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

David Berry, Clarissa Schwab, Gabriel Milinovich, Jochen Reichert, Karim Ben Mahfoudh, Thomas Decker, Marion Engel, Brigitte Hai, Eva Hainzl, Susanne Heider, Lukas Kenner, Mathias Müller, Isabella Rauch, Birgit Strobl, Michael Wagner, Christa Schleper, Tim Urich, Alexander Loy

Research output: Contribution to journalArticle

121 Citations (Scopus)

Abstract

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.

Original languageEnglish (US)
Pages (from-to)2091-2106
Number of pages16
JournalISME Journal
Volume6
Issue number11
DOIs
StatePublished - Nov 1 2012
Externally publishedYes

Fingerprint

Dextran Sulfate
sodium sulfate
colitis
dextran
Colitis
intestinal microorganisms
sodium
ribosomal RNA
sulfate
mice
Health
Microbiota
Verrucomicrobiaceae
gene
Bacteroidaceae
transcription (genetics)
phylogenetics
family structure
Flagellin
flagellin

Keywords

  • Akkermansia
  • colitis
  • dextran sodium sulfate
  • gut microbiota
  • Lachnospiraceae
  • Mucispirillum

ASJC Scopus subject areas

  • Microbiology
  • Ecology, Evolution, Behavior and Systematics

Cite this

Berry, D., Schwab, C., Milinovich, G., Reichert, J., Ben Mahfoudh, K., Decker, T., ... Loy, A. (2012). Phylotype-level 16S rRNA analysis reveals new bacterial indicators of health state in acute murine colitis. ISME Journal, 6(11), 2091-2106. https://doi.org/10.1038/ismej.2012.39

Phylotype-level 16S rRNA analysis reveals new bacterial indicators of health state in acute murine colitis. / Berry, David; Schwab, Clarissa; Milinovich, Gabriel; Reichert, Jochen; Ben Mahfoudh, Karim; Decker, Thomas; Engel, Marion; Hai, Brigitte; Hainzl, Eva; Heider, Susanne; Kenner, Lukas; Müller, Mathias; Rauch, Isabella; Strobl, Birgit; Wagner, Michael; Schleper, Christa; Urich, Tim; Loy, Alexander.

In: ISME Journal, Vol. 6, No. 11, 01.11.2012, p. 2091-2106.

Research output: Contribution to journalArticle

Berry, D, Schwab, C, Milinovich, G, Reichert, J, Ben Mahfoudh, K, Decker, T, Engel, M, Hai, B, Hainzl, E, Heider, S, Kenner, L, Müller, M, Rauch, I, Strobl, B, Wagner, M, Schleper, C, Urich, T & Loy, A 2012, 'Phylotype-level 16S rRNA analysis reveals new bacterial indicators of health state in acute murine colitis', ISME Journal, vol. 6, no. 11, pp. 2091-2106. https://doi.org/10.1038/ismej.2012.39
Berry D, Schwab C, Milinovich G, Reichert J, Ben Mahfoudh K, Decker T et al. Phylotype-level 16S rRNA analysis reveals new bacterial indicators of health state in acute murine colitis. ISME Journal. 2012 Nov 1;6(11):2091-2106. https://doi.org/10.1038/ismej.2012.39
Berry, David ; Schwab, Clarissa ; Milinovich, Gabriel ; Reichert, Jochen ; Ben Mahfoudh, Karim ; Decker, Thomas ; Engel, Marion ; Hai, Brigitte ; Hainzl, Eva ; Heider, Susanne ; Kenner, Lukas ; Müller, Mathias ; Rauch, Isabella ; Strobl, Birgit ; Wagner, Michael ; Schleper, Christa ; Urich, Tim ; Loy, Alexander. / Phylotype-level 16S rRNA analysis reveals new bacterial indicators of health state in acute murine colitis. In: ISME Journal. 2012 ; Vol. 6, No. 11. pp. 2091-2106.
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