Involvement of an Essential Gene,<i>mviN</i>, in Murein Synthesis in<i>Escherichia coli</i>

Inoue, Atsuyuki; Murata, Yoshimitsu; Takahashi, Hiroshi; Tsuji, Naoko; Fujisaki, Shingo; Kato, Junichi

doi:10.1128/jb.00551-08

Cited by 89 publications

(104 citation statements)

References 19 publications

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“…Although mviN is uncharacterized and is a putative gene in meningococcus, its products have been experimentally characterized in Escherichia coli and Salmonella enterica serovar Typhimurium, which are also Gram negative (3,18). A mutation in the functional S. Typhimurium homolog of mviN renders an otherwise avirulent isolate virulent.…”

Section: Resultsmentioning

confidence: 99%

Using Single-Nucleotide Polymorphisms To Discriminate Disease-Associated from Carried Genomes of Neisseria meningitidis

et al. 2011

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Neisseria meningitidis is one of the main agents of bacterial meningitis, causing substantial morbidity and mortality worldwide. However, most of the time N. meningitidis is carried as a commensal not associated with invasive disease. The genomic basis of the difference between disease-associated and carried isolates of N. meningitidis may provide critical insight into mechanisms of virulence, yet it has remained elusive. Here, we have taken a comparative genomics approach to interrogate the difference between disease-associated and carried isolates of N. meningitidis at the level of individual nucleotide variations (i.e., single nucleotide polymorphisms [SNPs]). We aligned complete genome sequences of 8 disease-associated and 4 carried isolates of N. meningitidis to search for SNPs that show mutually exclusive patterns of variation between the two groups. We found 63 SNPs that distinguish the 8 disease-associated genomes from the 4 carried genomes of N. meningitidis, which is far more than can be expected by chance alone given the level of nucleotide variation among the genomes. The putative list of SNPs that discriminate between disease-associated and carriage genomes may be expected to change with increased sampling or changes in the identities of the isolates being compared. Nevertheless, we show that these discriminating SNPs are more likely to reflect phenotypic differences than shared evolutionary history. Discriminating SNPs were mapped to genes, and the functions of the genes were evaluated for possible connections to virulence mechanisms. A number of overrepresented functional categories related to virulence were uncovered among SNP-associated genes, including genes related to the category "symbiosis, encompassing mutualism through parasitism."

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Section: Resultsmentioning

confidence: 99%

Using Single-Nucleotide Polymorphisms To Discriminate Disease-Associated from Carried Genomes of Neisseria meningitidis

et al. 2011

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“…The gene encodes a sigma factor necessary for the expression of the flg operon, resulting in flagellum synthesis (29). An mviN homolog gene was also found in E. coli (53%) and is involved in peptidoglycan and thus cellular membrane synthesis (17). The irgA gene encodes an outer membrane receptor for enterobactin (6) that is an abundant ironregulated protein in many bacteria, such as Marinobacter aquaeolei (57%).…”

Section: Discussionmentioning

confidence: 99%

Occurrence of Putative Virulence Genes in Arcobacter Species Isolated from Humans and Animals

et al. 2012

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Interest in arcobacters in veterinary and human public health has increased since the first report of the isolation of arcobacters from food of animal origin. Since then, studies worldwide have reported the occurrence of arcobacters on food and in food production animals and have highlighted possible transmission, especially of Arcobacter butzleri, to the human population. In humans, arcobacters are associated with enteritis and septicemia. To assess their clinical relevance for humans and animals, evaluation of potential virulence factors is required. However, up to now, little has been known about the mechanisms of pathogenicity. Because of their close phylogenetic affiliation to the food-borne pathogen Campylobacter and their similar clinical manifestations, the presence of nine putative Campylobacter virulence genes (cadF, ciaB, cj1349, hecA, hecB, irgA, mviN, pldA, and tlyA) previously identified in the recent Arcobacter butzleri ATCC 49616 genome sequence was determined in a large set of human and animal Arcobacter butzleri, Arcobacter cryaerophilus, and Arcobacter skirrowii strains after the development of rapid and accurate PCR assays and confirmed by sequencing and dot blot hybridization.A rcobacters are increasingly being isolated from a wide range of food products all over the world. These Gram-negative bacteria have been classified into the family Campylobacteraceae (35), although a recent annotation of the Arcobacter butzleri genome suggests a closer phylogenetic relation to Sulfurimonas denitrificans and Wolinella succinogenes, both members of the Helicobacteraceae, as well as to the deep-sea vent Epsilonproteobacteria members Sulfurovum and Nitratiruptor (26). At present, 13 Arcobacter species have been characterized, of which 6 were isolated from mammals. In humans, A. butzleri is predominantly associated with enteritis and septicemia (24,30,46), though Arcobacter cryaerophilus and Arcobacter skirrowii have also been isolated from diarrheal stool specimens (21,33,44). The other three species, Arcobacter cibarius (15), Arcobacter thereius (14), and Arcobacter trophiarum (4) are present in farm animals and on food of animal origin but have not yet been isolated from human specimens.Contaminated drinking water is identified as a major source of human Arcobacter infection in developing regions (1), whereas in industrialized countries, infections are assumed to be food-borne. Close contact with pets and person-to-person transmission are the other potential risk factors (9, 36). Arcobacters seem to be commonly present on food of animal origin, with the highest prevalence reported for poultry followed by pork and beef (38,42). The origin of the contamination on poultry products is still debated (39), but for pork and beef, feces transmitted during the slaughter process is regarded as the initial source of contamination (40, 44).The A. butzleri ATCC 49616 genome revealed that this strain has putative virulence determinants such as genes cadF and cj1349, coding for fibronectin binding proteins; the invasi...

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“…How this bacterium flips lipid II across its cytoplasmic membrane during PG biosynthesis is controversial. In recent years, three inner membrane proteins, RodA, FtsW, and MurJ, have been proposed to be lipid II flippases in E. coli (13)(14)(15)(16). RodA and FtsW are paralogs thought to perform the same function in PG biogenesis but at different stages of development.…”

Section: ) (7)mentioning

confidence: 99%

“…MurJ is an essential inner membrane protein whose depletion inhibits PG sacculus biosynthesis and leads to the accumulation of PG precursors, including lipid-linked intermediates (14,16). Orthologs in some Gram-positive bacteria are also required for PG biosynthesis (29,30).…”

Section: ) (7)mentioning

confidence: 99%

Structure-Function Analysis of MurJ Reveals a Solvent-Exposed Cavity Containing Residues Essential for Peptidoglycan Biogenesis in Escherichia coli

et al. 2013

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Gram-negative bacteria such as Escherichia coli build a peptidoglycan (PG) cell wall in their periplasm using the precursor known as lipid II. Lipid II is a large amphipathic molecule composed of undecaprenyl diphosphate and a disaccharide-pentapeptide that PG-synthesizing enzymes use to build the PG sacculus. During PG biosynthesis, lipid II is synthesized at the cytoplasmic face of the inner membrane and then flipped across the membrane. This translocation of lipid II must be assisted by flippases thought to shield the disaccharide-pentapeptide as it crosses the hydrophobic core of the membrane. The inner membrane protein MurJ is essential for PG biogenesis and homologous to known and putative flippases of the MOP (multidrug/oligo-saccharidyl-lipid/polysaccharide) exporter superfamily, which includes flippases that translocate undecaprenyl diphosphate-linked oligosaccharides across the cytoplasmic membranes of bacteria. Consequently, MurJ has been proposed to function as the lipid II flippase in E. coli. Here, we present a three-dimensional structural model of MurJ generated by the I-TASSER server that suggests that MurJ contains a solvent-exposed cavity within the plane of the membrane. Using in vivo topological studies, we demonstrate that MurJ has 14 transmembrane domains and validate features of the MurJ structural model, including the presence of a solvent-exposed cavity within its transmembrane region. Furthermore, we present functional studies demonstrating that specific charged residues localized in the central cavity are essential for function. Together, our studies support the structural homology of MurJ to MOP exporter proteins, suggesting that MurJ might function as an essential transporter in PG biosynthesis.T he cell envelope of most bacteria contains a cell wall exoskeleton composed of peptidoglycan (PG) that surrounds the cytoplasmic membrane (1, 2). The rigid PG structure protects the bacterium from osmotic rupture, serves as a scaffold onto which other envelope components are attached, and defines cell shape. Underscoring the essentiality of the PG cell wall is the fact that many antibiotics target PG biosynthesis (3).Bacteria build their PG sacculus by polymerizing an N-acetylglucosamine-N-acetylmuramic acid (GlcNAc-MurNAc) disaccharide-pentapeptide into long glycan chains that are cross-linked by peptide bonds between stem peptides (2). This GlcNAcMurNAc disaccharide-pentapeptide is synthesized at the cytoplasmic side of the membrane as a polyisoprenyl lipid-linked precursor known as lipid II (Fig. 1A) (4). Because lipid II polymerization occurs at the extracytoplasmic side of the membrane, an obligatory step in PG biosynthesis is the translocation of the lipidlinked disaccharide-pentapeptide across the cytoplasmic membrane.The use of polyisoprenyl lipid-linked precursors in the biogenesis of envelope glycopolymers is widespread in bacteria. Examples include the biogenesis of PG, certain capsules and exopolysaccharides, and O antigens (5, 6). In these systems, bacteria build each precursor ...

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Involvement of an Essential Gene,mviN, in Murein Synthesis inEscherichia coli

Cited by 89 publications

References 19 publications

Using Single-Nucleotide Polymorphisms To Discriminate Disease-Associated from Carried Genomes of Neisseria meningitidis

Using Single-Nucleotide Polymorphisms To Discriminate Disease-Associated from Carried Genomes of Neisseria meningitidis

Occurrence of Putative Virulence Genes in Arcobacter Species Isolated from Humans and Animals

Structure-Function Analysis of MurJ Reveals a Solvent-Exposed Cavity Containing Residues Essential for Peptidoglycan Biogenesis in Escherichia coli

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