Biosynthesis of Osmoregulated Periplasmic Glucans in<i>Escherichia coli</i>: The Phosphoethanolamine Transferase Is Encoded by<i>opgE</i>

Bontemps­-Gallo, Sébastien; Cogez, Virginie; Robbe-Masselot, Catherine; Quintard, Kévin; Dondeyne, Jacqueline; Madec, Edwige; Lacroix, Jean-Marie

doi:10.1155/2013/371429

Cited by 22 publications

(23 citation statements)

References 14 publications

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“…2, yellow shading). This cluster was from a main branch that included two PEtn transferases with distinctly different acceptor molecules: glucose-specific OpgE from E. coli (which transfers PEtn to osmoregulated periplasmic glucans [OPG] [22]) and PptA from N. gonorrhoeae (strain FA1090) (which is responsible for the transfer of PEtn to pilin [23]). Also in this group were the predicted PEtn transferases PtdA and PtdB from Haemophilus ducreyi.…”

Section: Resultsmentioning

confidence: 99%

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Characterization of Two Novel Lipopolysaccharide Phosphoethanolamine Transferases in Pasteurella multocida and Their Role in Resistance to Cathelicidin-2

et al. 2017

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The lipopolysaccharide (LPS) produced by the Gram-negative bacterial pathogen Pasteurella multocida has phosphoethanolamine (PEtn) residues attached to lipid A, 3-deoxy-D-manno-octulosonic acid (Kdo), heptose, and galactose. In this report, we show that PEtn is transferred to lipid A by the P. multocida EptA homologue, PetL, and is transferred to galactose by a novel PEtn transferase that is unique to P. multocida called PetG. Transcriptomic analyses indicated that petL expression was positively regulated by the global regulator Fis and negatively regulated by an Hfq-dependent small RNA. Importantly, we have identified a novel PEtn transferase called PetK that is responsible for PEtn addition to the single Kdo molecule (Kdo 1 ), directly linked to lipid A in the P. multocida glycoform A LPS. In vitro assays showed that the presence of a functional petL and petK, and therefore the presence of PEtn on lipid A and Kdo 1 , was essential for resistance to the cationic, antimicrobial peptide cathelicidin-2. The importance of PEtn on Kdo 1 and the identification of the transferase responsible for this addition have not previously been shown. Phylogenetic analysis revealed that PetK is the first representative of a new family of predicted PEtn transferases. The PetK family consists of uncharacterized proteins from a range of Gram-negative bacteria that produce LPS glycoforms with only one Kdo molecule, including pathogenic species within the genera Vibrio, Bordetella, and Haemophilus. We predict that many of these bacteria will require the addition of PEtn to Kdo for maximum protection against host antimicrobial peptides.

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Section: Resultsmentioning

confidence: 99%

“…PEtn is also incorporated into OPG, located in the periplasm of many bacteria, including E. coli (22). The addition of PEtn to key positions on bacterial surface structures confers resistance to polymyxins and host innate immune antimicrobials, including cathelicidins and alpha and beta defensins (21,24,40).…”

Section: Discussionmentioning

confidence: 99%

Characterization of Two Novel Lipopolysaccharide Phosphoethanolamine Transferases in Pasteurella multocida and Their Role in Resistance to Cathelicidin-2

et al. 2017

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“…Similarly, the glycosyltransferase activity of OpgH uses polyprenyl phosphates (including decaprenyl-phosphate) as substrates (93). Although Und-P has not been formally tested as a substrate, an opgH mutant exhibits increased resistance to bacitracin (which inhibits recycling of Und-PP to Und-P) (94) and enhanced exopolysaccharide (EPS) production (95,96); each of these phenotypes is consistent with the enhanced availability of Und-P. The idea that elevated pools of cell envelope precursors (especially PG precursors) can lead to enhanced cell division is also supported by additional studies discussed below.…”

Section: Udp-glucose and Ugtp (B Subtilis)mentioning

confidence: 99%

Metabolism Shapes the Cell

Sperber

Herman

2017

J Bacteriol

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More than 5 decades of work support the idea that cell envelope synthesis, including the inward growth of cell division, is tightly coordinated with DNA replication and protein synthesis through central metabolism. Remarkably, no unifying model exists to account for how these fundamentally disparate processes are functionally coupled. Recent studies demonstrate that proteins involved in carbohydrate and nitrogen metabolism can moonlight as direct regulators of cell division, coordinate cell division and DNA replication, and even suppress defects in DNA replication. In this minireview, we focus on studies illustrating the intimate link between metabolism and regulation of peptidoglycan (PG) synthesis during growth and division, and we identify the following three recurring themes. (i) Nutrient availability, not growth rate, is the primary determinant of cell size. (ii) The degree of gluconeogenic flux is likely to have a profound impact on the metabolites available for cell envelope synthesis, so growth medium selection is a critical consideration when designing and interpreting experiments related to morphogenesis. (iii) Perturbations in pathways relying on commonly shared and limiting metabolites, like undecaprenyl phosphate (Und-P), can lead to pleotropic phenotypes in unrelated pathways.KEYWORDS FtsZ, MreB, UDP-glucose, cell division, gluconeogenesis, metabolism, morphogenesis, peptidoglycan, phosphoenolpyruvate, undecaprenyl phosphate T o accurately partition chromosomes and other cell contents during reproduction, cells must possess mechanisms to organize repeated cycles of cell growth, chromosome replication, and division. Eukaryotes orchestrate this coordination using the cell cycle and separate growth, DNA synthesis, and cytokinesis into distinct, temporally sequestered phases. Bacteria, by contrast, simultaneously increase in cell size and replicate DNA before (or concurrently with) cell division. Elucidating the molecular mechanisms prokaryotes employ to achieve spatiotemporal organization of these intertwined yet functionally disparate processes is of considerable interest to scientists seeking to understand bacterial reproduction, and many outstanding questions remain to be answered. For example, how is DNA replication kept in sync with changing growth and division rates? How are cell dimensions maintained or actively rearranged in response to environmental or developmental cues? What signals do cells sense to switch between increasing in cell size and dividing during the cell cycle? Relatedly, how are these signals transduced to activate/deactivate the distinct machineries required for each process?Perhaps one of the biggest mysteries remaining in bacterial cell biology relates to understanding the regulatory cross talk that must occur to integrate central metabolism with macromolecular biosynthesis. Nutrients are converted into stored energy and precursors used to synthesize macromolecules like DNA and peptidoglycan (PG), so it is no surprise that nutrient availability has a profound impac...

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“…The first studies on the OPGs' biological role was done on the non‐pathogenic E. coli K12, which shows only a few phenotypes (Bontemps‐Gallo et al ., ). The inactivation of either opgG or opgH gene provokes a decrease of the motility and an increase of the mucoidy in E. coli (Bontemps‐Gallo et al ., ). New study models were required for a better understanding of the OPGs' biological role in virulence.…”

Section: Introductionmentioning

confidence: 97%

“…The synthesis of the glucose backbone requires either the opgGH operon (families I and IV) (see Bontemps‐Gallo et al ., , for a biosynthesis working model) or ndvAB/chvAB/cgs operon (families II and III). The inactivation of the operon provokes a total loss of OPGs (Bohin, ; Bohin and Lacroix, ).…”

Section: Introductionmentioning

confidence: 99%

New insights into the biological role of the osmoregulated periplasmic glucans in pathogenic and symbiotic bacteria

Bontemps-Gallo

Lacroix

2015

Environ Microbiol Rep

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Summary This review emphasizes the biological roles of the osmoregulated periplasmic glucans (OPGs). OPGs occur in almost all α, β and γ Proteobacteria. This polymer of glucose is required for full virulence. The roles of the OPGs are complex and vary depending on the species. Here, we outline the four major roles of the OPGs through four different pathogenic and one symbiotic bacterial models (Dickeya dadantii, Salmonella enterica, Pseudomonas aeruginosa, Brucella abortus and Sinorhizobium meliloti). When periplasmic, the OPGs are a part of the signal transduction pathway and indirectly regulate genes involved in virulence. The OPGs can also be secreted. When outside of the cell, they interact directly with antibiotics to protect the bacterial cell or interact with the host cell to facilitate the invasion process. When OPGs are not found, as in the ε Proteobacteria, OPG-like oligosaccharides are present. Their presence strengthens the evidence that OPGs play an important role in virulence.

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Biosynthesis of Osmoregulated Periplasmic Glucans inEscherichia coli: The Phosphoethanolamine Transferase Is Encoded byopgE

Cited by 22 publications

References 14 publications

Characterization of Two Novel Lipopolysaccharide Phosphoethanolamine Transferases in Pasteurella multocida and Their Role in Resistance to Cathelicidin-2

Characterization of Two Novel Lipopolysaccharide Phosphoethanolamine Transferases in Pasteurella multocida and Their Role in Resistance to Cathelicidin-2

Metabolism Shapes the Cell

New insights into the biological role of the osmoregulated periplasmic glucans in pathogenic and symbiotic bacteria

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