Revisiting long-chain fatty acid metabolism in Escherichia coli: integration with stress responses

Jaswal, Kanchan; Shrivastava, Megha; Chaba, Rachna

doi:10.1007/s00294-021-01178-z

Cited by 12 publications

(4 citation statements)

References 83 publications

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“…The initiation of Lp replication was delayed in axenic cultures in the presence of 300µM lauric, myristic, palmitic or oleic acids to various degrees (Fig 2A), indicating that these fatty acids can induce measurable direct growth defect in the absence of host cells. Under the same growth conditions Escherichia coli growth in axenic media was enhanced (Fig 2B) consistent with E. coli capacity for metabolic utilization of exogenous fatty acids (Jaswal et al, 2021). Palmitoleic acid at concentrations that enhanced Lp intracellular replication did not affect Lp growth in axenic cultures (Fig 2A).…”

Section: Resultssupporting

confidence: 64%

The intracellular growth of the vacuolar pathogenLegionella pneumophilais dependent on the acyl chain composition of host membranes

Wilkins,

Schwarz,

Torres-Escobar

et al. 2023

Preprint

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Legionella pneumophilais an accidental human bacterial pathogen that infects and replicates within alveolar macrophages causing a severe atypical pneumonia known as Legionnaires’ disease. As a prototypical vacuolar pathogenL. pneumophilaestablishes a unique endoplasmic reticulum (ER)-derived organelle within which bacterial replication takes place. Bacteria-derived proteins are deposited in the host cytosol and in the lumen of the pathogen-occupied vacuole via a type IVb (T4bSS) and a type II (T2SS) secretion system respectively. These secretion system effector proteins manipulate multiple host functions to facilitate intracellular survival of the bacteria. Subversion of host membrane glycerophospholipids (GPLs) by the internalized bacteria via distinct mechanisms feature prominently in trafficking and biogenesis of theLegionella-containing vacuole (LCV). Conventional GPLs composed of a glycerol backbone linked to a polar headgroup and esterified with two fatty acids constitute the bulk of membrane lipids in eukaryotic cells. The acyl chain composition of GPLs dictates phase separation of the lipid bilayer and therefore determines the physiochemical properties of biological membranes - such as membrane disorder, fluidity and permeability. In mammalian cells, fatty acids esterified in membrane GPLs are sourced endogenously fromde novosynthesis or via internalization from the exogenous pool of lipids present in serum and other interstitial fluids. Here, we exploited the preferential utilization of exogenous fatty acids for GPL synthesis by macrophages to reprogram the acyl chain composition of host membranes and investigated its impact on LCV homeostasis andL. pneumophilaintracellular replication. Using saturated fatty acids as well ascis- andtrans- isomers of monounsaturated fatty acids we discovered that under conditions promoting lipid packing and membrane rigidificationL. pneumophilaintracellular replication was significantly reduced. Palmitoleic acid – a C16:1 monounsaturated fatty acid – that promotes membrane disorder when enriched in GPLs significantly increased bacterial replication within human and murine macrophages but not in axenic growth assays. Lipidome analysis of infected macrophages showed that treatment with exogenous palmitoleic acid resulted in membrane acyl chain reprogramming in a manner that promotes membrane disorder and live-cell imaging revealed that the consequences of increasing membrane disorder impinge on several LCV homeostasis parameters. Collectively, we provide experimental evidence thatL. pneumophilareplication within its intracellular niche is a function of the lipid bilayer disorder and hydrophobic thickness.

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Section: Resultssupporting

confidence: 64%

The intracellular growth of the vacuolar pathogenLegionella pneumophilais dependent on the acyl chain composition of host membranes

Wilkins,

Schwarz,

Torres-Escobar

et al. 2023

Preprint

View full text Add to dashboard Cite

show abstract

“…The initiation of Lp replication was delayed in axenic cultures in the presence of 300µM lauric, myristic, palmitic or oleic acids to various degrees (Figure 2A), indicating that these fatty acids can induce measurable direct growth defect in the absence of host cells. Under the same growth conditions Escherichia coli growth in axenic medium was enhanced (Figure 2B) consistent with E. coli capacity for metabolic utilization of exogenous fatty acids (Jaswal et al, 2021). Palmitoleic acid at concentrations that enhanced Lp intracellular replication did not affect Lp growth in axenic cultures (Figure 2A).…”

Section: Resultssupporting

confidence: 59%

The intracellular growth of the vacuolar pathogen Legionella pneumophila is dependent on the acyl chain composition of host membranes

Wilkins,

Schwarz,

Torres-Escobar

et al. 2024

Front. Bacteriol.

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Legionella pneumophila is an accidental human bacterial pathogen that infects and replicates within alveolar macrophages causing a severe atypical pneumonia known as Legionnaires’ disease. As a prototypical vacuolar pathogen L. pneumophila establishes a unique endoplasmic reticulum (ER)-derived organelle within which bacterial replication takes place. Bacteria-derived proteins are deposited in the host cytosol and in the lumen of the pathogen-occupied vacuole via a type IVb (T4bSS) and a type II (T2SS) secretion system respectively. These secretion system effector proteins manipulate multiple host functions to facilitate intracellular survival of the bacteria. Subversion of host membrane glycerophospholipids (GPLs) by the internalized bacteria via distinct mechanisms feature prominently in trafficking and biogenesis of the Legionella-containing vacuole (LCV). Conventional GPLs composed of a glycerol backbone linked to a polar headgroup and esterified with two fatty acids constitute the bulk of membrane lipids in eukaryotic cells. The acyl chain composition of GPLs dictates phase separation of the lipid bilayer and therefore determines the physiochemical properties of biological membranes - such as membrane disorder, fluidity and permeability. In mammalian cells, fatty acids esterified in membrane GPLs are sourced endogenously from de novo synthesis or via internalization from the exogenous pool of lipids present in serum and other interstitial fluids. Here, we exploited the preferential utilization of exogenous fatty acids for GPL synthesis by macrophages to reprogram the acyl chain composition of host membranes and investigated its impact on LCV homeostasis and L. pneumophila intracellular replication. Using saturated fatty acids as well as cis- and trans- isomers of monounsaturated fatty acids we discovered that under conditions promoting lipid packing and membrane rigidification L. pneumophila intracellular replication was significantly reduced. Palmitoleic acid – a C16:1 monounsaturated fatty acid – that promotes membrane disorder when enriched in GPLs significantly increased bacterial replication within human and murine macrophages but not in axenic growth assays. Lipidome analysis of infected macrophages showed that treatment with exogenous palmitoleic acid resulted in membrane acyl chain reprogramming in a manner that promotes membrane disorder and live-cell imaging revealed that the consequences of increasing membrane disorder impinge on several LCV homeostasis parameters. Collectively, we provide experimental evidence that L. pneumophila replication within its intracellular niche is a function of the lipid bilayer disorder and hydrophobic thickness.

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“…In conclusion, this study shows that general predators with higher predation capacities can be readily selected in laboratory context. Interestingly, the metabolic changes observed in the evolved strains echo emerging research suggesting that the fatty acid degradation pathway might enhance bacterial stress responses, thereby better equipping them to navigate challenging environments (35). The study was performed in a laboratory setting, which could limit the ecological implications.…”

Section: Discussionmentioning

confidence: 84%

Fatty Acid Metabolism and The Oxidative Stress Response Support Bacterial Predation

Jain,

Le,

Bertaux

et al. 2023

Preprint

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Despite growing awareness for their importance in soil ecology, the genetic and physiological traits of bacterial predators are still relatively poorly understood. In the course of aMyxococcus xanthuspredator evolution experiment, we discovered a class of genotypes leading to enhanced predation against evolutionary-diverse species. Genetics and RNAseq analyses link this improved predation capacity to the fine-tuned control of intracellular Acetyl-CoA pools following increased activation of fatty acid beta-oxidation. Notably, these metabolic changes led to the constitutive expression of antioxidant genes. This is critical to the predatory advantage of the evolved strain because this response shields predatory cells against Reactive Oxygen Species (ROS), which arise following contact-dependent killing of the prey cells. Globally, these findings suggest that predators turning on lipid metabolism serves two purposes: energy production and adaptation to oxidative stress originating from interaction with their prey.

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Revisiting long-chain fatty acid metabolism in Escherichia coli: integration with stress responses

Cited by 12 publications

References 83 publications

The intracellular growth of the vacuolar pathogenLegionella pneumophilais dependent on the acyl chain composition of host membranes

The intracellular growth of the vacuolar pathogenLegionella pneumophilais dependent on the acyl chain composition of host membranes

The intracellular growth of the vacuolar pathogen Legionella pneumophila is dependent on the acyl chain composition of host membranes

Fatty Acid Metabolism and The Oxidative Stress Response Support Bacterial Predation

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