Marked seasonal variation in the wild mouse gut microbiota

ISME Journal

Volumn 9, Issue 11, 2015, Pages 2423-2434

  Maurice, Corinne F ^a   Cl Knowles, Sarah ^b,c   Ladau, Joshua ^d   Pollard, Katherine S ^d,e   Fenton, Andy ^f   Pedersen, Amy B ^b   Turnbaugh, Peter J ^a,g  

^a HARVARD UNIVERSITY   (United States)

^b UNIVERSITY OF EDINBURGH   (United Kingdom)

^c IMPERIAL COLLEGE LONDON   (United Kingdom)

^d GLADSTONE INSTITUTES   (United States)

^e UNIVERSITY OF CALIFORNIA   (United States)

^f UNIVERSITY OF LIVERPOOL   (United Kingdom)

^g UNIVERSITY OF CALIFORNIA   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

BACTERIUM; CAPTIVE POPULATION; COLONIZATION; DIETARY SHIFT; DIGESTIVE SYSTEM; ENVIRONMENTAL FACTOR; GENE EXPRESSION; INSECT; MICROBIAL COMMUNITY; MOLECULAR ANALYSIS; NEMATODE; RODENT; SEASONAL VARIATION; SEED; SPECIES DIVERSITY; WILD POPULATION; WOODLAND;

ALISTIPES; APODEMUS SYLVATICUS; BACTERIA (MICROORGANISMS); BACTEROIDETES; BACTEROIDETES PHYLUM; FIRMICUTES; HELICOBACTER; HEXAPODA; LACTOBACILLUS; MAMMALIA; MUS; NEMATODA; PROTEOBACTERIA; RODENTIA;

RNA 16S;

ANIMAL; BACTEROIDETES; CLASSIFICATION; ECOSYSTEM; FEMALE; GENETICS; INTESTINE; INTESTINE FLORA; LACTOBACILLUS; MALE; MICROBIOLOGY; MOUSE; PARASITOLOGY; PHENOTYPE; PROTEOBACTERIA; SEASON; STATISTICAL MODEL; UNITED KINGDOM; WILD ANIMAL;

ANIMALS; ANIMALS, WILD; BACTEROIDETES; ECOSYSTEM; FEMALE; GASTROINTESTINAL MICROBIOME; INTESTINES; LACTOBACILLUS; LINEAR MODELS; MALE; MICE; PHENOTYPE; PROTEOBACTERIA; RNA, RIBOSOMAL, 16S; SEASONS; UNITED KINGDOM;

EID: 84945485419     PISSN: 17517362     EISSN: 17517370     Source Type: Journal    
DOI: 10.1038/ismej.2015.53     Document Type: Article

References (55)

1. Amato KR, Yeoman CJ, Kent A, Righini N, Carbonero F, Estrada A, et al. (2013). Habitat degradation impacts black howler monkey (Alouatta pigra) gastrointestinal microbiomes. ISME J 7: 1344-1353
2. Amato KR, Leigh SR, Kent A, Mackie RI, Yeoman CJ, Stumpf RM, et al. (2015). The gut microbiota appears to compensate for seasonal diet variation in the wild black howler monkey (Alouatta pigra). Microb Ecol 69: 434-443
3. Bates D, Maechler M, Bolker B, Walker S. (2014). lme4: Linear mixed-effects models using Eigen and S4. R package version 0.999999-2. http://CRAN.R-project. org/package=lme4
4. Benson AK, Kelly SA, Legge R, Ma F, Low SJ, Kim J, et al. (2010). Individuality in gut microbiota composition is a complex polygenic trait shaped by multiple environmental and host genetic factors. Proc Natl Acad Sci USA 107: 18933-18938
5. Bolnick DI, Snowberg LK, Hirsch PE, Lauber CL, Knight R, Caporaso JG, et al. (2014). Individuals' diet diversity influences gut microbial diversity in two freshwater fish (threespine stickleback and Eurasian perch). Ecol Lett 17: 979-987
6. Caporaso JG, Kuczynski J, Stombaugh J, Bittinger K, Bushman FD, Costello EK, et al. (2010). QIIME allows analysis of high-Throughput community sequencing data. Nat Methods 7: 335-336
7. Carey HV, Walters WA, Knight R. (2013). Seasonal restructuring of the ground squirrel gut microbiota over the annual hibernation cycle. Am J Physiol Regul Integr Comp Physiol 304: R33-R42
8. Carmody RN, Gerber GK, Luevano Jr. JM, Gatti DM, Somes L, Svenson KL, et al. (2015). Diet dominates host genotype in shaping the murine gut microbiota. Cell Host Microbe 17: 72-84
9. Costello EK, Stagaman K, Dethlefsen L, Bohannan BJ, Relman DA. (2012). The application of ecological theory toward an understanding of the human microbiome. Science 336: 1255-1262
10. Davenport ER, Mizrahi-Man O, Michelini K, Barreiro LB, Ober C, Gilad Y. (2014). Seasonal variation in human gut microbiome composition. PLoS One 9: e90731
11. David LA, Maurice CF, Carmody RN, Gootenberg DB, Button JE, Wolfe BE, et al. (2014). Diet rapidly and reproducibly alters the human gut microbiome. Nature 505: 559-563
12. Degnan PH, Pusey AE, Lonsdorf EV, Goodall J, Wroblewski EE, Wilson ML, et al. (2012). Factors associated with the diversification of the gut microbial communities within chimpanzees from Gombe National Park. Proc Natl Acad Sci USA 109: 13034-13039
13. DeSantis TZ, Hugenholtz P, Larsen N, Rojas M, Brodie EL, Keller K, et al. (2006). Greengenes, a chimera-checked 16 S rRNA gene database and workbench compatible with ARB. Appl Environ Microbiol 72: 5069-5072
14. Di Rienzi SC, Sharon I, Wrighton KC, Koren O, Hug LA, Thomas BC, et al. (2013). The human gut and groundwater harbor non-photosynthetic bacteria belonging to a new candidate phylum sibling to Cyanobacteria. Elife 2: e01102
15. Duncan SH, Belenguer A, Holtrop G, Johnstone AM, Flint HJ, Lobley GE. (2007). Reduced dietary intake of carbohydrates by obese subjects results in decreased concentrations of butyrate and butyrate-producing bacteria in feces. Appl Environ Microbiol 73: 1073-1078
16. Eaton KA, Honkala A, Auchtung TA, Britton RA. (2011). Probiotic Lactobacillus reuteri ameliorates disease due to enterohemorrhagic Escherichia coli in germfree mice. Infect Immun 79: 185-191
17. Faith JJ, Guruge JL, Charbonneau M, Subramanian S, Seedorf H, Goodman AL, et al. (2013). The long-Term stability of the human gut microbiota. Science 341: 1237439
18. Godsall B, Coulson T, Malo AF. (2014). From physiology to space use: energy reserves and androgenization explain home-range size variation in a woodland rodent. J Anim Ecol 83: 126-135
19. Goodrich JK, Waters JL, Poole AC, Sutter JL, Koren O, Blekhman R, et al. (2014). Human genetics shape the gut microbiome. Cell 159: 789-799
20. Gurnell J. (1993). Tree seed production and food conditions for rodents in an Oak Wood in southern England. Forestry 66: 291-315
21. Hayes KS, Bancroft AJ, Goldrick M, Portsmouth C, Roberts IS, Grencis RK. (2010). Exploitation of the intestinal microflora by the parasitic nematode Trichuris muris. Science 328: 1391-1394
22. Kabir AM, Aiba Y, Takagi A, Kamiya S, Miwa T, Koga Y. (1997). Prevention of Helicobacter pylori infection by lactobacilli in a gnotobiotic murine model. Gut 41: 49-55
23. Keeney KM, Finlay BB. (2011). Enteric pathogen exploitation of the microbiota-generated nutrient environment of the gut. Curr Opin Microbiol 14: 92-98
24. Knowles SC, Fenton A, Petchey OL, Jones TR, Barber R, Pedersen AB. (2013). Stability of within-host-parasite communities in a wild mammal system. Proc Biol Sci 280: 20130598
25. Koren O, Goodrich JK, Cullender TC, Spor A, Laitinen K, Backhed HK, et al. (2012). Host remodeling of the gut microbiome and metabolic changes during pregnancy. Cell 150: 470-480
26. Ley RE, Hamady M, Lozupone C, Turnbaugh PJ, Ramey RR, Bircher JS, et al. (2008). Evolution of mammals and their gut microbes. Science 320: 1647-1651
27. Ley RE, Lozupone CA, Hamady M, Knight R, Gordon JI. (2008). Worlds within worlds: evolution of the vertebrate gut microbiota. Nat Rev Microbiol 6: 776-788
28. Linnenbrink M, Wang J, Hardouin EA, Kunzel S, Metzler D, Baines JF. (2013). The role of biogeography in shaping diversity of the intestinal microbiota in house mice. Mol Ecol 22: 1904-1916
29. Maurice CF, Haiser HJ, Turnbaugh PJ. (2013). Xenobiotics shape the physiology and gene expression of the active human gut microbiome. Cell 152: 39-50
30. McKnite AM, Perez-Munoz ME, Lu L, Williams EG, Brewer S, Andreux PA, et al. (2012). Murine gut microbiota is defined by host genetics and modulates variation of metabolic traits. PLoS One 7: e39191
31. Medellin-Pena MJ, Griffiths MW. (2009). Effect of molecules secreted by Lactobacillus acidophilus strain La-5 on Escherichia coli O157: H7 colonization. Appl Environ Microbiol 75: 1165-1172
32. Meyer F, Paarmann D, D'Souza M, Olson R, Glass EM, Kubal M, et al. (2008). The metagenomics RAST server-A public resource for the automatic phylogenetic and functional analysis of metagenomes. BMC Bioinformatics 9: 386
33. Moran PA. (1950). Notes on continuous stochastic phenomena. Biometrika 37: 17-23
34. Muegge BD, Kuczynski J, Knights D, Clemente JC, Gonzalez A, Fontana L, et al. (2011). Diet drives convergence in gut microbiome functions across mammalian phylogeny and within humans. Science 332: 970-974
35. Nakagawa S, Schielzeth H. (2013). A general and simple method for obtaining R2 from generalized linear mixedeffects models. Methods Ecol Evol 4: 133-142
36. Nowell F, Higgs S. (1989). Eimeria species infecting wood mice (genus Apodemus) and the transfer of two species to Mus musculus. Parasitology 98: 329-336
37. O'Rourke JL, Grehan M, Lee A. (2001). Non-pylori Helicobacter species in humans. Gut 49: 601-606
38. Ochman H, Worobey M, Kuo CH, Ndjango JB, Peeters M, Hahn BH, et al. (2010). Evolutionary relationships of wild hominids recapitulated by gut microbial communities. PLoS Biol 8: e1000546
39. Oksanen J, Blanchet FG, Kindt R, Legendre P, Minchin PR, O'Hara RB, et al. (2015), vegan: Community Ecology Package. R package version 2.2-1. http://CRANRprojectorg/package=vegan
40. Parker SE, Malone S, Bunte RM, Smith AL. (2009). Infectious diseases in wild mice (Mus musculus) collected on and around the University of Pennsylvania (Philadelphia) Campus. Comp Med 59: 424-430
41. Pena JA, Rogers AB, Ge Z, Ng V, Li SY, Fox JG, et al. (2005). Probiotic Lactobacillus spp. diminish Helicobacter hepaticus-induced inflammatory bowel disease in interleukin-10-deficient mice. Infect Immun 73: 912-920
42. Pike N. (2011). Using false discovery rates for multiple comparisons in ecology and evolution. Methods Ecol Evol 2: 278-282
43. Pritchard MH, Kruse GOW. (1982). The Collection and Preservation of Animal Parasites, vol. 1. University of Nebraska Press: Lincoln, NE
44. Rausch S, Held J, Fischer A, Heimesaat MM, Kuhl AA, Bereswill S, et al. (2013). Small intestinal nematode infection of mice is associated with increased enterobacterial loads alongside the intestinal tract. PLoS One 8: e74026
45. Reynolds LA, Smith KA, Filbey KJ, Harcus Y, Hewitson JP, Redpath SA, et al. (2014). Commensal-pathogen interactions in the intestinal tract: lactobacilli promote infection with, and are promoted by, helminth parasites. Gut Microbes 5: 522-532
46. Segata N, Izard J, Waldron L, Gevers D, Miropolsky L, Garrett WS, et al. (2012). Metagenomic biomarker discovery and explanation. Genome Biol 12: R60
47. Segata N, Waldron L, Ballarini A, Narasimhan V, Jousson O, Huttenhower C. (2012). Metagenomic microbial community profiling using unique clade-specific marker genes. Nat Methods 9: 811-814
48. Sommer F, Backhed F. (2013). The gut microbiota-masters of host development and physiology. Nat Rev Microbiol 11: 227-238
49. Walk ST, Blum AM, Ewing SA, Weinstock JV, Young VB. (2010). Alteration of the murine gut microbiota during infection with the parasitic helminth Heligmosomoides polygyrus. Inflamm Bowel Dis 16: 1841-1849
50. Wang J, Linnenbrink M, Kunzel S, Fernandes R, Nadeau MJ, Rosenstiel P, et al. (2014). Dietary history contributes to enterotype-like clustering and functional metagenomic content in the intestinal microbiome of wild mice. Proc Natl Acad Sci USA 111: E2703-E2710
51. Wasimuddin, Cizkova D, Bryja J, Albrechtova J, Hauffe HC, Pialek J. (2012). High prevalence and species diversity of Helicobacter spp. detected in wild house mice. Appl Environ Microbiol 78: 8158-8160
52. Watts CHB. (1968). Foods eaten by wood mice (Apodemus sylvaticus) and bank voles (Clethrionomys glareolus) in Wytham Woods, Berkshire. J Anim Ecol 37: 25-41
53. Wolfe BE, Button JE, Santarelli M, Dutton RJ. (2014). Cheese rind communities provide tractable systems for in situ and in vitro studies of microbial diversity. Cell 158: 422-433
54. Yatsunenko T, Rey FE, Manary MJ, Trehan I, Dominguez-Bello MG, Contreras M, et al. (2012). Human gut microbiome viewed across age and geography. Nature 486: 222-227
55. Zenewicz LA, Yin X, Wang G, Elinav E, Hao L, Zhao L, et al. (2013). IL-22 deficiency alters colonic microbiota to be transmissible and colitogenic. J Immunol 190: 5306-5312