Effects of vendor and genetic background on the composition of the fecal microbiota of inbred mice

PLoS ONE

Volumn 10, Issue 2, 2015, Pages

  Ericsson, Aaron C ^a   Davis, J Wade ^a   Spollen, William ^a   Bivens, Nathan ^a   Givan, Scott ^a   Hagan, Catherine E ^a   McIntosh, Mark ^a,b   Franklin, Craig L ^a  

^a UNIVERSITY OF MISSOURI   (United States)

^b University of Missouri   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

DNA 16S; RNA 16S;

AMPLICON; ARTICLE; CONTROLLED STUDY; DNA EXTRACTION; DNA SEQUENCE; FECES COMPOSITION; FECES MICROFLORA; FEMALE; GENOME ANALYSIS; INBRED MOUSE STRAIN; INTESTINE FLORA; MOUSE; NEXT GENERATION SEQUENCING; NONHUMAN; OPERATIONAL TAXONOMIC UNIT; SPECIES DIVERSITY; SPECIES RICHNESS; STRAIN DIFFERENCE; TAXONOMY; ANIMAL; BIODIVERSITY; CLUSTER ANALYSIS; EXPERIMENTAL ANIMAL; FECES; GASTROINTESTINAL TRACT; GENETICS; METAGENOME; MICROBIOLOGY; MICROFLORA;

ANIMALIA; MUS; MUS MUSCULUS;

ANIMALS; ANIMALS, LABORATORY; BIODIVERSITY; CLUSTER ANALYSIS; FECES; FEMALE; GASTROINTESTINAL TRACT; METAGENOME; MICE; MICE, INBRED STRAINS; MICROBIOTA; RNA, RIBOSOMAL, 16S;

EID: 84922982129     PISSN: None     EISSN: 19326203     Source Type: Journal    
DOI: 10.1371/journal.pone.0116704     Document Type: Article

References (43)

1. Metzker ML. Sequencing technologies - the next generation. Nature reviews Genetics. 2010; 11(1): 31-46. doi: 10.1038/nrg2626 PMID: 19997069
2. Sekirov I, Russell SL, Antunes LC, Finlay BB. Gut microbiota in health and disease. Physiological reviews. 2010; 90(3): 859-904. doi: 10.1152/physrev.00045.2009 PMID: 20664075
3. de Vos WM, de Vos EA. Role of the intestinal microbiome in health and disease: from correlation to causation. Nutrition reviews. 2012; 70 Suppl 1: S45-56. doi: 10.1111/j.1753-4887.2012.00505.x PMID: 22861807
4. Collins FS, Tabak LA. Policy: NIH plans to enhance reproducibility. Nature. 2014; 505(7485): 612-613. PMID: 24482835
5. Perrin S. Preclinical research: Make mouse studies work. Nature. 2014; 507(7493): 423-425. PMID: 24678540
6. Wu HJ, Ivanov II, Darce J, Hattori K, Shima T, Umesaki Y, et al. Gut-residing segmented filamentous bacteria drive autoimmune arthritis via T helper 17 cells. Immunity. 32(6): 815-827. doi: 10.1016/j.immuni.2010.06.001 PMID: 20620945
7. Denning TL, Norris BA, Medina-Contreras O, Manicassamy S, Geem D, Madan R, et al. Functional specializations of intestinal dendritic cell and macrophage subsets that control Th17 and regulatory T cell responses are dependent on the T cell/APC ratio, source of mouse strain, and regional localization. J Immunol. 2011; 187(2): 733-747. doi: 10.4049/jimmunol.1002701 PMID: 21666057
8. Ivanov II, Atarashi K, Manel N, Brodie EL, Shima T, Karaoz U, et al. Induction of intestinal Th17 cells by segmented filamentous bacteria. Cell. 2009; 139(3): 485-498. doi: 10.1016/j.cell.2009.09.033 PMID: 19836068
9. Yang I, Eibach D, Kops F, Brenneke B, Woltemate S, Schulze J, et al. Intestinal microbiota composition of interleukin-10 deficient C57BL/6J mice and susceptibility to Helicobacter hepaticus-induced colitis. PloS one. 2013; 8(8): e70783. doi: 10.1371/journal.pone.0070783 PMID: 23951007
10. Lee YK, Menezes JS, Umesaki Y, Mazmanian SK. Proinflammatory T-cell responses to gut microbiota promote experimental autoimmune encephalomyelitis. Proc Natl Acad Sci U S A. 2011; 108 Suppl 1: 4615-4622. doi: 10.1073/pnas.1000082107 PMID: 20660719
11. Deloris Alexander A, Orcutt RP, Henry JC, Baker J Jr, Bissahoyo AC, Threadgill DW. Quantitative PCR assays for mouse enteric flora reveal strain-dependent differences in composition that are influenced by the microenvironment. Mammalian genome: official journal of the International Mammalian Genome Society. 2006; 17(11): 1093-1104. PMID: 17091319
12. Kovacs A, Ben-Jacob N, Tayem H, Halperin E, Iraqi FA, Gophna U. Genotype is a stronger determinant than sex of the mouse gut microbiota. Microb Ecol. 2011; 61(2): 423-428. doi: 10.1007/s00248-010-9787-2 PMID: 21181142
13. Hufeldt MR, Nielsen DS, Vogensen FK, Midtvedt T, Hansen AK. Variation in the gut microbiota of laboratory mice is related to both genetic and environmental factors. Comp Med. 2010; 60(5): 336-347. PMID: 21262117
14. Friswell MK, Gika H, Stratford IJ, Theodoridis G, Telfer B, Wilson ID, et al. Site and strain-specific variation in gut microbiota profiles and metabolism in experimental mice. PloS one. 2010; 5(1): e8584. doi: 10.1371/journal.pone.0008584 PMID: 20052418
15. Yu Z, Morrison M. Improved extraction of PCR-quality community DNA from digesta and fecal samples. BioTechniques. 2004; 36(5): 808-812. PMID: 15152600
16. Caporaso JG, Lauber CL, Walters WA, Berg-Lyons D, Lozupone CA, Turnbaugh PJ, et al. Global patterns of 16S rRNA diversity at a depth of millions of sequences per sample. Proc Natl Acad Sci U S A. 2011; 108 Suppl 1: 4516-4522. doi: 10.1073/pnas.1000080107 PMID: 20534432
17. Walters WA, Caporaso JG, Lauber CL, Berg-Lyons D, Fierer N, Knight R. PrimerProspector: de novo design and taxonomic analysis of barcoded polymerase chain reaction primers. Bioinformatics. 2011; 27(8): 1159-1161. doi: 10.1093/bioinformatics/btr087 PMID: 21349862
18. Loy A, Maixner F, Wagner M, Horn M. probeBase-an online resource for rRNA-targeted oligonucleotide probes: new features 2007. Nucleic acids research. 2007; 35(Database issue): D800-804. PMID: 17099228
19. Magoc T, Salzberg SL. FLASH: fast length adjustment of short reads to improve genome assemblies. Bioinformatics. 2011; 27(21): 2957-2963. doi: 10.1093/bioinformatics/btr507 PMID: 21903629
20. Kuczynski J, Stombaugh J, Walters WA, Gonzalez A, Caporaso JG, Knight R. Using QIIME to analyze 16S rRNA gene sequences from microbial communities. Current protocols in bioinformatics / editoral board, Baxevanis Andreas D[et al]. 2011; Chapter 10: Unit 10 17. doi: 10.1002/0471250953.bi0801s36 PMID: 22161570
21. Altschul SF, Madden TL, Schaffer AA, Zhang J, Zhang Z, Miller W, et al. Gapped BLAST and PSIBLAST: a new generation of protein database search programs. Nucleic acids research. 1997; 25(17): 3389-3402. PMID: 9254694
22. DeSantis TZ, Hugenholtz P, Larsen N, Rojas M, Brodie EL, Keller K, et al. Greengenes, a chimera-checked 16S rRNA gene database and workbench compatible with ARB. Applied and environmental microbiology. 2006; 72(7): 5069-5072. PMID: 16820507
23. McMurdie PJ, Holmes S. phyloseq: an R package for reproducible interactive analysis and graphics of microbiome census data. PloS one. 2013; 8(4): e61217. doi: 10.1371/journal.pone.0061217 PMID: 23630581
24. Paulson JN, Pop M, Bravo HC. metagenomeSeq: Statistical analysis for sparse high-throughput sequencing. Bioconductor package 160.http://cbcb.umd.edu/software/metagenomeSeq.
25. McMurdie PJ, Holmes S. Waste not, want not: why rarefying microbiome data is inadmissible. PLoS computational biology. 2014; 10(4): e1003531. doi: 10.1371/journal.pcbi.1003531 PMID: 24699258
26. Bourgon R, Gentleman R, Huber W. Independent filtering increases detection power for high-throughput experiments. Proc Natl Acad Sci U S A. 2010; 107(21): 9546-9551. doi: 10.1073/pnas.0914005107 PMID: 20460310
27. Smyth GK. Linear models and empirical bayes methods for assessing differential expression in microarray experiments. Statistical applications in genetics and molecular biology. 2004; 3: Article3.
28. Smyth GK. Limma: linear models for microarray data. Gentleman R, Carey V, Dudoit S, Irizarry R, Huber W, editors. New York, NY: Springer; 2005.
29. Benjamini Y HY. Controlling the false discovery rate: a practical and powerful approach to multiple testing. Journal of the Royal Statistical Society Series B. 1995; 57: 289-300.
30. Ivanov II, Frutos Rde L, Manel N, Yoshinaga K, Rifkin DB, Sartor RB, et al. Specific microbiota direct the differentiation of IL-17-producing T-helper cells in the mucosa of the small intestine. Cell host & microbe. 2008; 4(4): 337-349. doi: 10.1155/2015/395307 PMID: 25632391
31. Ericsson AC, Hagan CE, Davis DJ, Franklin CL. A review of segmented filamentous bacteria-commensal microbes with potential impact on research. Comparative Medicine. 2014;in press. PMID: 25527031
32. Derrien M, Van Baarlen P, Hooiveld G, Norin E, Muller M, de Vos WM. Modulation of Mucosal Immune Response, Tolerance, and Proliferation in Mice Colonized by the Mucin-Degrader Akkermansia muciniphila. Frontiers in microbiology. 2011; 2: 166. doi: 10.3389/fmicb.2011.00166 PMID: 21904534
33. Everard A, Belzer C, Geurts L, Ouwerkerk JP, Druart C, Bindels LB, et al. Cross-talk between Akkermansia muciniphila and intestinal epithelium controls diet-induced obesity. Proc Natl Acad Sci U S A. 2013; 110(22): 9066-9071. doi: 10.1073/pnas.1219451110 PMID: 23671105
34. Shin NR, Lee JC, Lee HY, Kim MS, Whon TW, Lee MS, et al. An increase in the Akkermansia spp. population induced by metformin treatment improves glucose homeostasis in diet-induced obese mice. Gut. 2014; 63(5): 727-735. doi: 10.1136/gutjnl-2012-303839 PMID: 23804561
35. Lathrop SK, Bloom SM, Rao SM, Nutsch K, Lio CW, Santacruz N, et al. Peripheral education of the immune system by colonic commensal microbiota. Nature. 2011; 478(7368): 250-254. doi: 10.1038/nature10434 PMID: 21937990
36. Round JL, Mazmanian SK. Inducible Foxp3+ regulatory T-cell development by a commensal bacterium of the intestinal microbiota. Proc Natl Acad Sci U S A. 2010; 107(27): 12204-12209. doi: 10.1073/pnas.0909122107 PMID: 20566854
37. Kverka M, Zakostelska Z, Klimesova K, Sokol D, Hudcovic T, Hrncir T, et al. Oral administration of Parabacteroides distasonis antigens attenuates experimental murine colitis through modulation of immunity and microbiota composition. Clin Exp Immunol. 2011; 163(2): 250-259. doi: 10.1111/j.1365-2249.2010.04286.x PMID: 21087444
38. Baron EJ. Bilophila wadsworthia: a unique Gram-negative anaerobic rod. Anaerobe. 1997; 3(2-3): 83-86. PMID: 16887616
39. Mosca A, D'Alagni M, Del Prete R, De Michele GP, Summanen PH, Finegold SM, et al. Preliminary evidence of endotoxic activity of Bilophila wadsworthia. Anaerobe. 1995; 1(1): 21-24. PMID: 16887503
40. Wang L, Christophersen CT, Sorich MJ, Gerber JP, Angley MT, Conlon MA. Increased abundance of Sutterella spp. and Ruminococcus torques in feces of children with autism spectrum disorder. Molecular autism. 2013; 4(1): 42. doi: 10.1186/2040-2392-4-42 PMID: 24188502
41. Manichanh C, Borruel N, Casellas F, Guarner F. The gut microbiota in IBD. Nature reviews Gastroenterology & hepatology. 2012; 9(10): 599-608. doi: 10.1038/nrgastro.2014.229 PMID: 25582351
42. Campbell JH, Foster CM, Vishnivetskaya T, Campbell AG, Yang ZK, Wymore A, et al. Host genetic and environmental effects on mouse intestinal microbiota. The ISME journal. 2012; 6(11): 2033-2044. doi: 10.1038/ismej.2012.54 PMID: 22695862
43. Hildebrand F, Nguyen TL, Brinkman B, Yunta RG, Cauwe B, Vandenabeele P, et al. Inflammation-associated enterotypes, host genotype, cage and inter-individual effects drive gut microbiota variation in common laboratory mice. Genome biology. 2013; 14(1): R4. doi: 10.1186/gb-2013-14-1-r4 PMID: 23347395