microbiology Letters, 95, 235-240.
23. Dahllöf I, (2002) Molecular community analysis of microbial diversity. Current Opinion in Biotechnology, 13, 213-217.
24. Dahllöf I, Baillie H, Kjelleberg S, (2000) rpoB-based microbial community analysis avoids limitations inherent in 16S rRNA gene intraspecies heterogeneity. Applied and Environmental Microbiology, 66, 3376-3380.
25. Droual R, Ghazikhanian GY, Shivaprasad HL, Barr BC, Bland MB, (1997) Streptococcus bovis infection in turkey poults. Avian Pathology, 26, 433-439.
26. Edwards U, Rogall T, Blöcker H, Emde M, Böttger EC, (1989) Isolation and direct complete nucleotide determination of entire genes. Characterization of a gene coding for 16S ribosomal RNA. Nucleic Acids Research, 17, 7843-7853.
27. Falconer DS, Mackay TFC, (1996) Introduction to Quantitative Genetics, 4th edn. Longman, Essex.
28. Feher O, Wang HB, Saar S, Mitra PP, Tchernichovski O, (2009) De novo establishment of wild-type song culture in the zebra finch. Nature, 459, 564-568.
29. Felske A, Rheims H, Wolterink A, Stackebrandt E, Akkermans ADL, (1997) Ribosome analysis reveals prominent activity of an uncultured member of the class Actinobacteria in grassland soils. Microbiology, 143, 2983-2989.
30. Fielding AH, (2007) Cluster and Classification Techniques for the Biosciences. Cambridge University Press, Cambridge.
31. Fogel GB, Collins CR, Li J, Brunk CF, (1999) Prokaryotic genome size and SSU rDNA copy number: estimation of microbial relative abundance from a mixed population. Microbial Ecology, 38, 93-113.
32. Fujisawa T, Shirasaka S, Watabe J, Mitsuoka T, (1984) Lactobacillus aviarius sp. nov.: a new species isolated from the intestine of chickens. Systematic and Applied Microbiology, 5, 414-420.
33. Goldstein G, Flory KR, Browne BA, et al. (2004) Bacterial degradation of black and white feathers. The Auk, 121, 656-659.
34. Gunderson AR, Forsyth MH, Swaddle JP, (2009) Evidence that plumage bacteria influence feather coloration and body condition of eastern bluebirds Sialia sialis. Journal of Avian Biology, 40, 440-447.
35. Hartley IR, Griffith SC, Wilson K, Shepherd M, Burke T, (1999) Nestling sex ratios in the polygynously breeding Corn Bunting Miliaria calandra. Journal of Avian Biology, 30, 7-14.
36. Heuer H, Krsek M, Baker P, Smalla K, Wellington EMH, (1997) Analysis of actinomycete communities by specific amplification of genes encoding 16S rRNA and gel-electrophoretic separation in denaturing gradients. Applied and Environmental Microbiology, 63, 3233-3241.
37. Hudson PJ, Rizzoli A, Grenfell BT, Heesterbeek H, Dobson AP, (2002) The Ecology of Wildlife Diseases. Oxford University Press, Oxford.
38. Jaccard P, (1908) Nouvelles recherches sur la distribution florale. Bulletin de la Société Vaudoise des Sciences Naturelles, 44, 223-270.
39. Jin LZ, Ho YW, Abdullah N, (1998) Growth performance, intestinal microbial populations and serum cholesterol of broilers fed diets containing Lactobacillus cultures. Poultry Science, 77, 1259-1265.
40. Kapperud G, Rosef O, (1983) Avian wildlife reservoir of Campylobacter fetus subsp. jejuni, Yersinia spp., and Salmonella spp. in Norway. Applied and Environmental Microbiology, 45, 375-380.
41. Kizerwetter-Świda M, Binek M, (2008) Bacterial microflora of the chicken embryos and newly hatched chicken. Journal of Animal and Feed Sciences, 17, 224-232.
42. Kube M, Migdoll AM, Muller I, et al. (2008) The genome of Erwinia tasmaniensis strain Et1/99, a non-pathogenic bacterium in the genus Erwinia. Environmental Microbiology, 10, 2211-2222.
43. Lan PTN, Sakamoto M, Benno Y, (2004) Effects of two probiotic Lactobacillus strains on jejunal and cecal microbiota of broiler chicken under acute heat stress condition as revealed by molecular analysis of 16S rRNA genes. Microbiology and Immunology, 48, 917-929.
44. Lan Y, Vertegen MWA, Tamminga S, Williams BA, (2005) The role of the commensal gut microbial community in broiler chickens. World's Poultry Science Journal, 61, 95-104.
45. Lane D, Pace B, Olsen GJ, et al. (1985) Rapid determination of 16S ribosomal RNA sequences for phylogenetic analyses. Proceedings of the National Academy of Sciences USA, 82, 6955-6959.
46. Lastovica AJ, Skirrow MB, (2000) Clinical significance of Campylobacter and related species other than Campylobacter jejuni and C. Coli. In: Campylobacter (eds, Nachamkin I, Blaser MJ,), pp. 89-120. ASM, Washington, D.C.
47. Lemon WC, (1991) Fitness consequences of foraging behavior in the zebra finch. Nature, 352, 153-155.
48. Levesque B, Brousseau P, Bernier F, Dewailly E, Joly J, (2000) Study of the bacterial content of ring-billed gull droppings in relation to recreational water quality. Water Research, 34, 1089-1096.
49. Lu J, Idris U, Harmon B, et al. (2003) Diversity and succession of the intestinal bacterial community of the maturing broiler chicken. Applied and Environmental Microbiology, 69, 6816-6824.
50. Lu J, Domingo JWS, Lamendella R, Edge T, Hill S, (2008) Phylogenetic diversity and molecular detection of bacteria in gull feces. Applied and Environmental Microbiology, 74, 3969-3976.
51. Lucas FS, Heeb P, (2005) Environmental factors shape cloacal bacterial assemblages in great tit Parus major and blue tit P. caeruleus nestlings. Journal of Avian Biology, 36, 510-516.
52. Mantel N, (1967) The detection of disease clustering and a generalized regression approach. Cancer Research, 27, 209-220.
53. Matsuda M, Moore JE, (2004) Urease-positive thermophilic Campylobacter species. Applied and Environmental Microbiology, 70, 4415-4418.
54. McCracken VJ, Simpson JM, Mackie RI, Gaskins HR, (2001) Molecular ecological analysis of dietary and antibiotic-induced alterations of the mouse intestinal microbiota. Journal of Nutrition, 131, 1862-1870.
55. McCullagh P, Nelder JA, (1989) Generalized Linear Models. Taylor & Francis Ltd, London.
56. McCurdy DG, Shutler D, Mullie A, Forbes MR, (1998) Sex-biased parasitism of avian hosts: relations to blood parasite taxon and mating system. Oikos, 82, 303-312.
57. Mead GC, (1997) Bacteria in the gastrointestinal tract of birds. In: Gastrointestinal Microbiology 2.2 Gastrointestinal Microbes and Host Interaction (eds, Mackie RI, White BA, Isaacson RE,), pp. 216-240. Chapman and Hall, New York.
58. Moore S, Wilson K, (2002) Parasites as a viability cost of natural selection in natural populations of mammals. Science, 297, 2015-2018.
59. Moore JE, Gilpin D, Crothers E, et al. (2002) Occurrence of Campylobacter spp. and Cryptosporidium spp. in seagulls (Larus spp.). Vector Borne Zoonotic Diseases, 2, 111-114.
60. Murray G, Hollibaugh JT, Dobbs FC, Karl DM, (1996) Phylogenetic compositions of bacterioplankton from two California estuaries compared by denaturing gradient gel electrophoresis of 16S rDNA fragments. Applied and Environmental Microbiology, 62, 2676-2680.
61. Muyzer G, (1999) DGGE/TGGE a method for identifying genes from natural ecosystems. Current Opinion in Microbiology, 2, 317-322.
62. Muyzer G, Smalla K, (1998) Application of denaturing gradient gel electrophoresis (DGGE) and temperature gradient gel electrophoresis (TGGE) in microbial ecology. Antonie van Leeuwenhoek, 73, 127-141.
63. 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 encoding for 16S rRNA. Applied and Environmental Microbiology, 59, 695-700.
64. Pacha RE, Clark GW, Williams EA, Carter AM, (1988) Migratory birds of central Washington as reservoirs of Campylobacter jejuni. Canadian Journal of Microbiology, 34, 80-82.
65. Pennycott TW, Cinderey RN, Park A, Mather HA, Foster G, (2002) Salmonella enterica subspecies enterica serotype Typhimurium and Escherichia coli 086 in wild birds at two garden sites in south-west Scotland. The Veterinary Record, 151, 563-567.
66. Poulin R, (1996) Sexual inequalities in helminth infections: a cost of being a male? The American Naturalist, 147, 287-295. (Pubitemid 2625402)
67. Qin J, Li R, Raes J, et al. (2010) A human gut microbial gene catalogue established by metagenomic sequencing. Nature, 464, 59-67.
68. Quigley EMM, (2010) Prebiotics and probiotics: modifying and mining microbiota. Pharmacological Research, 61, 213-218.
69. Reynolds JH, Bolker B, (2001) Available from http://www.biostat.wustl. edu/archives/html/s-news/2001-03/msg00154.html.
70. Royle NJ, Hartley IR, Parker GA, (2002) Sexual conflict reduces offspring fitness in zebra finches. Nature, 416, 733-736.
71. Ruiz-Rodríguez M, Soler JJ, Lucas FS, et al. (2009) Bacterial diversity at the cloaca relates to an immune response in magpie Pica pica and to body condition of great spotted cuckoo Clamator glandarius nestlings. Journal of Avian Biology, 40, 42-48.
72. Santure AW, Stapley J, Ball AD, et al. (2010) On the use of large marker panels to estimate inbreeding and relatedness: empirical and simulation studies of a pedigreed zebra finch population typed at 771 SNPs. Molecular Ecology, 19, 1439-1451.
73. Savage DC, (1977) Microbial ecology of the gastrointestinal tract. Annual Review of Microbiology, 31, 107-133.
74. Schalk G, Forbes MR, (1997) Male biases in parasitism of mammals: effects of study type, host age, and parasite taxon. Oikos, 78, 67-74.
75. Shawkey MD, Mills KL, Dale C, Hill GE, (2005) Microbial diversity of wild bird feathers revealed through culture-based and culture-independent techniques. Microbial Ecology, 50, 40-47.
76. Simpson JM, McCracken VJ, White BA, Gaskins HR, Mackie RI, (1999) Application of denaturant gradient gel electrophoresis for the analysis of the porcine gastrointestinal microbiota. Journal of Microbiological Methods, 36, 167-179.
77. Simpson JM, McCracken VJ, Gaskins HR, Mackie RI, (2000) Denaturing gradient gel electrophoresis analysis of 16s ribosomal DNA amplicons to monitor changes in fecal bacterial populations of weaning pigs after introduction of Lactobacillus reuteri strain MM53. Applied and Environmental Microbiology, 66, 4705-4714.
78. Simpson JM, Martineau B, Jones WE, Ballam JM, Mackie RI, (2002) Characterization of fecal bacterial populations in canines: effects of age, breed and dietary fiber. Microbial Ecology, 44, 186-197.
79. Sneath PHA, Mair NS, Sharpe ME, Holt JG, (1986) Bergey's Manual of Determinative Bacteriology. Williams and Wilkins, Baltimore.
80. Stolp H, (1988) Microbial Ecology: Organisms, Habitats, Activities. Cambridge University Press, Cambridge.
81. Suchodolski JS, Ruaux CG, Steiner JM, Fetz K, Williams DA, (2004) Application of molecular fingerprinting for qualitative assessment of small-intestinal bacterial diversity in dogs. Journal of Clinical Microbiology, 42, 4702-4708.
82. Vaahtovuo J, Toivanen P, Eerola E, (2001) Study of murine fecal microflora by cellular fatty acids analysis; effect of age and mouse strain. Antonie van Leeuwenhoek, 80, 35-42.
83. Van der Wielen PWJJ, Keuzenkamp DA, Lipman LJA, Van Knapen F, Biesterveld S, (2002) Spatial and temporal variation of the intestinal bacterial community in commercially raised broiler chickens during growth. Microbial Ecology, 44, 286-293.
84. Waldenström J, Broman T, Carlsson I, et al. (2002) Prevalence of Campylobacter jejuni, Campylobacter lari, and Campylobacter coli in different ecological guilds and taxa of migrating birds. Applied and Environmental Microbiology, 68, 5911-5917.
85. Walker SE, Sander JE, Cline JL, Helton JS, (2002) Characterization of Pseudomonas aeruginosa isolates associated with mortality in broiler chicks. Avian Diseases, 46, 1045-1050.
86. Wallace RB, Johnson MJ, Suggs SV, et al. (1981) A set of synthetic oligodeoxyribonucleotide primers for DNA sequencing in the plasmid vector pBR322. Gene, 16, 21-26.
87. Warren WC, Clayton DF, Ellegren H, et al. (2010) The genome of a songbird. Nature, 464, 757-762.
88. Wehausen JD, Ramey II RR, Epps CW, (2004) Experiments in DNA extraction and PCR amplification from bighorn sheep feces: the importance of DNA extraction method. Journal of Heredity, 95, 503-509.
89. Wei G, Lu H, Zhou Z, et al. (2007) The microbial community in the feces of the giant panda (Ailuropoda melanoleuca) as determined by PCR-TGGE profiling and clone library analysis. Microbial Ecology, 54, 194-202.
90. White DG, Ayers S, Maurer JJ, Thayer SG, Hofacre C, (2003) Antimicrobial susceptibilities of Staphylococcus aureus isolated from commercial broilers in northeastern Georgia. Avian Diseases, 47, 203-210.
91. Wilson K, Grenfell BT, (1997) Generalized linear modelling for parasitologists. Parasitology Today, 13, 33-38.
92. Wilson K, Hardy ICW, (2002) Statistical analysis of sex ratios: an introduction. In: Sex ratios: Concepts and Research Methods (ed., Hardy ICW,), pp. 48-92. Cambridge University Press, Cambridge.
93. Wilson K, Grenfell BT, Shaw DJ, (1996) Analysis of aggregated parasite distributions: a comparison of methods. Functional Ecology, 10, 592-601.
94. Wobeser G, Kost W, (1992) Starvation, staphylococcosis and vitamin A deficiency among mallards overwintering in Saskatchewan. Journal of Wildlife Diseases, 28, 215-222.
95. Zann RA, (1996) The Zebra Finch: A Synthesis of Field and Laboratory Studies. Oxford University Press, Oxford.
96. Zhao Y, Li W, Zhou Z, et al. (2005) Dynamics of microbial community structure and cellulolytic activity in agricultural soil amended with two biofertilizers. European Journal of Soil Biology, 41, 21-29.
97. Zhu XY, Zhong T, Pandya Y, Joerger RD, (2002) 16S rRNA-based analysis of microbiota from the cecum of broiler chickens. Applied and Environmental Microbiology, 68, 124-137.
98. Zoetendal EG, Akkermans ADL, De Vos WM, (1998) Temperature gradient gel electrophoresis analysis from human fecal samples reveals stable and host-specific communities of active bacteria. Applied and Environmental Microbiology, 64, 3854-3859.
99. Zoetendal EG, Cheng B, Koike S, Mackie RI, (2004) Molecular microbial ecology of the gastrointestinal tract: from phylogeny to function. Current Issues in Intestinal Microbiology, 5, 31-48.
100. Zuk M, (2009) The sicker sex. PLoS Pathogens, 5, e1000267.