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

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.

SUBMITTER: Kelly SM

PROVIDER: S-EPMC7360559 | biostudies-literature | 2020 Jul

REPOSITORIES: biostudies-literature

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

Kelly Sandra M SM Lanigan Noreen N O'Neill Ian J IJ Bottacini Francesca F Lugli Gabriele Andrea GA Viappiani Alice A Turroni Francesca F Ventura Marco M van Sinderen Douwe D

Scientific reports 20200714 1

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 trans ...[more]

PMID: 32665665

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Project description:UnlabelledBiofilms are thought to play an important role during colonization of the nasopharynx by Streptococcus pneumoniae, yet how they form in vivo and the determinants responsible remain unknown. Using scanning electron microscopy, we show that biofilm aggregates of increasing complexity form on murine nasal septa following intranasal inoculation. These biofilms were highly distinct from in vitro biofilms, as they were discontiguous and appeared to incorporate nonbacterial components such as intact host cells. Biofilms initially formed on the surface of ciliated epithelial cells and, as cells were sloughed off, were found on the basement membrane. The size and number of biofilm aggregates within nasal lavage fluid were digitally quantitated and revealed strain-specific capabilities that loosely correlated with the ability to form robust in vitro biofilms. We tested the ability of isogenic mutants deficient in CbpA, pneumolysin, hydrogen peroxide, LytA, LuxS, CiaR/H, and PsrP to form biofilms within the nasopharynx. This analysis revealed that CiaR/H was absolutely required for colonization, that PsrP and SpxB strongly impacted aggregate formation, and that other determinants affected aggregate morphology in a modest fashion. We determined that mice colonized with ΔpsrP mutants had greater levels of the proinflammatory cytokines tumor necrosis factor alpha (TNF-α), interleukin-6 (IL-6), IL-1β, and KC in nasal lavage fluid than did mice colonized with wild-type controls. This phenotype correlated with a diminished capacity of biofilm pneumococci to invade host cells in vitro despite enhanced attachment. Our results show that biofilms form during colonization and suggest that they may contribute to persistence through a hyperadhesive, noninvasive state that elicits a dampened cytokine response.ImportanceThis work demonstrates the first temporal characterization of Streptococcus pneumoniae biofilm formation in vivo. Our results show that the morphology of biofilms formed by both invasive and noninvasive clinical isolates in vivo is distinct from that of formed biofilms in vitro, yet propensity to form biofilms in vivo loosely correlates with the degree of in vitro biofilm formation on a microtiter plate. We show that host components, including intact host cells, influence the formation of in vivo structures. We also found that efficient biofilm formation in vivo requires multiple bacterial determinants. While some factors are essential for in vivo biofilm formation (CiaRH, PsrP, and SpxB), other factors are less critical (CbpA, LytA, LuxS, and pneumolysin). In comparison to their planktonic counterparts, biofilm pneumococci are hyperadhesive but less invasive and elicit a weaker proinflammatory cytokine response. These findings give insight into the requirements for and potential role of biofilms during prolonged asymptomatic colonization.

Dataset Information

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

Publications

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

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