Role and regulation of the stress activated sigma factor sigma B (σB) in the saprophytic and host-associated life stages of Listeria monocytogenes

Dorey, Amber; Marinho, Catarina; Piveteau, Pascal; O’Byrne, Conor

doi:10.1016/bs.aambs.2018.11.001

Cited by 45 publications

(36 citation statements)

References 189 publications

(293 reference statements)

Supporting

Mentioning

Contrasting

Order By: Relevance

“…These mutations most likely interfere with signal transduction through the σ B regulatory pathway since they are predicted to affect stressosome function (rsbS), dephosphorylation of the anti-anti sigma factor RsbV (rsbU, which encodes a phosphatase) or partner switching with the anti-sigma factor RsbW (rsbV). Indeed these data provide additional genetic support for the existing model for σ B activation in L. monocytogenes, reviewed in (49,50).…”

Section: Discussionsupporting

confidence: 62%

Mild Stress Conditions during Laboratory Culture Promote the Proliferation of Mutations That Negatively Affect Sigma B Activity in Listeria monocytogenes

Guerreiro

Dessaux

et al. 2020

J Bacteriol

View full text Add to dashboard Cite

In Listeria monocytogenes, the full details of how stress signals are integrated into the σB regulatory pathway are not yet available. To help shed light on this question, we investigated a collection of transposon mutants that were predicted to have compromised activity of the alternative sigma factor B (σB). These mutants were tested for acid tolerance, a trait that is known to be under σB regulation, and they were found to display increased acid sensitivity, similar to a mutant lacking σB (ΔsigB). The transposon insertions were confirmed by whole-genome sequencing, but in each case, the strains were also found to carry a frameshift mutation in the sigB operon. The changes were predicted to result in premature stop codons, with negative consequences for σB activation, independently of the transposon location. Reduced σB activation in these mutants was confirmed. Growth measurements under conditions similar to those used during the construction of the transposon library revealed that the frameshifted sigB operon alleles conferred a growth advantage at higher temperatures, during late exponential phase. Mixed-culture experiments at 42°C demonstrated that the loss of σB activity allowed mutants to take over a population of parental bacteria. Together, our results suggest that mutations affecting σB activity can arise during laboratory culture because of the growth advantage conferred by these mutations under mild stress conditions. The data highlight the significant cost of stress protection in this foodborne pathogen and emphasize the need for whole-genome sequence analysis of newly constructed strains to confirm the expected genotype. IMPORTANCE In the present study, we investigated a collection of Listeria monocytogenes strains that all carried sigB operon mutations. The mutants all had reduced σB activity and were found to have a growth advantage under conditions of mild heat stress (42°C). In mixed cultures, these mutants outcompeted the wild type when mild heat stress was present but not at an optimal growth temperature. An analysis of 22,340 published L. monocytogenes genome sequences found a high rate of premature stop codons present in genes positively regulating σB activity. Together, these findings suggest that the occurrence of mutations that attenuate σB activity can be favored under conditions of mild stress, probably highlighting the burden on cellular resources that stems from deploying the general stress response.

show abstract

Section: Discussionsupporting

confidence: 62%

Mild Stress Conditions during Laboratory Culture Promote the Proliferation of Mutations That Negatively Affect Sigma B Activity in Listeria monocytogenes

Guerreiro

Dessaux

et al. 2020

J Bacteriol

View full text Add to dashboard Cite

show abstract

“…We also review the acid tolerance mechanisms of Listeria monocytogenes, a Gram-positive rod that belongs to the division Firmicutes, which is very well studied for its role as an intracellular food-borne pathogen of humans and cattle. In nature, L. monocytogenes is a saprophyte and is characterized by its tolerance to stresses such as low pH, elevated osmolarity, and bile salts and its ability to grow at refrigeration temperatures [6][7][8]. While these bacteria are phylogenetically unrelated, they share the ability to enter the host via contaminated food or water, and therefore both can encounter the gastrointestinal environment, including the extreme acid conditions prevailing in the stomach, as part of their life cycles.…”

Section: Introductionmentioning

confidence: 99%

Comparative Review of the Responses of Listeria monocytogenes and Escherichia coli to Low pH Stress

Arcari

Feger

Guerreiro

et al. 2020

Genes

View full text Add to dashboard Cite

Acidity is one of the principal physicochemical factors that influence the behavior of microorganisms in any environment, and their response to it often determines their ability to grow and survive. Preventing the growth and survival of pathogenic bacteria or, conversely, promoting the growth of bacteria that are useful (in biotechnology and food production, for example), might be improved considerably by a deeper understanding of the protective responses that these microorganisms deploy in the face of acid stress. In this review, we survey the molecular mechanisms used by two unrelated bacterial species in their response to low pH stress. We chose to focus on two well-studied bacteria, Escherichia coli (phylum Proteobacteria) and Listeria monocytogenes (phylum Firmicutes), that have both evolved to be able to survive in the mammalian gastrointestinal tract. We review the mechanisms that these species use to maintain a functional intracellular pH as well as the protective mechanisms that they deploy to prevent acid damage to macromolecules in the cells. We discuss the mechanisms used to sense acid in the environment and the regulatory processes that are activated when acid is encountered. We also highlight the specific challenges presented by organic acids. Common themes emerge from this comparison as well as unique strategies that each species uses to cope with acid stress. We highlight some of the important research questions that still need to be addressed in this fascinating field.

show abstract

“…Stress-related gene sigB contributes to overcome different conditions encountered in foods such as acidic, osmotic, or oxidative stresses [12] and to the adaptation of the pathogen to HPP [13]. Moreover, it contributes to the transcription of the prfA virulence gene cluster, the major virulence genetic locus identified in L. monocytogenes [14], which exerts a positive control on some virulence factors, including plcA and hly genes.…”

Section: Introductionmentioning

confidence: 99%

Impact of Water Activity on the Inactivation and Gene Expression of Listeria monocytogenes during Refrigerated Storage of Pressurized Dry-Cured Ham

Pérez-Baltar¹,

Alía

Rodríguez

et al. 2020

Foods

View full text Add to dashboard Cite

Listeria monocytogenes population and the expression patterns of three virulence (plcA, hly, and iap) and one stress-related (sigB) genes in dry-cured ham with different water activity (aw) values (0.92, 0.88, and 0.84) and treated with high pressure processing (HPP, 450 MPa/10 min and 600 MPa/5 min) were monitored throughout 30 days (d) at 4 °C. The antimicrobial effect of HPP at 600 MPa against L. monocytogenes S4-2 (serotype 1/2b) and S12-1 (serotype 1/2c) was greater in dry-cured ham with aw values of 0.92, with reductions of 2.5 and 2.8 log units, respectively. The efficacy of HPP treatments decreased at lower aw values. Regarding gene expression, L. monocytogenes strains responded differently to HPP. For strain S4-2, the four target genes were generally overexpressed in dry-cured ham immediately after HPP treatments at the three aw values investigated, although the extent of this induction was lower in the samples pressurized at 600 MPa and with aw values of 0.84. For strain S12-1, the expression of all target genes was repressed at the three aw values investigated. The antimicrobial efficacy of HPP against L. monocytogenes could be compromised by low aw values in food products. However, no growth of HPP-survival cells was observed during refrigerated storage in low-aw dry-cured ham, and the overexpression of virulence and stress-related genes decreased.

show abstract

Role and regulation of the stress activated sigma factor sigma B (σB) in the saprophytic and host-associated life stages of Listeria monocytogenes

Cited by 45 publications

References 189 publications

Mild Stress Conditions during Laboratory Culture Promote the Proliferation of Mutations That Negatively Affect Sigma B Activity in Listeria monocytogenes

Mild Stress Conditions during Laboratory Culture Promote the Proliferation of Mutations That Negatively Affect Sigma B Activity in Listeria monocytogenes

Comparative Review of the Responses of Listeria monocytogenes and Escherichia coli to Low pH Stress

Impact of Water Activity on the Inactivation and Gene Expression of Listeria monocytogenes during Refrigerated Storage of Pressurized Dry-Cured Ham

Contact Info

Product

Resources

About