TY - JOUR
T1 - Longitudinal study of murine microbiota activity and interactions with the host during acute inflammation and recovery
AU - Schwab, Clarissa
AU - Berry, David
AU - Rauch, Isabella
AU - Rennisch, Ina
AU - Ramesmayer, Julia
AU - Hainzl, Eva
AU - Heider, Susanne
AU - Decker, Thomas
AU - Kenner, Lukas
AU - Müller, Mathias
AU - Strobl, Birgit
AU - Wagner, Michael
AU - Schleper, Christa
AU - Loy, Alexander
AU - Urich, Tim
N1 - Funding Information:
This work was financially supported by the Austrian Federal Ministry of Science and Research (GEN-AU III InflammoBiota) and the Austrian Science Fund (FWF, P25369-B22). The authors wish to thank Carmen Czepe, Heinz Ekker and Andreas Sommer from Campus Science Support Facilities GmbH (CSF), Vienna, for Illumina HiSeq sequencing.
PY - 2014
Y1 - 2014
N2 - 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.The ISME Journal advance online publication, 9 January 2014; doi:10.1038/ismej.2013.223.
AB - 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.The ISME Journal advance online publication, 9 January 2014; doi:10.1038/ismej.2013.223.
KW - butyrate
KW - flagellin
KW - metatranscriptomics
KW - mucin
KW - recovery
UR - https://www.scopus.com/pages/publications/84899484295
U2 - 10.1038/ismej.2013.223
DO - 10.1038/ismej.2013.223
M3 - Article
C2 - 24401855
SN - 1751-7362
VL - 8
SP - 1101
EP - 1114
JO - The ISME Journal: multidisciplinary journal of microbial ecology
JF - The ISME Journal: multidisciplinary journal of microbial ecology
IS - 5
ER -