Changes in Gene Expression during Adaptation of Listeria monocytogenes to the Soil Environment

Piveteau, Pascal; Depret, Géraldine; Pivato, Barbara; Garmyn, Dominique; Hartmann, Alain

doi:10.1371/journal.pone.0024881

Cited by 47 publications

(59 citation statements)

References 45 publications

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“…These results strongly suggest that the 11 L. innocua genes are organized into an operon (Fig. 1), which is in good agreement with previously reported L. monocytogenes transcriptome data acquired during soil adaptation (37), where all genes, except for the pedB-like gene, were reported to be transiently upregulated after 15 and 30 min of adaptation to soil extracts or soil microcosms. During growth on glycerol to the late log phase, 7 of the 11 L. monocytogenes genes were also reported to be upregulated (26).…”

Section: Methodssupporting

confidence: 92%

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Novel Listerial Glycerol Dehydrogenase- and Phosphoenolpyruvate-Dependent Dihydroxyacetone Kinase System Connected to the Pentose Phosphate Pathway

Monniot¹,

Zébré²,

Aké³

et al. 2012

J. Bacteriol.

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ABSTRACTSeveral bacteria use glycerol dehydrogenase to transform glycerol into dihydroxyacetone (Dha). Dha is subsequently converted into Dha phosphate (Dha-P) by an ATP- or phosphoenolpyruvate (PEP)-dependent Dha kinase.Listeria innocuapossesses two potential PEP-dependent Dha kinases. One is encoded by 3 of the 11 genes forming the glycerol (gol) operon. This operon also containsgolD(lin0362), which codes for a new type of Dha-forming NAD+-dependent glycerol dehydrogenase. The subsequent metabolism of Dha requires its phosphorylation via the PEP:sugar phosphotransferase system components enzyme I, HPr, and EIIADha-2 (Lin0369). P∼EIIADha-2 transfers its phosphoryl group to DhaL-2, which phosphorylates Dha bound to DhaK-2. The resulting Dha-P is probably metabolized mainly via the pentose phosphate pathway, because two genes of thegoloperon encode proteins resembling transketolases and transaldolases. In addition, purified Lin0363 and Lin0364 exhibit ribose-5-P isomerase (RipB) and triosephosphate isomerase activities, respectively. The latter enzyme converts part of the Dha-P into glyceraldehyde-3-P, which, together with Dha-P, is metabolized via gluconeogenesis to form fructose-6-P. Together with another glyceraldehyde-3-P molecule, the transketolase transforms fructose-6-P into intermediates of the pentose phosphate pathway. Thegoloperon is preceded bygolR, transcribed in the opposite orientation and encoding a DeoR-type repressor. Its inactivation causes the constitutive but glucose-repressible expression of the entiregoloperon, including the last gene, encoding a pediocin immunity-like (PedB-like) protein. Its elevated level of synthesis in thegolRmutant causes slightly increased immunity against pediocin PA-1 compared to the wild-type strain or apedB-like deletion mutant.

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Section: Methodssupporting

confidence: 92%

“…Regarding the second question, we hypothesize that some listerial species probably fused the pedB-like gene to the gol operon because it is induced by glycerol during growth in soil (37). The organism producing the corresponding bacteriocin might therefore also be a soil bacterium.…”

Section: Methodsmentioning

confidence: 99%

Novel Listerial Glycerol Dehydrogenase- and Phosphoenolpyruvate-Dependent Dihydroxyacetone Kinase System Connected to the Pentose Phosphate Pathway

Monniot¹,

Zébré²,

Aké³

et al. 2012

J. Bacteriol.

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“…(53)(54)(55)(56). Indeed, the prevalence of nutrient acquisition mechanisms in the onset of soil adaptation has been reported previously (30). Similarly, modification of the bacterial cell surface is required for environmental adaptation and during growth and survival in soil (30,38,(57)(58)(59).…”

Section: Figmentioning

confidence: 73%

“…Indeed, the prevalence of nutrient acquisition mechanisms in the onset of soil adaptation has been reported previously (30). Similarly, modification of the bacterial cell surface is required for environmental adaptation and during growth and survival in soil (30,38,(57)(58)(59). Inactivation of AgrA could have prevented appropriate adjustment of the cell surface to the conditions of the environment.…”

Section: Figmentioning

confidence: 76%

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Survival of Listeria monocytogenes in Soil Requires AgrA-Mediated Regulation

Vivant

Garmyn

Gal

et al. 2015

Appl Environ Microbiol

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In this study, we investigated whether the Agr-mediated response is triggered during adaptation in soil, and we compared survival patterns in a set of 10 soils. The fate of the parental strain L. monocytogenes L9 (a rifampin-resistant mutant of L. monocytogenes EGD-e) and that of a ⌬agrA deletion mutant were compared in a collection of 10 soil microcosms. The ⌬agrA mutant displayed significantly reduced survival in these biotic soil microcosms, and differential transcriptome analyses showed large alterations of the transcriptome when AgrA was not functional, while the variations in the transcriptomes between the wild type and the ⌬agrA deletion mutant were modest under abiotic conditions. Indeed, in biotic soil environments, 578 protein-coding genes and an extensive repertoire of noncoding RNAs (ncRNAs) were differentially transcribed. The transcription of genes coding for proteins involved in cell envelope and cellular processes, including the phosphotransferase system and ABC transporters, and proteins involved in resistance to antimicrobial peptides was affected. Under sterilized soil conditions, the differences were limited to 86 genes and 29 ncRNAs. These results suggest that the response regulator AgrA of the Agr communication system plays important roles during the saprophytic life of L. monocytogenes in soil. Listeria monocytogenes is the causative agent of listeriosis, a serious foodborne infection affecting essentially immunocompromised individuals, the elderly, and pregnant women (1). The pathogen is largely spread in the environment. It has been isolated from water systems (2-4), vegetation (5), soil (6-8), farms (9-12), food industries (13-15), and the feces of animals (16-18). Environmental adaptation requires that the cell have the ability to integrate environmental cues in order to adapt its physiology to the surrounding conditions through the regulation of gene expression. Genomics showed that an important part of the L. monocytogenes genome (7.3%) is dedicated to regulation and includes 209 transcriptional regulators, 15 histidine kinases, and 16 response regulators constituting two-component systems (19). Two-component systems participate in the ability of bacteria to sense and respond to fluctuating environmental conditions. AgrC/AgrA is a two-component regulatory system that is part of the Agr communication system. Initially described in Staphylococcus aureus, this communication system is organized as a four-gene operon, agrBDCA. AgrB is a membrane-bound protein that processes the propeptide AgrD into a mature autoinducing peptide (AIP). Detection of AIP by the histidine kinase AgrC induces transcriptional regulation through activation of the regulator AgrA. Detailed data concerning the role of the Agr system in the physiology of S. aureus are available (20)(21)(22). So far, its role in the adaptation of L. monocytogenes to its environment is only partially understood (23). Reports show that the Agr communication system of L. monocytogenes is involved in adhesion to abiotic surfaces (24) in ...

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Application of Molecular and Sequencing Techniques in Analysis of Microbial Diversity in Agroecosystem

Parmar

Sharma

Kumar

2019

Microbial Genomics in Sustainable Agroecosystems

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Changes in Gene Expression during Adaptation of Listeria monocytogenes to the Soil Environment

Cited by 47 publications

References 45 publications

Novel Listerial Glycerol Dehydrogenase- and Phosphoenolpyruvate-Dependent Dihydroxyacetone Kinase System Connected to the Pentose Phosphate Pathway

Novel Listerial Glycerol Dehydrogenase- and Phosphoenolpyruvate-Dependent Dihydroxyacetone Kinase System Connected to the Pentose Phosphate Pathway

Survival of Listeria monocytogenes in Soil Requires AgrA-Mediated Regulation

Application of Molecular and Sequencing Techniques in Analysis of Microbial Diversity in Agroecosystem

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