Salmonella Utilizes D-Glucosaminate via a Mannose Family Phosphotransferase System Permease and Associated Enzymes

Miller, Katherine A.; Phillips, Robert S.; Mrázek, Jan; Hoover, Timothy R.

doi:10.1128/jb.00290-13

Cited by 28 publications

(35 citation statements)

References 71 publications

Supporting

Mentioning

Contrasting

Order By: Relevance

“…For example, the PTS Man transports mannose, glucose, and in some bacteria also several other carbohydrates albeit with low efficiency. This PTS family shows the greatest variability in transported substrates; its members also catalyze the uptake of less-common carbon sources such as gluconate (7), D-glucosaminate (8), sorbose (9), D-ribitol (10), lacto-N-biose, and galacto-N-biose (11).…”

mentioning

confidence: 99%

Interaction with Enzyme IIB^Mpo(EIIB^Mpo) and Phosphorylation by Phosphorylated EIIB^MpoExert Antagonistic Effects on the Transcriptional Activator ManR of Listeria monocytogenes

et al. 2015

View full text Add to dashboard Cite

Listeriae take up glucose and mannose predominantly through a mannose class phosphoenolpyruvate:carbohydrate phosphotransferase system (PTS Man ), whose three components are encoded by the manLMN genes. Mpo and PϳPRD2 of ManR, which together lead to the induction of the manLMN operon. Complementation of a ⌬manR mutant with various manR alleles confirmed the antagonistic effects of PTS-catalyzed phosphorylation at the two different histidine residues of ManR. Deletion of manR prevented not only the expression of the manLMN operon but also glucose-mediated repression of virulence gene expression; however, repression by other carbohydrates was unaffected. Interestingly, the expression of manLMN in Listeria innocua was reported to require not only ManR but also the Crp-like transcription activator Lin0142. Unlike Lin0142, the L. monocytogenes homologue, Lmo0095, is not required for manLMN expression; its absence rather stimulates man expression. IMPORTANCEListeria monocytogenes is a human pathogen causing the foodborne disease listeriosis. The expression of most virulence genes is controlled by the transcription activator PrfA. Its activity is strongly repressed by carbohydrates, including glucose, which is transported into L. monocytogenes mainly via a mannose/glucose-specific phosphotransferase system (PTS Man ). Expression of the man operon is regulated by the transcription activator ManR, the activity of which is controlled by a second, low-efficiency PTS of the mannose family, which functions as glucose sensor. Here we demonstrate that the EIIB Mpo component plays a dual role in ManR regulation: it inactivates ManR by phosphorylating its His871 residue and stimulates ManR by interacting with its two C-terminal domains. Glucose is recognized as a preferred carbon source for numerous bacteria. When multiple carbohydrates are present in a growth medium, glucose represses the synthesis of the enzymes required for the utilization of other carbon sources and is therefore the first to be transported and metabolized. This phenomenon is known as carbon catabolite repression. Glucose is taken up by bacterial cells either by ion-driven permeases, such as GlcP (1) and GlcU (2), or via the phosphoenolpyruvate (PEP):glycose phosphotransferase system (PTS), with the latter being the most common bacterial glucose transporter. The PTS is composed of four proteins or protein domains, which form a phosphorylation cascade, and one or two membrane-spanning proteins (3). The phosphorylation cascade starts with the PEP-requiring autophosphorylation of a histidyl residue in enzyme I (EI) (4). Phosphorylated EI (PϳEI) then transfers the phosphoryl group to histidine 15 in HPr, the second general PTS protein (Fig. 1). In the next step, PϳHis-HPr phosphorylates a histidyl residue in a carbohydrate-specific EIIA component; bacteria usually contain several EIIA components. PϳEIIA subsequently phosphorylates a cysteyl or histidyl residue in the EIIB component of the same

show abstract

mentioning

confidence: 99%

Interaction with Enzyme IIB^Mpo(EIIB^Mpo) and Phosphorylation by Phosphorylated EIIB^MpoExert Antagonistic Effects on the Transcriptional Activator ManR of Listeria monocytogenes

et al. 2015

View full text Add to dashboard Cite

show abstract

“…The latter is a monomer which results from the breakdown of pectic polymers (34). Furthermore, Goudeau et al reported that genes involved in the uptake of gluconate and idonate (metabolized via the Entner-Doudoroff pathway) were upregulated in Salmonella grown on lettuce leaf macerate caused by D. dadantii (12,(33)(34)(35).…”

Section: Figmentioning

confidence: 99%

“…Eda is involved in the conversion of the phosphorylated KDG molecule (KDPG) into pyruvate and glyceraldehyde-3-phosphate, which feeds into the tricarboxylic acid (TCA) cycle. It has been reported that eda is important for growth of Salmonella on D-gluconate and D-glucuronate (33). The latter is a monomer which results from the breakdown of pectic polymers (34).…”

Section: Figmentioning

confidence: 99%

Contribution of the Salmonella enterica KdgR Regulon to Persistence of the Pathogen in Vegetable Soft Rots

George

González

Lorca

et al. 2016

Appl Environ Microbiol

View full text Add to dashboard Cite

bDuring their colonization of plants, human enteric pathogens, such as Salmonella enterica, are known to benefit from interactions with phytopathogens. At least in part, benefits derived by Salmonella from the association with a soft rot caused by Pectobacterium carotovorum were shown to be dependent on Salmonella KdgR, a regulator of genes involved in the uptake and utilization of carbon sources derived from the degradation of plant polymers. A Salmonella kdgR mutant was more fit in soft rots but not in the lesions caused by Xanthomonas spp. and Pseudomonas spp. Bioinformatic, phenotypic, and gene expression analyses demonstrated that the KdgR regulon included genes involved in uptake and metabolism of molecules resulting from pectin degradation as well as those central to the utilization of a number of other carbon sources. Mutant analyses indicated that the Entner-Doudoroff pathway, in part controlled by KdgR, was critical for the persistence within soft rots and likely was responsible for the kdgR phenotype.

show abstract

mentioning

confidence: 99%

“…One of these activators, DgaR, regulates expression of the dgaABCDEF operon, which encodes a PTS and enzymes for the transport and catabolism D-glucosaminate (36). DgaR has the conserved histidine required for activation (His-497), and glucose inhibits D-glucosaminate utilization in S. Typhimurium (36). The other LevR-like activator (SL1344_0559) presumably stimulates transcription of a PTS operon of unknown function, and like GfrR, this activator has a tyrosine residue (Tyr-476) in place of the activating histidine; therefore, its activity likely is insensitive to carbon catabolite repression.…”

mentioning

confidence: 99%

A Mannose Family Phosphotransferase System Permease and Associated Enzymes Are Required for Utilization of Fructoselysine and Glucoselysine in Salmonella enterica Serovar Typhimurium

et al. 2015

View full text Add to dashboard Cite

Salmonella enteric serovar Typhimurium, a major cause of food-borne illness, is capable of using a variety of carbon and nitrogen sources. Fructoselysine and glucoselysine are Maillard reaction products formed by the reaction of glucose or fructose, respectively, with the -amine group of lysine. We report here that S. Typhimurium utilizes fructoselysine and glucoselysine as carbon and nitrogen sources via a mannose family phosphotransferase (PTS) encoded by gfrABCD (glucoselysine/fructoselysine PTS components EIIA, EIIB, EIIC, and EIID; locus numbers STM14_5449 to STM14_5454 in S. Typhimurium 14028s). Genes coding for two predicted deglycases within the gfr operon, gfrE and gfrF, were required for growth with glucoselysine and fructoselysine, respectively. GfrF demonstrated fructoselysine-6-phosphate deglycase activity in a coupled enzyme assay. The biochemical and genetic analyses were consistent with a pathway in which fructoselysine and glucoselysine are phosphorylated at the C-6 position of the sugar by the GfrABCD PTS as they are transported across the membrane. The resulting fructoselysine-6-phosphate and glucoselysine-6-phosphate subsequently are cleaved by GfrF and GfrE to form lysine and glucose-6-phosphate or fructose-6-phosphate. Interestingly, although S. Typhimurium can use lysine derived from fructoselysine or glucoselysine as a sole nitrogen source, it cannot use exogenous lysine as a nitrogen source to support growth. Expression of gfrABCDEF was dependent on the alternative sigma factor RpoN ( 54 ) and an RpoN-dependent LevR-like activator, which we designated GfrR. IMPORTANCESalmonella physiology has been studied intensively, but there is much we do not know regarding the repertoire of nutrients these bacteria are able to use for growth. This study shows that a previously uncharacterized PTS and associated enzymes function together to transport and catabolize fructoselysine and glucoselysine. Knowledge of the range of nutrients that Salmonella utilizes is important, as it could lead to the development of new strategies for reducing the load of Salmonella in food animals, thereby mitigating its entry into the human food supply. Salmonella enterica serovar Typhimurium is one of the leading causes of food-borne illness. Salmonella causes 11% of all infections caused by bacterial food-borne pathogens in the United States and is responsible for an estimated 1 million cases of salmonellosis in the United States each year, which result in approximately 19,000 hospitalizations and 400 deaths (1). S. Typhimurium causes gastroenteritis in humans but is capable of colonizing a wide range of animals with few or no disease symptoms. S. Typhimurium utilizes a broad array of carbon and nitrogen sources (2), which may contribute to the wide host range of this bacterium. Chadhuri and coworkers found that genes encoding enzymes in a variety of catabolic processes appear to be important for S. Typhimurium colonization of the chicken, pig, and calf (3). Among those catabolic genes, some encoded phosphoenolp...

show abstract

Salmonella Utilizes D-Glucosaminate via a Mannose Family Phosphotransferase System Permease and Associated Enzymes

Cited by 28 publications

References 71 publications

Interaction with Enzyme IIB^Mpo(EIIB^Mpo) and Phosphorylation by Phosphorylated EIIB^MpoExert Antagonistic Effects on the Transcriptional Activator ManR of Listeria monocytogenes

Interaction with Enzyme IIB^Mpo(EIIB^Mpo) and Phosphorylation by Phosphorylated EIIB^MpoExert Antagonistic Effects on the Transcriptional Activator ManR of Listeria monocytogenes

Contribution of the Salmonella enterica KdgR Regulon to Persistence of the Pathogen in Vegetable Soft Rots

A Mannose Family Phosphotransferase System Permease and Associated Enzymes Are Required for Utilization of Fructoselysine and Glucoselysine in Salmonella enterica Serovar Typhimurium

Contact Info

Product

Resources

About

Salmonella Utilizes D-Glucosaminate via a Mannose Family Phosphotransferase System Permease and Associated Enzymes

Cited by 28 publications

References 71 publications

Interaction with Enzyme IIBMpo(EIIBMpo) and Phosphorylation by Phosphorylated EIIBMpoExert Antagonistic Effects on the Transcriptional Activator ManR of Listeria monocytogenes

Interaction with Enzyme IIBMpo(EIIBMpo) and Phosphorylation by Phosphorylated EIIBMpoExert Antagonistic Effects on the Transcriptional Activator ManR of Listeria monocytogenes

Contribution of the Salmonella enterica KdgR Regulon to Persistence of the Pathogen in Vegetable Soft Rots

A Mannose Family Phosphotransferase System Permease and Associated Enzymes Are Required for Utilization of Fructoselysine and Glucoselysine in Salmonella enterica Serovar Typhimurium

Contact Info

Product

Resources

About

Interaction with Enzyme IIB^Mpo(EIIB^Mpo) and Phosphorylation by Phosphorylated EIIB^MpoExert Antagonistic Effects on the Transcriptional Activator ManR of Listeria monocytogenes

Interaction with Enzyme IIB^Mpo(EIIB^Mpo) and Phosphorylation by Phosphorylated EIIB^MpoExert Antagonistic Effects on the Transcriptional Activator ManR of Listeria monocytogenes