How do bifidobacteria counteract environmental challenges? Mechanisms involved and physiological consequences

Abstract

An effective response to stress is of paramount importance for probiotic bifidobacteria administered in foods, since it determines their performance as beneficial microorganisms. Firstly, bifidobacteria have to be resistant to the stress sources typical in manufacturing, including heating, exposure to low water activities, osmotic shock and presence of oxygen. Secondly, and once they are orally ingested, bifidobacteria have to overcome physiological barriers in order to arrive in the large intestine biologically active. These barriers are mainly the acid pH in the stomach and the presence of high bile salt concentrations in the small intestine. In addition, the large intestine is, in terms of microbial amounts, a densely populated environment in which there is an extreme variability in carbon source availability. For this reason, bifidobacteria harbours a wide molecular machinery allowing the degradation of a wide variety of otherwise non-digestible sugars. In this review, the molecular mechanisms allowing this bacterial group to favourably react to the presence of different stress sources are presented and discussed.

Fig. 1

Schematic representation summarizing the different stress sources, stress treatments and the techniques employed for the study of their effects on bifidobacteria. Upper panel, stress sources can be classified into two groups, technological or gastrointestinal. Middle panel, relating to the duration of the treatment, a short exposure, cell growth for a given time, or long-time exposure to the stress may lead to a stable (or transient) phenotype of resistance. Lower panel, different strategies used to study stress responses in Bifidobacterium strains

Fig. 2

Main molecular mechanisms involved in the response of bifodobacteria to different stresses. a Bile is detoxified from the cytoplasm by the activity of bile efflux pumps and/or multidrug transporters. Conjugated bile acids are deconjugated by the bile salt hydrolase (BSH), although the relationship of this enzyme with the resistance to bile is unclear. b Finally, both bile and heat shock induce protein aggregation and misfolding, which is counteracted by the action of chaperones and proteases. c The F₁F₀-ATPase is used by bifidobacteria for counteracting the cytoplasm acidification that occurs in acidic environments. In addition, production of branched-chain amino acids is coupled with glutamine deamination, rendering ammonia that acts as a cytoplasmic buffer

Fig. 3

Schematic representation of the stress gene regulatory network proposed for B. breve UCC2003. Dotted lines indicate the predicted interaction, and closed lines indicate a proven interaction. A dash at the end of a line indicates repression, while a triangle at the end of a line indicates activation. Connections between the various regulons occur at different levels, which is indicative of complex interactions. [Reproduced with ASM press permission, Copyright 2009; from [105]