Phylotype-level 16S rRNA analysis reveals new bacterial indicators of health state in acute murine colitis

被引:266
作者
Berry, David [2 ]
Schwab, Clarissa [1 ]
Milinovich, Gabriel [1 ]
Reichert, Jochen [2 ]
Ben Mahfoudh, Karim [2 ]
Decker, Thomas [3 ]
Engel, Marion [4 ]
Hai, Brigitte [4 ]
Hainzl, Eva [5 ]
Heider, Susanne [6 ]
Kenner, Lukas [6 ]
Mueller, Mathias [5 ]
Rauch, Isabella [3 ]
Strobl, Birgit [5 ]
Wagner, Michael [2 ]
Schleper, Christa [1 ]
Urich, Tim [1 ]
Loy, Alexander [2 ]
机构
[1] Univ Vienna, Dept Genet Ecol, Vienna Ecol Ctr, Fac Life Sci, A-1090 Vienna, Austria
[2] Univ Vienna, Dept Microbial Ecol, Vienna Ecol Ctr, Fac Life Sci, A-1090 Vienna, Austria
[3] Univ Vienna, Dept Microbiol Immunobiol & Genet, Max F Perutz Labs, A-1090 Vienna, Austria
[4] Deutsch Forschungszentrum Gesundheit & Umwelt Gmb, Res Unit Environm Genom, Helmholtz Zentrum Munchen, Neuherberg, Germany
[5] Univ Vet Med Vienna, Inst Anim Breeding & Genet, Vienna, Austria
[6] Med Univ Vienna, Ludwig Boltzmann Inst Canc Res, Vienna, Austria
关键词
gut microbiota; Lachnospiraceae; Akkermansia; Mucispirillum; dextran sodium sulfate; colitis; INFLAMMATORY-BOWEL-DISEASE; SULFATE-INDUCED COLITIS; HUMAN-COLON ECOSYSTEMS; GUT MICROBIOTA; AKKERMANSIA-MUCINIPHILA; TARGETED DISRUPTION; ULCERATIVE-COLITIS; COMMENSAL BACTERIA; MUCIN DEGRADATION; SIGNAL TRANSDUCER;
D O I
10.1038/ismej.2012.39
中图分类号
Q14 [生态学(生物生态学)];
学科分类号
071012 ; 0713 ;
摘要
Human inflammatory bowel disease and experimental colitis models in mice are associated with shifts in intestinal microbiota composition, but it is unclear at what taxonomic/phylogenetic level such microbiota dynamics can be indicative for health or disease. Here, we report that dextran sodium sulfate (DSS)-induced colitis is accompanied by major shifts in the composition and function of the intestinal microbiota of STAT1(-/-) and wild-type mice, as determined by 454 pyrosequencing of bacterial 16S rRNA (gene) amplicons, metatranscriptomics and quantitative fluorescence in situ hybridization of selected phylotypes. The bacterial families Ruminococcaceae, Bacteroidaceae, Enterobacteriaceae, Deferribacteraceae and Verrucomicrobiaceae increased in relative abundance in DSS-treated mice. Comparative 16S rRNA sequence analysis at maximum possible phylogenetic resolution identified several indicator phylotypes for DSS treatment, including the putative mucin degraders Akkermansia and Mucispirillum. The analysis additionally revealed strongly contrasting abundance changes among phylotypes of the same family, particularly within the Lachnospiraceae. These extensive phylotype-level dynamics were hidden when reads were grouped at higher taxonomic levels. Metatranscriptomic analysis provided insights into functional shifts in the murine intestinal microbiota, with increased transcription of genes associated with regulation and cell signaling, carbohydrate metabolism and respiration and decreased transcription of flagellin genes during inflammation. These findings (i) establish the first in-depth inventory of the mouse gut microbiota and its metatranscriptome in the DSS colitis model, (ii) reveal that family-level microbial community analyses are insufficient to reveal important colitis-associated microbiota shifts and (iii) support a scenario of shifting intra-family structure and function in the phylotype-rich and phylogenetically diverse Lachnospiraceae in DSS-treated mice. The ISME Journal (2012) 6, 2091-2106; doi:10.1038/ismej.2012.39; published online 10 May 2012
引用
收藏
页码:2091 / 2106
页数:16
相关论文
共 85 条
[1]   Microbial diversity and the genetic nature of microbial species [J].
Achtman, Mark ;
Wagner, Michael .
NATURE REVIEWS MICROBIOLOGY, 2008, 6 (06) :431-440
[2]   Divergence and redundancy of 16S rRNA sequences in genomes with multiple rrn operons [J].
Acinas, SG ;
Marcelino, LA ;
Klepac-Ceraj, V ;
Polz, MF .
JOURNAL OF BACTERIOLOGY, 2004, 186 (09) :2629-2635
[3]   T-bet is a STAT1-induced regulator of IL-12R expression in naive CD4+ T cells [J].
Afkarian, M ;
Sedy, JR ;
Yang, J ;
Jacobson, NG ;
Cereb, N ;
Yang, SY ;
Murphy, TL ;
Murphy, KM .
NATURE IMMUNOLOGY, 2002, 3 (06) :549-557
[4]   Monitoring Bacterial Community of Human Gut Microbiota Reveals an Increase in Lactobacillus in Obese Patients and Methanogens in Anorexic Patients [J].
Armougom, Fabrice ;
Henry, Mireille ;
Vialettes, Bernard ;
Raccah, Denis ;
Raoult, Didier .
PLOS ONE, 2009, 4 (09)
[5]   Hyaluronan-Mediated Leukocyte Adhesion and Dextran Sulfate Sodium-Induced Colitis Are Attenuated in the Absence of Signal Transducer and Activator of Transcription 1 [J].
Bandyopadhyay, Sudip K. ;
de la Motte, Carol A. ;
Kessler, Sean P. ;
Hascall, Vincent C. ;
Hill, David R. ;
Strong, Scott A. .
AMERICAN JOURNAL OF PATHOLOGY, 2008, 173 (05) :1361-1368
[6]   MOVEMENT OF MICROORGANISMS IN VISCOUS ENVIRONMENTS [J].
BERG, HC ;
TURNER, L .
NATURE, 1979, 278 (5702) :349-351
[7]   Barcoded Primers Used in Multiplex Amplicon Pyrosequencing Bias Amplification [J].
Berry, David ;
Ben Mahfoudh, Karim ;
Wagner, Michael ;
Loy, Alexander .
APPLIED AND ENVIRONMENTAL MICROBIOLOGY, 2011, 77 (21) :7846-7849
[8]   Commensal Bacteroides Species Induce Colitis in Host-Genotype-Specific Fashion in a Mouse Model of Inflammatory Bowel Disease [J].
Bloom, Seth M. ;
Bijanki, Vinieth N. ;
Nava, Gerardo M. ;
Sun, Lulu ;
Malvin, Nicole P. ;
Donermeyer, David L. ;
Dunne, W. Michael, Jr. ;
Allen, Paul M. ;
Stappenbeck, Thaddeus S. .
CELL HOST & MICROBE, 2011, 9 (05) :390-403
[9]   Body traffic: Ecology, genetics, and immunity in inflammatory bowel disease [J].
Braun, Jonathan ;
Wei, Bo .
ANNUAL REVIEW OF PATHOLOGY-MECHANISMS OF DISEASE, 2007, 2 :401-429
[10]   QIIME allows analysis of high-throughput community sequencing data [J].
Caporaso, J. Gregory ;
Kuczynski, Justin ;
Stombaugh, Jesse ;
Bittinger, Kyle ;
Bushman, Frederic D. ;
Costello, Elizabeth K. ;
Fierer, Noah ;
Pena, Antonio Gonzalez ;
Goodrich, Julia K. ;
Gordon, Jeffrey I. ;
Huttley, Gavin A. ;
Kelley, Scott T. ;
Knights, Dan ;
Koenig, Jeremy E. ;
Ley, Ruth E. ;
Lozupone, Catherine A. ;
McDonald, Daniel ;
Muegge, Brian D. ;
Pirrung, Meg ;
Reeder, Jens ;
Sevinsky, Joel R. ;
Tumbaugh, Peter J. ;
Walters, William A. ;
Widmann, Jeremy ;
Yatsunenko, Tanya ;
Zaneveld, Jesse ;
Knight, Rob .
NATURE METHODS, 2010, 7 (05) :335-336