title: Host-compound foraging by intestinal microbiota revealed by single-cell stable isotope probing.
abstract: The animal and human intestinal mucosa secretes an assortment of compounds to establish a physical barrier between the host tissue and intestinal contents, a separation that is vital for health. Some pathogenic microorganisms as well as members of the commensal intestinal microbiota have been shown to be able to break down these secreted compounds. Our understanding of host-compound degradation by the commensal microbiota has been limited to knowledge about simplified model systems because of the difficulty in studying the complex intestinal ecosystem in vivo. In this study, we introduce an approach that overcomes previous technical limitations and allows us to observe which microbial cells in the intestine use host-derived compounds. We added stable isotope-labeled threonine i.v. to mice and combined fluorescence in situ hybridization with high-resolution secondary ion mass spectrometry imaging to characterize utilization of host proteins by individual bacterial cells. We show that two bacterial species, Bacteroides acidifaciens and Akkermansia muciniphila, are important host-protein foragers in vivo. Using gnotobiotic mice we show that microbiota composition determines the magnitude and pattern of foraging by these organisms, demonstrating that a complex microbiota is necessary in order for this niche to be fully exploited. These results underscore the importance of in vivo studies of intestinal microbiota, and the approach presented in this study will be a powerful tool to address many other key questions in animal and human microbiome research.
authors.affiliation: Department of Microbial Ecology, Vienna Ecology Center, Faculty of Life Sciences, University of Vienna, A-1090 Vienna, Austria.
authors.forename: David
authors.initials: D
authors.lastname: Berry
authors.forename: Bärbel
authors.initials: B
authors.lastname: Stecher
authors.forename: Arno
authors.initials: A
authors.lastname: Schintlmeister
authors.forename: Jochen
authors.initials: J
authors.lastname: Reichert
authors.forename: Sandrine
authors.initials: S
authors.lastname: Brugiroux
authors.forename: Birgit
authors.initials: B
authors.lastname: Wild
authors.forename: Wolfgang
authors.initials: W
authors.lastname: Wanek
authors.forename: Andreas
authors.initials: A
authors.lastname: Richter
authors.forename: Isabella
authors.initials: I
authors.lastname: Rauch
authors.forename: Thomas
authors.initials: T
authors.lastname: Decker
authors.forename: Alexander
authors.initials: A
authors.lastname: Loy
authors.forename: Michael
authors.initials: M
authors.lastname: Wagner
mesh_terms: D000818:Animals; D001439:Bacteroides / Q000502:physiology*; D017753:Ecosystem; D006801:Humans; D007422:Intestines / Q000382:microbiology*; D007553:Isotope Labeling; D054892:Metagenome / Q000502:physiology*; D051379:Mice