Bifidobacterial biofilm formation is a multifactorial adaptive phenomenon in response to bile exposure

Sandra M Kelly,Ian J O’Neill,Alice Viappiani,Marco Ventura,Gabriele Andrea Lugli,Francesca Bottacini,Douwe Van Sinderen,Francesca Turroni,Noreen Lanigan

doi:10.1038/s41598-020-68179-9

Sandra M Kelly, Ian J O’Neill + Show 7 more

Open Access

https://doi.org/10.1038/s41598-020-68179-9

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Abstract

In the current study, we show that biofilm formation by various strains and species belonging to Bifidobacterium, a genus that includes gut commensals with reported health-promoting activities, is induced by high concentrations of bile (0.5% (w/v) or higher) and individual bile salts (20 mM or higher), rather than by acid or osmotic stress. The transcriptomic response of a bifidobacterial prototype Bifidobacterium breve UCC2003 to such high bile concentrations was investigated and a random transposon bank of B. breve UCC2003 was screened for mutants that affect biofilm formation in order to identify genes involved in this adaptive process. Eleven mutants affected in their ability to form a biofilm were identified, while biofilm formation capacity of an insertional mutation in luxS and an exopolysaccharide (EPS) negative B. breve UCC2003 was also studied. Reduced capacity to form biofilm also caused reduced viability when exposed to porcine bile. We propose that bifidobacterial biofilm formation is an adaptive response to high concentrations of bile in order to avoid bactericidal effects of high bile concentrations in the gastrointestinal environment. Biofilm formation appears to be a multi-factorial process involving EPS production, proteins and extracellular DNA release, representing a crucial strategy in response to bile stress in order to enhance fitness in the gut environment.

Highlights

In the current study, we show that biofilm formation by various strains and species belonging to Bifidobacterium, a genus that includes gut commensals with reported health-promoting activities, is induced by high concentrations of bile (0.5% (w/v) or higher) and individual bile salts (20 mM or higher), rather than by acid or osmotic stress
Using the prototype bifidobacterial gut commensal B. breve UCC2003 it was shown that biofilm formation occurs following bile exposure
Because bile concentrations fluctuate throughout the gastrointestinal tract (GIT), we wanted to assess if biofilm formation is induced by other conditions pertinent to the intestinal environment and to what extent this occurs by varying porcine bile concentrations (Fig. 1)

Summary

Introduction

We show that biofilm formation by various strains and species belonging to Bifidobacterium, a genus that includes gut commensals with reported health-promoting activities, is induced by high concentrations of bile (0.5% (w/v) or higher) and individual bile salts (20 mM or higher), rather than by acid or osmotic stress. Biofilm formation appears to be a multi-factorial process involving EPS production, proteins and extracellular DNA release, representing a crucial strategy in response to bile stress in order to enhance fitness in the gut environment. Bile has previously been shown to induce biofilm formation in certain gut commensals, such as particular species/strains of Bacteroides, bifidobacteria and lactobacilli[34–36]. It is important to study biofilm formation in commensal strains, such as bifidobacteria, and to obtain insights into how they adjust to and survive bile stress, and how this contributes to gut colonisation

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