The Role of Sigma B (σB) in the Stress Adaptations of Listeria monocytogenes: Overlaps Between Stress Adaptation and Virulence

O’Byrne, Conor; Karatzas, Kimon-Andreas

doi:10.1016/s0065-2164(08)00605-9

Cited by 96 publications

(113 citation statements)

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“…Sigma B coordinates the transcription of genes required for the general stress response (33). To determine the stress responsiveness of hpf transcript abundance, we grew bacteria to mid-log phase and then exposed them to one of several stressful conditions for a period of 5 min.…”

Section: Monocytogenes Hpf Expression Is Stimulated By Starvation mentioning

confidence: 99%

The Listeria monocytogenes Hibernation-Promoting Factor Is Required for the Formation of 100S Ribosomes, Optimal Fitness, and Pathogenesis

et al. 2014

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During exposure to certain stresses, bacteria dimerize pairs of 70S ribosomes into translationally silent 100S particles in a process called ribosome hibernation. Although the biological roles of ribosome hibernation are not completely understood, this process appears to represent a conserved and adaptive response that contributes to optimal survival during stress and post-exponential-phase growth. Hibernating ribosomes are formed by the activity of one or more highly conserved proteins; gammaproteobacteria produce two relevant proteins, ribosome modulation factor (RMF) and hibernation promoting factor (HPF), while most Gram-positive bacteria produce a single, longer HPF protein. Here, we report the formation of 100S ribosomes by an HPF homolog in Listeria monocytogenes. L. monocytogenes 100S ribosomes were observed by sucrose density gradient centrifugation of bacterial extracts during mid-logarithmic phase, peaked at the transition to stationary phase, and persisted at lower levels during post-exponential-phase growth. 100S ribosomes were undetectable in bacteria carrying an hpf::Himar1 transposon insertion, indicating that HPF is required for ribosome hibernation in L. monocytogenes. Additionally, epitope-tagged HPF cosedimented with 100S ribosomes, supporting its previously described direct role in 100S formation. We examined hpf mRNA by quantitative PCR (qPCR) and identified several conditions that upregulated its expression, including carbon starvation, heat shock, and exposure to high concentrations of salt or ethanol. Survival of HPF-deficient bacteria was impaired under certain conditions both in vitro and during animal infection, providing evidence for the biological relevance of 100S ribosome formation. Listeria monocytogenes is a Gram-positive, food-borne, facultative intracellular pathogen that infects a broad range of vertebrate hosts (1, 2). The bacterium leads a saprophytic lifestyle in the environment and is commonly found in soil, water, and decaying organic matter. L. monocytogenes most commonly causes disease in elderly, immunocompromised, or pregnant individuals but can pose a general public health risk in cases of severe food contamination. Because of its ability to shift quickly between saprophytic growth in the environment and potentially lethal pathogenesis upon contacting a host, L. monocytogenes has been referred to as a bacterial "Dr. Jekyll and Mr. Hyde" (3). The ability to tolerate or thrive in a variety of unfavorable conditions, including high salt, low pH, and refrigeration temperatures, has made L. monocytogenes a formidable challenge to the food industry (1, 2). Therefore, it is important to understand the set of factors that enable L. monocytogenes to survive so effectively in a wide variety of inhospitable environments. Some of these factors are involved in conserved bacterial stress responses, while others may be specific to Listeria spp. and their close relatives (4).Ribosome hibernation is thought to be an alternative to the classical ribosome recycling pathway, shunting r...

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Section: Monocytogenes Hpf Expression Is Stimulated By Starvation mentioning

confidence: 99%

The Listeria monocytogenes Hibernation-Promoting Factor Is Required for the Formation of 100S Ribosomes, Optimal Fitness, and Pathogenesis

et al. 2014

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“…The general stress response alternative s factor s B is an important transcriptional regulator in the facultative intracellular pathogen Listeria monocytogenes (O'Byrne & Karatzas, 2008). L. monocytogenes is not only the causative agent of listeriosis, a life-threatening foodborne infection in humans and animals, but is also commonly found in many non-host environments and has the ability to survive under a variety of environmental stress conditions that are lethal to other bacteria.…”

Section: Introductionmentioning

confidence: 99%

“…L. monocytogenes is not only the causative agent of listeriosis, a life-threatening foodborne infection in humans and animals, but is also commonly found in many non-host environments and has the ability to survive under a variety of environmental stress conditions that are lethal to other bacteria. s B contributes to the resistance of L. monocytogenes to different stress conditions, including acid, osmotic and energy stress, and also plays an important role in survival during stationary phase (O'Byrne & Karatzas, 2008). s B has also been shown to directly regulate transcription of some virulence genes as well as other genes that contribute to L. monocytogenes growth and survival during gastrointestinal passage as well as intracellular survival and replication (Chaturongakul et al, 2008;Garner et al, 2006;Kazmierczak et al, 2005;van Schaik & Abee, 2005).…”

Section: Introductionmentioning

confidence: 99%

Refinement of the Listeria monocytogenes σB regulon through quantitative proteomic analysis

et al. 2013

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“…A variety of stress and virulence-related phenotypes are associated with loss of the sigB gene, indicating that s B plays an important role both during infections and under stressful conditions (reviewed by O'Byrne, 2008). 5 After the full genome sequence of L. monocytogenes became available 6 a number of studies identified components of the s B regulon by looking at genes differentially expressed in L. monocytogenes wild-type and corresponding sigB mutants using proteomic approaches 7,8 or gene microarray technology. [9][10][11][12] The mechanism responsible for sensing stress that leads to the activation of s B has not been fully characterized in L. monocytogenes.…”

Section: Introductionmentioning

confidence: 99%

Development and optimization of an EGFP-based reporter for measuring the general stress response inListeria monocytogenes

et al. 2012

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A characteristic of the food-borne pathogen Listeria monocytogenes is its tolerance to the harsh conditions found both in minimally processed foods and the human gastrointestinal tract. This trait is partly under the control of the alternative sigma factor sigma B (s B ). To study the mechanisms that trigger the activation of s B , and hence the development of stress tolerance, we have developed a fluorescent reporter fusion that allows the real-time activity of s B to be monitored. The reporter, designated P lmo2230 ::egfp, fuses the strong s B -dependent promoter from the lmo2230 gene (which encodes a putative arsenate reductase) to a gene encoding enhanced green fluorescence protein (EGFP). The reporter was integrated into the genomes of the wild-type strain L. monocytogenes EGD-e as well as two mutant derivatives lacking either sigB or rsbV. The resulting strains were used to study s B activation in response to growth phase and hyperosmotic stress. The wild-type was strongly fluorescent in stationary phase or in cultures with added NaCl and this fluorescence was abolished in both the sigB and rsbV backgrounds, consistent with the s B -dependency of the lmo2230 promoter. During sudden osmotic upshock (addition of 0.5 M NaCl during growth) a real-time increase in fluorescence was observed microscopically, reaching maximal activation after 30 min. Flow cytometry was used to study the activation of s B at a population level by hyperosmotic stress during exponential growth. A strong and proportional increase in fluorescence was observed as the salt concentration increased from 0 to 0.9 M NaCl. Interestingly, there was considerable heterogeneity within the population and a significant proportion of cells failed to induce a high level of fluorescence, suggesting that s B activation occurs stochastically in response to hyperosmotic stress. Thus the P lmo2230 ::egfp is a powerful tool that will allow the stress response to be better studied in this important human pathogen.

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The Role of Sigma B (σB) in the Stress Adaptations of Listeria monocytogenes: Overlaps Between Stress Adaptation and Virulence

Cited by 96 publications

References 94 publications

The Listeria monocytogenes Hibernation-Promoting Factor Is Required for the Formation of 100S Ribosomes, Optimal Fitness, and Pathogenesis

The Listeria monocytogenes Hibernation-Promoting Factor Is Required for the Formation of 100S Ribosomes, Optimal Fitness, and Pathogenesis

Refinement of the Listeria monocytogenes σB regulon through quantitative proteomic analysis

Development and optimization of an EGFP-based reporter for measuring the general stress response inListeria monocytogenes

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