Autoinducer-2 plays a crucial role in gut colonization and probiotic functionality of Bifidobacterium breve UCC2003.

Steven E A Christiaen,Francesca Bottacini,Mary O'Connell Motherway,Tom Coenye,Noreen Lanigan,Hans J Nelis,Pat G Casey,Geert Huys,Douwe Van Sinderen,Christian U Riedel

doi:10.1371/journal.pone.0098111

Steven E A Christiaen, Francesca Bottacini + Show 8 more

Open Access

https://doi.org/10.1371/journal.pone.0098111

Copy DOI

Journal: PloS one	Publication Date: May 28, 2014
Citations: 143	License type: CC BY 4.0

Affiliation: University College Cork, Ghent University

Abstract

In the present study we show that luxS of Bifidobacterium breve UCC2003 is involved in the production of the interspecies signaling molecule autoinducer-2 (AI-2), and that this gene is essential for gastrointestinal colonization of a murine host, while it is also involved in providing protection against Salmonella infection in Caenorhabditis elegans. We demonstrate that a B. breve luxS-insertion mutant is significantly more susceptible to iron chelators than the WT strain and that this sensitivity can be partially reverted in the presence of the AI-2 precursor DPD. Furthermore, we show that several genes of an iron starvation-induced gene cluster, which are downregulated in the luxS-insertion mutant and which encodes a presumed iron-uptake system, are transcriptionally upregulated under in vivo conditions. Mutation of two genes of this cluster in B. breve UCC2003 renders the derived mutant strains sensitive to iron chelators while deficient in their ability to confer gut pathogen protection to Salmonella-infected nematodes. Since a functional luxS gene is present in all tested members of the genus Bifidobacterium, we conclude that bifidobacteria operate a LuxS-mediated system for gut colonization and pathogen protection that is correlated with iron acquisition.

Highlights

Various beneficial or probiotic effects have been attributed to strains belonging to the genera Bifidobacterium and Lactobacillus
In the present study we show that a functional luxS gene is widespread in the genus Bifidobacterium and that this gene in Bifidobacterium breve UCC2003 is involved in providing protection of Caenorhabditis elegans against Salmonella infection, a property which is linked to iron acquisition
Using Vibrio harveyi BB170 as a biosensor, we demonstrated that all (n = 59) Bifidobacterium spp. strains tested produce AI-2 during stationary phase planktonic growth (Table 1)

Summary

Introduction

Various beneficial or probiotic effects have been attributed to strains belonging to the genera Bifidobacterium and Lactobacillus. Probiotic bacteria have been used to treat, among others, antibiotic-associated diarrhea, food allergies, atopic eczema, inflammatory bowel disease and arthritis [1,2,3,4,5,6]. Whether probiotics need to adhere to epithelial cells of the human gut in order to exert their beneficial effect is still a matter of debate, but close contact between the two is required at some stage [13]. Bacterial adhesion to the gut epithelium is a complex process in which host, bacterial and environmental factors interact, and it is reasoned that adhesion and associated probiotic activities are regulated by bacterial cell-to-cell communication systems

Methods

Results

Conclusion