Like Will to Like: Abundances of Closely Related Species Can Predict Susceptibility to Intestinal Colonization by Pathogenic and Commensal Bacteria
Open Access
- 8 January 2010
- journal article
- research article
- Published by Public Library of Science (PLoS) in PLoS Pathogens
- Vol. 6 (1), e1000711
- https://doi.org/10.1371/journal.ppat.1000711
Abstract
The intestinal ecosystem is formed by a complex, yet highly characteristic microbial community. The parameters defining whether this community permits invasion of a new bacterial species are unclear. In particular, inhibition of enteropathogen infection by the gut microbiota ( = colonization resistance) is poorly understood. To analyze the mechanisms of microbiota-mediated protection from Salmonella enterica induced enterocolitis, we used a mouse infection model and large scale high-throughput pyrosequencing. In contrast to conventional mice (CON), mice with a gut microbiota of low complexity (LCM) were highly susceptible to S. enterica induced colonization and enterocolitis. Colonization resistance was partially restored in LCM-animals by co-housing with conventional mice for 21 days (LCMcon21). 16S rRNA sequence analysis comparing LCM, LCMcon21 and CON gut microbiota revealed that gut microbiota complexity increased upon conventionalization and correlated with increased resistance to S. enterica infection. Comparative microbiota analysis of mice with varying degrees of colonization resistance allowed us to identify intestinal ecosystem characteristics associated with susceptibility to S. enterica infection. Moreover, this system enabled us to gain further insights into the general principles of gut ecosystem invasion by non-pathogenic, commensal bacteria. Mice harboring high commensal E. coli densities were more susceptible to S. enterica induced gut inflammation. Similarly, mice with high titers of Lactobacilli were more efficiently colonized by a commensal Lactobacillus reuteri RR strain after oral inoculation. Upon examination of 16S rRNA sequence data from 9 CON mice we found that closely related phylotypes generally display significantly correlated abundances (co-occurrence), more so than distantly related phylotypes. Thus, in essence, the presence of closely related species can increase the chance of invasion of newly incoming species into the gut ecosystem. We provide evidence that this principle might be of general validity for invasion of bacteria in preformed gut ecosystems. This might be of relevance for human enteropathogen infections as well as therapeutic use of probiotic commensal bacteria. The commensal microbiota, populating the intestinal tract to high levels, is fundamental to human health. It exerts beneficial effects on the immune system and contributes to protection against gastrointestinal infections ( = colonization resistance) by largely unknown mechanisms. Here, we reveal characteristics of the commensal microbiota indicative for a high or low degree of colonization resistance. Using a mouse model for Salmonella enterica induced gut inflammation and microbiota analysis by 454 amplicon sequencing, we show that mice having different types of microbiota exhibit differential susceptibility to pathogen infection. In addition, our data lead to the description of a new concept in gut ecosystem biology: the intrusion-success of an extrinsic bacterial species into an established gut ecosystem is related to the abundance of closely related bacteria, already present in this gut ecosystem. We show that this principle applies not only to enteropathogen infection but also to inoculation with beneficial gut bacteria. Humans can display largely different degrees of susceptibility to enteric infections. Similarly, the effectiveness of probiotic therapy varies greatly from person to person. Our data might explain these differences and could be used for increasing the efficacy of probiotic therapy and for identifying patients at risk of developing enteric infections.Keywords
This publication has 74 references indexed in Scilit:
- Wrinkles in the rare biosphere: pyrosequencing errors can lead to artificial inflation of diversity estimatesEnvironmental Microbiology, 2009
- A core gut microbiome in obese and lean twinsNature, 2008
- The Ribosomal Database Project: improved alignments and new tools for rRNA analysisNucleic Acids Research, 2008
- Evolution of Mammals and Their Gut MicrobesScience, 2008
- Microbe sampling by mucosal dendritic cells is a discrete, MyD88-independent stepin ΔinvG S. Typhimurium colitisThe Journal of Experimental Medicine, 2008
- Naïve Bayesian Classifier for Rapid Assignment of rRNA Sequences into the New Bacterial TaxonomyApplied and Environmental Microbiology, 2007
- MyD88-mediated signals induce the bactericidal lectin RegIIIγ and protect mice against intestinal Listeria monocytogenes infectionThe Journal of Experimental Medicine, 2007
- New Screening Software Shows that Most Recent Large 16S rRNA Gene Clone Libraries Contain ChimerasApplied and Environmental Microbiology, 2006
- Symbiotic Bacteria Direct Expression of an Intestinal Bactericidal LectinScience, 2006
- Microbial diversity in the deep sea and the underexplored “rare biosphere”Proceedings of the National Academy of Sciences of the United States of America, 2006