Longitudinal study of murine microbiota activity and interactions with the host during acute inflammation and recovery

Clarissa Schwab, David Berry, Isabella Rauch, Ina Rennisch, Julia Ramesmayer, Eva Hainzl, Susanne Heider, Thomas Decker, Lukas Kenner, Mathias Müller, Birgit Strobl, Michael Wagner, Christa Schleper, Alexander Loy, Tim Urich

Research output: Contribution to journalArticle

73 Citations (Scopus)

Abstract

Although alterations in gut microbiota composition during acute colitis have been repeatedly observed, associated functional changes and the recovery from dysbiosis received little attention. In this study, we investigated structure and function of the gut microbiota during acute inflammation and recovery in a dextran sodium sulfate (DSS)-colitis mouse model using metatranscriptomics, bacterial 16S rRNA gene amplicon sequencing and monitoring of selected host markers. Parallel to an increase of host markers of inflammation during acute colitis, we observed relative abundance shifts and alterations in phylotype composition of the dominant bacterial orders Clostridiales and Bacteroidales, and an increase of the low abundant Enterobacteriales, Deferribacterales, Verrucomicrobiales and Erysipelotrichales. During recovery, the microbiota began to resume, but did not reach its original composition until the end of the experiment. Microbial gene expression was more resilient to disturbance, with pre-perturbation-Type transcript profiles appearing quickly after acute colitis. The decrease of Clostridiales during inflammation correlated with a reduction of transcripts related to butyrate formation, suggesting a disturbance in host-microbe signalling and mucosal nutrient provision. The impact of acute inflammation on the Clostridiales was also characterized by a significant downregulation of their flagellin-encoding genes. In contrast, the abundance of members of the Bacteroidales increased along with an increase in transcripts related to mucin degradation. We propose that acute inflammation triggered a selective reaction of the immune system against flagella of commensals and temporarily altered murine microbiota composition and functions relevant for the host. Despite changes in specific interactions, the host-microbiota homeostasis revealed a remarkable ability for recovery.

Original languageEnglish (US)
Pages (from-to)1101-1114
Number of pages14
JournalISME Journal
Volume8
Issue number5
DOIs
StatePublished - Jan 1 2014
Externally publishedYes

Fingerprint

Microbiota
longitudinal studies
Clostridiales
colitis
Longitudinal Studies
Colitis
inflammation
Inflammation
mice
intestinal microorganisms
Verrucomicrobiales
Enterobacteriales
Microbial Genes
Dysbiosis
Flagellin
functional change
disturbance
flagellin
Dextran Sulfate
sodium sulfate

Keywords

  • butyrate
  • flagellin
  • metatranscriptomics
  • mucin
  • recovery

ASJC Scopus subject areas

  • Microbiology
  • Ecology, Evolution, Behavior and Systematics

Cite this

Longitudinal study of murine microbiota activity and interactions with the host during acute inflammation and recovery. / Schwab, Clarissa; Berry, David; Rauch, Isabella; Rennisch, Ina; Ramesmayer, Julia; Hainzl, Eva; Heider, Susanne; Decker, Thomas; Kenner, Lukas; Müller, Mathias; Strobl, Birgit; Wagner, Michael; Schleper, Christa; Loy, Alexander; Urich, Tim.

In: ISME Journal, Vol. 8, No. 5, 01.01.2014, p. 1101-1114.

Research output: Contribution to journalArticle

Schwab, C, Berry, D, Rauch, I, Rennisch, I, Ramesmayer, J, Hainzl, E, Heider, S, Decker, T, Kenner, L, Müller, M, Strobl, B, Wagner, M, Schleper, C, Loy, A & Urich, T 2014, 'Longitudinal study of murine microbiota activity and interactions with the host during acute inflammation and recovery', ISME Journal, vol. 8, no. 5, pp. 1101-1114. https://doi.org/10.1038/ismej.2013.223
Schwab, Clarissa ; Berry, David ; Rauch, Isabella ; Rennisch, Ina ; Ramesmayer, Julia ; Hainzl, Eva ; Heider, Susanne ; Decker, Thomas ; Kenner, Lukas ; Müller, Mathias ; Strobl, Birgit ; Wagner, Michael ; Schleper, Christa ; Loy, Alexander ; Urich, Tim. / Longitudinal study of murine microbiota activity and interactions with the host during acute inflammation and recovery. In: ISME Journal. 2014 ; Vol. 8, No. 5. pp. 1101-1114.
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