Accumulation of ornithine lipids in Vibrio cholerae under phosphate deprivation is dependent on VC0489 (OlsF) and PhoBR system

Barbosa, Livia C.; Goulart, Carolina L.; Avellar, Marcela M.; Bisch, Paulo Mascarello; Krüger, Wanda M. A. von

doi:10.1099/mic.0.000607

Cited by 13 publications

(14 citation statements)

References 33 publications

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“…During periods of phosphate starvation, some bacteria access cellular phosphate reserves by using acylated amino acids such as OL to replace the phospholipids normally found in bacterial membranes (37)(38)(39). On the other hand, OL production in Rhizobium tropici and Burkholderia cepacia has been shown to be important for the normal tolerance of the bacterial cell to acid and temperature stress (13,40,41).…”

Section: Discussionmentioning

confidence: 99%

The Glycine Lipids of Bacteroides thetaiotaomicron Are Important for Fitness during Growth In Vivo and In Vitro

Lynch

Tammireddy

Doherty

et al. 2019

Appl Environ Microbiol

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Acylated amino acids function as important components of the cellular membrane in some bacteria. Biosynthesis is initiated by the N-acylation of the amino acid, and this is followed by subsequent O-acylation of the acylated molecule, resulting in the production of the mature diacylated amino acid lipid. In this study, we use both genetics and liquid chromatography-mass spectrometry (LC-MS) to characterize the biosynthesis and function of a diacylated glycine lipid (GL) species produced in Bacteroides thetaiotaomicron. We, and others, have previously reported the identification of a gene, named glsB in this study, that encodes an N-acyltransferase activity responsible for the production of a monoacylated glycine called N-acyl-3-hydroxy-palmitoyl glycine (or commendamide). In all of the Bacteroidales genomes sequenced so far, the glsB gene is located immediately downstream from a gene, named glsA, that is also predicted to encode a protein with acyltransferase activity. We use LC-MS to show that the coexpression of glsB and glsA results in the production of GL in Escherichia coli. We constructed a deletion mutant of the glsB gene in B. thetaiotaomicron, and we confirm that glsB is required for the production of GL in B. thetaiotaomicron. Moreover, we show that glsB is important for the ability of B. thetaiotaomicron to adapt to stress and colonize the mammalian gut. Therefore, this report describes the genetic requirements for the biosynthesis of GL, a diacylated amino acid species that contributes to fitness in the human gut bacterium B. thetaiotaomicron. IMPORTANCE The gut microbiome has an important role in both health and disease of the host. The mammalian gut microbiome is often dominated by bacteria from the Bacteroidales, an order that includes Bacteroides and Prevotella. In this study, we have identified an acylated amino acid, called glycine lipid, produced by Bacteroides thetaiotaomicron, a beneficial bacterium originally isolated from the human gut. In addition to identifying the genes required for the production of glycine lipids, we show that glycine lipids have an important role during the adaptation of B. thetaiotaomicron to a number of environmental stresses, including exposure to either bile or air. We also show that glycine lipids are important for the normal colonization of the murine gut by B. thetaiotaomicron. This work identifies glycine lipids as an important fitness determinant in B. thetaiotaomicron and therefore increases our understanding of the molecular mechanisms underpinning colonization of the mammalian gut by beneficial bacteria.

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Section: Discussionmentioning

confidence: 99%

The Glycine Lipids of Bacteroides thetaiotaomicron Are Important for Fitness during Growth In Vivo and In Vitro

Lynch

Tammireddy

Doherty

et al. 2019

Appl Environ Microbiol

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“…During periods of phosphorous starvation some bacteria access cellular phosphorous reserves by using acylated amino acids such as OL to replace the phospholipids normally found in bacterial membranes (37-39). On the other hand, OL production in Rhizobium tropici and Burholderia cepacia has been shown to be important for the normal tolerance of the bacterial cell to acid and temperature stress (13, 40, 41).…”

Section: Discussionmentioning

confidence: 99%

Characterization of the role of glycine lipids inBacteroides thetaiotaomicron

Lynch

Tammireddy

Doherty

et al. 2018

Preprint

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18Acylated amino acids function as important components of the cellular membrane in some 19 bacteria. Biosynthesis is initiated by the N-acylation of the amino acid and this is followed by 20 subsequent O-acylation of the acylated molecule resulting in the production of the mature 21 diacylated amino acid lipid. In this study we use both genetics and liquid chromatography- 22 mass spectrometry (LC-MS) to characterize the biosynthesis and function of novel diacylated 23 glycine lipid (GL) species in Bacteroides thetaiotaomicron. We, and others, have previously 24 reported the identification of a gene, named glsB in this study, that encodes a N- 25 acyltransferase activity responsible for the production of a monoacylated glycine called N-26 acyl-3-hydroxy-palmitoyl glycine (or commendamide). In all of the Bacteroidales genomes so 27 far sequenced the glsB gene is located immediately downstream from a gene, named glsA, 28 also predicted to encode a protein with acyltransferase activity. We use LC-MS to show that 29 co-expression of glsB and glsA results in the production of GL in Escherichia coli. We 30 constructed a deletion mutant of the glsB gene in B. thetaiotaomicron and we confirm that 31 glsB is required for the production of GL in B. thetaiotaomicron. Moreover, we show that glsB 32 is important for the ability of B. thetaiotaomicron to adapt to stress and colonize the 33 mammalian gut. Therefore, this report is the first to describe the genetic requirements for 34 the biosynthesis of GL, a novel diacylated amino acids species that contributes to fitness in 35 the human gut bacterium, B. thetaiotaomicron. 36 37 38 39 42 healthy human gut microbiota (1). The gut-associated Bacteroidetes are required to digest 43 complex dietary glycans into short-chain fatty acids (such as acetate and propionate) that 44 are accessible to the host (2-4). A longitudinal study in infants has revealed the presence of 45 Bacteroides in the infant gut within 1 week of birth and some species of Bacteroides have 46 been shown to utilize the polysaccharides present in human breast milk (5, 6). Therefore it 47 has been suggested that Bacteroides may have an important role during the early 48 development of the infant gut (6). 49 50Acylated amino acids can be found in the membranes of many bacteria (7, 8). The best-51 characterized, and most widespread, acylated amino acid is ornithine lipid (OL). OL contains 52 a 3'-hydroxy fatty acid group attached by an amide linkage to the a-amino group of 53 ornithine with a second fatty acid group ester linked to the 3'-hydroxy group of the first 54 fatty acid (9). The genetics of OL production was first described in Sinorhizobium meliloti 55 where it was shown that a N-acyltransferase encoded by olsB catalysed the attachment of 56 the first fatty acid group to ornithine, resulting in monoacylated ornithine or lyso-OL (10). 57 The second fatty acid was subsequently attached to lyso-OL through the activity of an O-58 acyltransferase encoded by olsA, resulting in the producti...

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“…(data no shown). Bacterial species such as Sinorhizobium meliloti, Rhodobacter sphaeroides, Pseudomonas fluorescens, Pseudomonas diminuta, Desulfovibrio alaskensis, Serratia proteamaculans, and Vibrio cholerae do not form OL when the bacteria are grown in complex media (which are usually rich in phosphate), but induce the synthesis of OLs or/and other phosphorus-free lipids under phosphate-limiting growth conditions and replace some of their membrane phospholipids (Minnikin and Abdolrahimzadeh, 1974;Benning et al, 1995;Geiger et al, 1999;Lewenza et al, 2011;Bosak et al, 2016;Barbosa et al, 2018). In some of these bacteria, gene expression in response to phosphate limitation is known to be regulated by the two-component system PhoBR.…”

Section: Burkholderia Sensu Lato Strains and Their Membrane Lipid Commentioning

confidence: 99%

Ornithine Lipids in Burkholderia spp. Pathogenicity

Córdoba-Castro

Salgado-Morales

Torres

et al. 2021

Front. Mol. Biosci.

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The genus Burkholderia sensu lato is composed of a diverse and metabolically versatile group of bacterial species. One characteristic thought to be unique for the genus Burkholderia is the presence of two forms each (with and without 2-hydroxylation) of the membrane lipids phosphatidylethanolamine (PE) and ornithine lipids (OLs). Here, we show that only Burkholderia sensu stricto strains constitutively form OLs, whereas all other analyzed strains belonging to the Burkholderia sensu lato group constitutively form the two forms of PE, but no OLs. We selected two model bacteria to study the function of OL in Burkholderia sensu lato: (1) Burkholderia cenocepacia wild-type which constitutively forms OLs and its mutant deficient in the formation of OLs and (2) Robbsia andropogonis (formerly Burkholderia andropogonis) which does not form OL constitutively, and a derived strain constitutively forming OLs. Both were characterized under free-living conditions and during pathogenic interactions with their respective hosts. The absence of OLs in B. cenocepacia slightly affected bacterial growth under specific abiotic stress conditions such as high temperature and low pH. B. cenocepacia lacking OLs caused lower mortality in Galleria mellonella larvae while R. andropogonis constitutively forming OLs triggers an increased formation of reactive oxygen species immediately after infection of maize leaves, suggesting that OLs can have an important role during the activation of the innate immune response of eukaryotes.

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Accumulation of ornithine lipids in Vibrio cholerae under phosphate deprivation is dependent on VC0489 (OlsF) and PhoBR system

Cited by 13 publications

References 33 publications

The Glycine Lipids of Bacteroides thetaiotaomicron Are Important for Fitness during Growth In Vivo and In Vitro

The Glycine Lipids of Bacteroides thetaiotaomicron Are Important for Fitness during Growth In Vivo and In Vitro

Characterization of the role of glycine lipids inBacteroides thetaiotaomicron

Ornithine Lipids in Burkholderia spp. Pathogenicity

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