Genome-wide transcriptional profiling of the cell envelope stress response and the role of LisRK and CesRK in Listeria monocytogenes

Andersen, Ann Zahle; Mols, Maarten; Veen, Stijn van der; Abee, Tjakko; Kallipolitis, Birgitte H.

doi:10.1099/mic.0.055467-0

Cited by 49 publications

(81 citation statements)

References 58 publications

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“…One can easily envision the glp gene products being part of this scenario, given that glycerol-3-phosphate is required for synthesis of the phospholipid precursor phosphatidic acid (121), in addition to being an alternate carbon source (12). It is worth noting that links between TCS and remodeling of the bacterial cell envelope in stressful milieus are well documented, with Cpx in E. coli, PhoPQ in Salmonella enterica serovar Typhimurium, and MprAB in Mycobacterium tuberculosis being among the best-characterized examples (122)(123)(124)(125)(126)(127)(128).…”

Section: Discussionmentioning

confidence: 99%

Cyclic di-GMP Modulates Gene Expression in Lyme Disease Spirochetes at the Tick-Mammal Interface To Promote Spirochete Survival during the Blood Meal and Tick-to-Mammal Transmission

et al. 2015

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e Borrelia burgdorferi, the Lyme disease spirochete, couples environmental sensing and gene regulation primarily via the Hk1/ Rrp1 two-component system (TCS) and Rrp2/RpoN/RpoS pathways. Beginning with acquisition, we reevaluated the contribution of these pathways to spirochete survival and gene regulation throughout the enzootic cycle. Live imaging of B. burgdorferi caught in the act of being acquired revealed that the absence of RpoS and the consequent derepression of tick-phase genes impart a Stay signal required for midgut colonization. In addition to the behavioral changes brought on by the RpoS-off state, acquisition requires activation of cyclic di-GMP (c-di-GMP) synthesis by the Hk1/Rrp1 TCS; B. burgdorferi lacking either component is destroyed during the blood meal. Prior studies attributed this dramatic phenotype to a metabolic lesion stemming from reduced glycerol uptake and utilization. In a head-to-head comparison, however, the B. burgdorferi ⌬glp mutant had a markedly greater capacity to survive tick feeding than B. burgdorferi ⌬hk1 or ⌬rrp1 mutants, establishing unequivocally that glycerol metabolism is only one component of the protection afforded by c-di-GMP. Data presented herein suggest that the protective response mediated by c-di-GMP is multifactorial, involving chemotactic responses, utilization of alternate substrates for energy generation and intermediary metabolism, and remodeling of the cell envelope as a means of defending spirochetes against threats engendered during the blood meal. Expression profiling of c-di-GMP-regulated genes through the enzootic cycle supports our contention that the Hk1/Rrp1 TCS functions primarily, if not exclusively, in ticks. These data also raise the possibility that c-di-GMP enhances the expression of a subset of RpoS-dependent genes during nymphal transmission. Borrelia burgdorferi, the causative agent of Lyme disease, is maintained in nature within an enzootic cycle that involves an arthropod vector and vertebrate reservoir hosts, typically, small rodents and birds (1). In the northeastern United States, the primary vector for B. burgdorferi is the black-legged deer tick, Ixodes scapularis (2, 3). Because B. burgdorferi cannot be passaged transovarially, naive larvae acquire spirochetes by feeding on infected reservoir hosts. Successful colonization of the vector requires B. burgdorferi to establish an intimate association with rapidly differentiating, highly endocytic midgut epithelial cells (4-6). In order to accomplish this feat, spirochetes must resist deleterious substances within the midgut lumen, such as host-and tick-derived innate immune effector molecules, reactive oxygen species (ROS), and salivary enzymes imbibed from the feeding site (4, 7-11). At the same time, B. burgdorferi also must alter its metabolic machinery to exploit the availability of alternative carbon sources (e.g., glycerol, N-acetylglucosamine [GlcNAc], chitobiose) as the supply of ingested glucose diminishes (12-15). During nymphal transmission, spirochetes are almost certai...

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Section: Discussionmentioning

confidence: 99%

Cyclic di-GMP Modulates Gene Expression in Lyme Disease Spirochetes at the Tick-Mammal Interface To Promote Spirochete Survival during the Blood Meal and Tick-to-Mammal Transmission

et al. 2015

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“…Gene ftsE in L. monocytogenes is regulated by B (31), which is a general stress response regulator. Various stresses, such as liquid smoke (32), cold (33), antibiotic (31,34), and heat (35), also downregulate fts genes in Listeria. The up-or downregulation of fts genes may depend on the type of stress and time of exposure.…”

Section: Discussionmentioning

confidence: 99%

Stress Response and Adaptation of Listeria monocytogenes 08-5923 Exposed to a Sublethal Dose of Carnocyclin A

Liu

Basu

Miller

et al. 2014

Appl Environ Microbiol

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Carnocyclin A (CCLA) is an antimicrobial peptide produced by Carnobacterium maltaromaticum ATCC PTA-5313, which can be used to control the growth of Listeria monocytogenes in ready-to-eat meat products. The aim of this research was to elucidate the cellular responses of L. monocytogenes 08-5923 exposed to a sublethal dose of CCLA. Microarray, quantitative reverse transcription-PCR, tandem mass spectrometry, and electron microscopy were used to investigate the alteration in gene expression, protein production, and morphological changes in cells of Listeria following treatment with CCLA. The genes involved in metabolism (baiE, trn, and pykA), cell wall synthesis (murZ and dacB2), and cell division (clpE and divIVA) were upregulated following a 15-min exposure to CCLA as a result of stress responses. Genes involved in cell division, cell wall synthesis, flagellar synthesis, and metabolism were downregulated after 4 h as a result of adaptation. Analysis of total soluble proteins confirmed the downregulation of pykA and gnd after 4 h of exposure to CCLA. The absence of flagella was observed in L. monocytogenes following 30 h of exposure to CCLA. A sublethal dose of CCLA induced adaptation in L. monocytogenes 08-5923 by inhibition of expression of genes and proteins critical for synthesis of cell wall structures and maintaining metabolic functions. Both the mannose-and cellobiose-specific phosphotransferase systems could be targets for CCLA.

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“…LisK has been proposed to positively regulate htrA (lmo0292), encoding a serine protease (46); lmo2229, encoding the penicillin-binding protein PBPA2; and lmo1021, encoding an HK (43). LisK is thus probably involved in cell envelope-related stress (47,48). The failure to complement the ⌬lisK mutation at low temperature could be explained by the intentional integration of pPL2 into a chromosomal target position at the tRNA Arg prophage attachment site in the EGD-e genome (37).…”

Section: Figmentioning

confidence: 99%

Two-Component-System Histidine Kinases Involved in Growth of Listeria monocytogenes EGD-e at Low Temperatures

Pöntinen

Markkula

Lindström

et al. 2015

Appl Environ Microbiol

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Two-component systems (TCSs) aid bacteria in adapting to a wide variety of stress conditions. While the role of TCS response regulators in the cold tolerance of the psychrotrophic foodborne pathogen Listeria monocytogenes has been demonstrated previously, no comprehensive studies showing the role of TCS histidine kinases of L. monocytogenes at low temperature have been performed. We compared the expression levels of each histidine kinase-encoding gene of L. monocytogenes EGD-e in logarithmic growth phase at 3°C and 37°C, as well as the expression levels 30 min, 3 h, and 7 h after cold shock at 5°C and preceding cold shock (at 37°C). We constructed a deletion mutation in each TCS histidine kinase gene, monitored the growth of the EGD-e wild-type and mutant strains at 3°C and 37°C, and measured the minimum growth temperature of each strain. Two genes, yycG and lisK, proved significant in regard to induced relative expression levels under cold conditions and cold-sensitive mutant phenotypes. Moreover, the ⌬resE mutant showed a lower growth rate than that of wild-type EGD-e at 3°C. Eleven other genes showed upregulated gene expression but revealed no cold-sensitive phenotypes. The results show that the histidine kinases encoded by yycG and lisK are important for the growth and adaptation of L. monocytogenes EGD-e at low temperature. Listeria monocytogenes is a low-GϩC, Gram-positive, nonspore-forming coccobacillus ubiquitously found in the environment (1, 2). It has been isolated from foods and food-processing premises, where it has been confirmed to be able to persist for several years (3-7). L. monocytogenes is the causative agent of listeriosis, with a reported annual incidence of approximately 0.3 case per 100,000 population in the United States and 0.2 to 0.8 case per 100,000 population in Europe (8-10). Although relatively rare, listeriosis is nevertheless a severe foodborne disease with a mortality of up to 20 to 30% (1,8,11,12). L. monocytogenes surmounts a wide range of stress conditions and is able to grow at temperatures as low as Ϫ0.4°C (13). This sets critical challenges for the modern food industry, since L. monocytogenes is consequently able to grow in ready-to-eat foods with a long shelf-life and in products stored at refrigeration temperatures. Thus, it is crucial to study and elucidate the factors enhancing the cold tolerance of L. monocytogenes. Two-component regulatory signaling systems (TCSs) are among the major systems that aid bacteria in adapting to many arduous stress factors encountered in nature and during food processing. A typical TCS is constituted of a transmembrane sensor histidine kinase (HK) and a cognate cytoplasmic response regulator (RR) (14-17). The signaling pathway of the TCS is based on protein phosphorylation. In the simplest form of signal transduction, the sensor domain of the HK detects a specific stimulus or stress factor in cells or in their environment. This leads to the autophosphorylation of a specific His residue in the HK dimerization domain. The cognate RR then ca...

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Genome-wide transcriptional profiling of the cell envelope stress response and the role of LisRK and CesRK in Listeria monocytogenes

Cited by 49 publications

References 58 publications

Cyclic di-GMP Modulates Gene Expression in Lyme Disease Spirochetes at the Tick-Mammal Interface To Promote Spirochete Survival during the Blood Meal and Tick-to-Mammal Transmission

Cyclic di-GMP Modulates Gene Expression in Lyme Disease Spirochetes at the Tick-Mammal Interface To Promote Spirochete Survival during the Blood Meal and Tick-to-Mammal Transmission

Stress Response and Adaptation of Listeria monocytogenes 08-5923 Exposed to a Sublethal Dose of Carnocyclin A

Two-Component-System Histidine Kinases Involved in Growth of Listeria monocytogenes EGD-e at Low Temperatures

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