Age-related differences in the cloacal microbiota of a wild bird species

Annals of Occupational and Environmental Medicine

Richard H Wagner²  Scott A Hatch¹  Étienne Danchin³  Pierrick Blanchard³  Sarah Leclaire³  Thomas Merkling³  Yoshan Moodley²  Hanja B Brandl²  Joël White³  Wouter FD van Dongen² 

[1]US Geological Survey, Alaska Science Center, 4210 University Drive, Anchorage, AK, 99508, USA

[2]Konrad Lorenz Institute of Ethology, Department of Integrative Biology and Evolution, University of Veterinary Medicine Vienna, Savoyenstrasse 1a, Vienna, 1160, Austria

[3]CNRS-UPS-ENFA

[4] Laboratoire Évolution & Diversité Biologique (EDB), UMR 5174, 118 Route de Narbonne, Toulouse, F-31062, France

关键词: Gastrointestinal tract;    Cloaca;    Black-legged kittiwakes;    Bacteria;    Automated ribosomal intergenic spacer analysis;    Age-differences;   

Others  :  1085478
DOI  :  10.1186/1472-6785-13-11

 received in 2012-11-16, accepted in 2013-03-14,  发布年份 2013

【 摘 要 】

Background

Gastrointestinal bacteria play a central role in the health of animals. The bacteria that individuals acquire as they age may therefore have profound consequences for their future fitness. However, changes in microbial community structure with host age remain poorly understood. We characterised the cloacal bacteria assemblages of chicks and adults in a natural population of black-legged kittiwakes (Rissa tridactyla), using molecular methods.

Results

We show that the kittiwake cloaca hosts a diverse assemblage of bacteria. A greater number of total bacterial OTUs (operational taxonomic units) were identified in chicks than adults, and chicks appeared to host a greater number of OTUs that were only isolated from single individuals. In contrast, the number of bacteria identified per individual was higher in adults than chicks, while older chicks hosted more OTUs than younger chicks. Finally, chicks and adults shared only seven OTUs, resulting in pronounced differences in microbial assemblages. This result is surprising given that adults regurgitate food to chicks and share the same nesting environment.

Conclusions

Our findings suggest that chick gastrointestinal tracts are colonised by many transient species and that bacterial assemblages gradually transition to a more stable adult state. Phenotypic differences between chicks and adults may lead to these strong differences in bacterial communities. These data provide the framework for future studies targeting the causes and consequences of variation in bacterial assemblages in wild birds.

【 授权许可】

   
2013 van Dongen et al.; licensee BioMed Central Ltd.

【 图 表 】

Figure 1.

Figure 2.

Figure 3.

Figure 4.

【 参考文献 】

• [1]Archie EA, Theis TR: Animal behaviour meets microbial ecology. Anim Behav 2011, 82:425-436.
• [2]Hill MJ: Intestinal flora and endogenous vitamin synthesis. Europ J Cancer Prevent, Supp 1997, 6:S43-S45.
• [3]Ley RE, Lozupone CA, Hamady M, Knight R, Gordon JI: Worlds within worlds: evolution of the vertebrate gut microbiota. Nat Rev Microbiol 2008, 6:776-788.
• [4]Macpherson AJ, Harris NL: Interactions between commensal intestinal bacteria and the immune system. Nat Rev Immun 2004, 4:478-485.
• [5]Benskin CMH, Wilson K, Jones K, Hartley IR: Bacterial pathogens in wild birds: a review of the frequency and effects of infection. Biol Rev Camb Philos Soc 2009, 84:349-373.
• [6]Ezenwa VO, Gerardo NM, Inouye DW, Medina M, Xavier JB: Animal behavior and the microbiome. Science 2012, 338:198-199.
• [7]Kohl KD: Diversity and function of the avian gut microbiota. J Comp Physiol B - Biochem Syst Environ Physiol 2012, 182:591-602.
• [8]Macfarlane GT, Macfarlane LE: Acquisition, evolution and maintenance of the normal gut microbiota. Dig Dis 2009, 27:90-98.
• [9]Palmer C, Bik EM, DiGiulio DB, Relman DA, Brown PO: Development of the human infant intestinal microbiota. PLoS Biol 2007, 5:1556-1573.
• [10]Godoy-Vitorino F, Goldfarb KC, Brodie EL, Garcia-Amado MA, Michelangeli F, Dominguez-Bello MG: Developmental microbial ecology of the crop of the folivorous hoatzin. Isme J 2010, 4:611-620.
• [11]Sharon G, Segal D, Ringo JM, Hefetz A, Zilber-Rosenberg I, Rosenberg E: Commensal bacteria play a role in mating preference of Drosophila melanogaster. Proc Natl Acad Sci USA 2010, 107:20051-20056.
• [12]Stecher B, Hardt WD: Mechanisms controlling pathogen colonization of the gut. Curr Opin Microbiol 2011, 14:82-91.
• [13]White J, Mirleau P, Danchin E, Mulard H, Hatch SA, Heeb P, Wagner RH: Sexually transmitted bacteria affect female cloacal assemblages in a wild bird. Ecol Lett 2010, 13:1515.
• [14]Lombardo MP: On the evolution of sexually transmitted diseases in birds. J Avian Biol 1998, 29:314-321.
• [15]Sheldon BC: Sexually transmitted disease in birds: occurrence and evolutionary significance. Philos Trans Biol Sci 1993, 339:491-497.
• [16]Lombardo MP, Thorpe PA, Power HW: The beneficial sexually transmitted microbe hypothesis of avian copulation. Behav Ecol 1999, 10:333-337.
• [17]Gong J, Yu H, Liu T, Gill JJ, Chambers JR, Wheatcroft R, Sabour PM: Effects of zinc bacitracin, bird age and access to range on bacterial microbiota in the ileum and caeca of broiler chickens. J Appl Microbiol 2008, 104:1372-1382.
• [18]Lan Y, Verstegen MWA, Tamminga S, Williams BA: The role of the commensal gut microbial community in broiler chickens. World Poultry Sci J 2005, 61:95-104.
• [19]Scupham AJ: Succession in the intestinal microbiota of preadolescent turkeys. FEMS Microbiol Ecol 2007, 60:136-147.
• [20]Tanikawa T, Shoji N, Sonohara N, Saito S, Shimura Y, Fukushima J, Inamoto T: Aging transition of the bacterial community structure in the chick ceca. Poult Sci 2011, 90:1004-1008.
• [21]Villers LM, Jang SS, Lent CL, Lewin-Koh SC, Norosoarinaivo JA: Survey and comparison of major intestinal flora in captive and wild ring-tailed lemur (Lemur catta) populations. Am J Primat 2008, 70:175-184.
• [22]Xenoulis PG, Gray PL, Brightsmith D, Palculict B, Hoppes S, Steiner JM, Tizard I, Suchodolski JS: Molecular characterization of the cloacal microbiota of wild and captive parrots. Vet Microbiol 2010, 146:320-325.
• [23]Gonzalez-Braojos S, Vela AI, Ruiz-de-Castaneda R, Briones V, Moreno J: Age-related changes in abundance of enterococci and Enterobacteriaceae in Pied Flycatcher (Ficedula hypoleuca) nestlings and their association with growth. J Ornithol 2012, 153:181-188.
• [24]Janiga M, Sedlarova A, Rigg R, Novotna M: Patterns of prevalence among bacterial communities of alpine accentors (Prunella collaris) in the Tatra Mountains. J Ornithol 2007, 148:135-143.
• [25]Lombardo MP, Thorpe PA, Cichewicz R, Henshaw M, Millard C, Steen C, Zeller TK: Communities of cloacal bacteria in Tree Swallow families. Condor 1996, 98:167-172.
• [26]Mills TK, Lombardo MP, Thorpe PA: Microbial colonization of the cloacae of nestling tree swallows. Auk 1999, 116:947-956.
• [27]Meade GC: Bacteria in the gastrointestinal tract of birds. In Gastrointestinal microbiology. Edited by Mackie RI, White BA, Isaacson RE. New York: Chapman and Hall; 1997.
• [28]Ranjard L, Brothier E, Nazaret S: Sequencing bands of ribosomal intergenic spacer analysis fingerprints for characterization and microscale distribution of soil bacterium populations responding to mercury spiking. Appl Environ Microbiol 2000, 66:5334-5339.
• [29]Kovacs A, Yacoby K, Gophna U: A systematic assessment of automated ribosomal intergenic spacer analysis (ARISA) as a tool for estimating bacterial richness. Res Microbiol 2010, 161:192-197.
• [30]Altschul SF, Gish W, Miller W, Myers EW, Lipman DJ: Basic local alignment search tool. J Mol Biol 1990, 215:403-410.
• [31]Jobb G, von Haeseler A, Strimmer K: TREEFINDER: A powerful graphical analysis environment for molecular phylogenetics. BMC Evol Biol 2004, 4:18. BioMed Central Full Text
• [32]Huelsenbeck JP, Ronquist F: MRBAYES: Bayesian inference of phylogeny. Bioinformatics 2001, 17:754-755.
• [33]Lozupone C, Hamady M, Knight R: UniFrac - an online tool for comparing microbial community diversity in a phylogenetic context. BMC Bioinformatics 2006, 7:371. BioMed Central Full Text
• [34]Banning NC, Gleeson DB, Grigg AH, Grant CD, Andersen GL, Brodie EL, Murphy DV: Soil microbial community successional patterns during forest ecosystem restoration. Appl Environ Microbiol 2011, 77:6158-6164.
• [35]Corrigan A, Horgan K, Clipson N, Murphy RA: Effect of dietary supplementation with a Saccharomyces cerevisiae mannan oligosaccharide on the bacterial community structure of broiler cecal contents. Appl Environ Microbiol 2011, 77:6653-6662.
• [36]Schottner S, Pfitzner B, Grunke S, Rasheed M, Wild C, Ramette A: Drivers of bacterial diversity dynamics in permeable carbonate and silicate coral reef sands from the Red Sea. Environ Microbiol 2011, 13:1815-1826.
• [37]Weimer PJ, Stevenson DM, Mantovani HC, Man SLC: Host specificity of the ruminal bacterial community in the dairy cow following near-total exchange of ruminal contents. J Dairy Sci 2011, 93:5902-5912.
• [38]White J, Richard M, Massot M, Meylan S: Cloacal bacterial diversity increases with multiple mates: evidence of sexual transmission in female common lizards. PLoS ONE 2011, 6:e22339.
• [39]Chandler DP, Fredrickson JK, Brockman FJ: Effect of PCR template concentration on the composition and distribution of total community 16S rDNA clone libraries. Mol Ecol 1997, 6:475-482.
• [40]Scupham AJ, Jones JA, Wesley IV: Comparison of DNA extraction methods for analysis of turkey cecal microbiota. J Appl Microbiol 2007, 102:401-409.
• [41]Haussmann MF, Winkler DW, Huntington CE, Vleck D, Sanneman CE, Hanley D, Vleck CM: Cell-mediated immunosenescence in birds. Oecologia 2005, 145:270-275.
• [42]Lavoie ET, Sorrell EM, Perez DR, Ottinger MA: Immunosenescence and age-related susceptibility to influenza virus in Japanese quail. Dev Comp Immunol 2007, 31:407-414.
• [43]Noreen E, Bourgeon S, Bech C: Growing old with the immune system: a study of immunosenescence in the zebra finch (Taeniopygia guttata). J Comp Physiol B - Biochem Syst Environ Physiol 2011, 181:649-656.
• [44]Flint JF, Garner MR: Feeding beneficial bacteria: A natural solution for increasing efficiency and decreasing pathogens in animal agriculture. J Appl Poultry Res 2009, 18:367-378.
• [45]Koenen ME, Kramer J, van der Hulst R, Heres L, Jeurissen SH, Boersma WJ: Immunomodulation by probiotic lactobacilli in layer- and meat-type chickens. Brit Poultry Sci 2004, 45:355-366.
• [46]Duriez P, Clermont O, Bonacorsi S, Bingen E, Chaventre A, Elion J, Picard B, Denamur E: Commensal Escherichia coli isolates are phylogenetically distributed among geographically distinct human populations. Microbiology-Sgm 2001, 147:1671-1676.
• [47]Blanco G, Lemus JA, Grande J: Faecal bacteria associated with different diets of wintering red kites: influence of livestock carcass dumps in microflora alteration and pathogen acquisition. J Appl Ecol 2006, 43:990-998.
• [48]Klomp JE, Murphy MT, Smith SB, McKay JE, Ferrera I, Reysenbach AL: Cloacal microbial communities of female spotted towhees Pipilo maculatus: microgeographic variation and individual sources of variability. J Avian Biol 2008, 39:530-538.
• [49]Banks JC, Cary SC, Hogg ID: The phylogeography of Adelie penguin faecal flora. Environ Microbiol 2009, 11:577-588.
• [50]Ruiz-de-Castaneda R, Vela AI, Lobato E, Briones V, Moreno J: Prevalence of potentially pathogenic culturable bacteria on eggshells and in cloacae of female Pied Flycatchers in a temperate habitat in central Spain. J Field Ornithol 2011, 82:215-224.
• [51]Arumugam M, Raes J, Pelletier E, Le Paslier D, Yamada T, Mende DR, Fernandes GR, Tap J, Bruls T, Batto JM: Enterotypes of the human gut microbiome. Nature 2011, 473:174-180.