Fatty Acids Regulate Stress Resistance and Virulence Factor Production for Listeria monocytogenes

Sun, Yvonne; Wilkinson, Brian J.; Standiford, Theodore J.; Akinbi, Henry T.; O’Riordan, Mary X.

doi:10.1128/jb.00045-12

Cited by 98 publications

(90 citation statements)

References 64 publications

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“…1b supplemental) that were identified as anteiso C15:0 (52.3%) and anteiso C17:0 (40.8%). The results are in perfect accord with previous studies on strain cld-2 [2, 5, 12]. Growth in the presence of 2-MP led to two novel major peaks in the chromatograph with retention times of 2.61 and 3.24 min (Fig.…”

Section: Resultssupporting

confidence: 92%

“…Sun and O'Riordan [11] showed that BCFA-deficient mutants grew and survived less well in macrophages, exhibited decreased production of the key virulence factor listeriolysin O, and were highly attenuated in a murine model of infection. In an extension of these studies, BCFAs played a critical role in protection against antimicrobial peptides and peptidoglycan hydrolases [12]. In all these cases 2-MB restored the anteiso C15:0 and anteiso C17:0 fatty acid content and the defects in the mutants to a large extent.…”

Section: Introductionmentioning

confidence: 99%

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Short branched-chain C6 carboxylic acids result in increased growth, novel ‘unnatural’ fatty acids and increased membrane fluidity in a Listeria monocytogenes branched-chain fatty acid-deficient mutant

Sen

Sirobhushanam

Hantak

et al. 2015

Biochimica et Biophysica Acta (BBA) - Molecular and Cell Biolog

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Listeria monocytogenes is a psychrotolerant food borne pathogen, responsible for the high fatality disease listeriosis, and expensive food product recalls. Branched-chain fatty acids (BCFAs) of the membrane play a critical role in providing appropriate membrane fluidity and optimum membrane biophysics. The fatty acid composition of a BCFA-deficient mutant is characterized by high amounts of straight-chain fatty acids and even-numbered iso fatty acids, in contrast to the parent strain where odd-numbered anteiso fatty acids predominate. The presence of 2-methylbutyrate (C5) stimulated growth of the mutant at 37°C and restored growth at 10°C along with the content of odd-numbered anteiso fatty acids. The C6 branched-chain carboxylic acids 2-ethylbutyrate and 2-methylpentanoate also stimulated growth to a similar extent as 2-methylbutyrate. However, 3-methylpentanoate was ineffective in rescuing growth. 2-ethylbutyrate and 2-methylpentanoate led to novel major fatty acids in the lipid profile of the membrane that were identified as 12-ethyltetradecanoic acid and 12-methylpentadecanoic acid respectively. Membrane anisotropy studies indicated that growth of strain MOR401 in the presence of these precursors increased its membrane fluidity to levels of the wild type. Cells supplemented with 2-methylpentanoate or 2-ethylbutyrate at 10°C shortened the chain length of novel fatty acids, thus showing homeoviscous adaptation. These experiments use the mutant as a tool to modulate the membrane fatty acid compositions through synthetic precursor supplementation, and show how existing enzymes in L. monocytogenes adapt to exhibit non-native activity yielding unique ‘unnatural’ fatty acid molecules, which nevertheless possess the correct biophysical properties for proper membrane function in the BCFA-deficient mutant.

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Section: Resultssupporting

confidence: 92%

Section: Introductionmentioning

confidence: 99%

Short branched-chain C6 carboxylic acids result in increased growth, novel ‘unnatural’ fatty acids and increased membrane fluidity in a Listeria monocytogenes branched-chain fatty acid-deficient mutant

Sen

Sirobhushanam

Hantak

et al. 2015

Biochimica et Biophysica Acta (BBA) - Molecular and Cell Biolog

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“…As examples, Salmonella enterica senses its levels of ATP to control a virulence locus (98), while Listeria monocytogenes and Legionella pneumophila regulate virulence factor production in response to metabolites such as fatty acids and amino acids (99)(100)(101). The demonstrated effects of various metabolic activities in B. burgdorferi and other pathogens indicate that previously reported effects of temperature on other bacteria should be reexamined to determine the actual regulatory cue(s) (30).…”

Section: Discussionmentioning

confidence: 99%

Changes in Bacterial Growth Rate Govern Expression of the Borrelia burgdorferi OspC and Erp Infection-Associated Surface Proteins

Jutras

Chenail

Stevenson

2012

Journal of Bacteriology

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The Lyme disease spirochete controls production of its OspC and Erp outer surface proteins, repressing protein synthesis during colonization of vector ticks but increasing expression when those ticks feed on vertebrate hosts. Early studies found that the synthesis of OspC and Erps can be stimulated in culture by shifting the temperature from 23°C to 34°C, leading to a hypothesis that Borrelia burgdorferi senses environmental temperature to determine its location in the tick-mammal infectious cycle. However, borreliae cultured at 34°C divide several times faster than do those cultured at 23°C. We developed methods that disassociate bacterial growth rate and temperature, allowing a separate evaluation of each factor's impacts on B. burgdorferi gene and protein expression. Altogether, the data support a new paradigm that B. burgdorferi actually responds to changes in its own replication rate, not temperature per se, as the impetus to increase the expression of the OspC and Erp infection-associated proteins.V ector-borne pathogens, such as the Lyme disease spirochete, Borrelia burgdorferi, have overcome the challenges of persisting within two very different animal environments and possess mechanisms to efficiently transmit back and forth between vertebrate hosts and arthropod vectors. To facilitate this complex lifestyle, the bacterium produces specific proteins appropriate for each step in the infectious cycle. Considerable effort has been expended to identify the mechanisms by which B. burgdorferi senses its environment and accordingly regulates gene expression (1, 2). Such information both provides insight into pathogenic mechanisms and identifies new targets for preventative and curative therapies.One of the first studies to delve into the mechanisms of B. burgdorferi gene regulation focused on OspC (outer surface protein C). The exact function of that protein remains to be elucidated, but it is necessary for the establishment of mammalian infection (3)(4)(5)(6)(7)(8)(9)(10). In a landmark study in 1995, Schwan et al. demonstrated that synthesis of OspC is repressed in bacteria within unfed ticks, yet OspC production is induced as those ticks begin to feed (11). Furthermore, they showed that regulation of OspC synthesis can be recapitulated in culture: the protein is poorly expressed by bacteria cultured at 23°C but is abundantly expressed by bacteria that are first grown at 23°C, diluted into fresh medium, and then cultured at 34°C to 37°C (11).Shortly thereafter, it was demonstrated that increasing the culture temperature from 23°C to 34°C enhances the production of several other antigenic proteins (12). Among these are a paralogous family of outer surface lipoproteins designated Erp (OspE/ OspF-related proteins) (12-15). Erp proteins are expressed throughout vertebrate infection, adhere to various host factors, and appear to play roles in dissemination and colonization (16)(17)(18)(19)(20)(21)(22)(23)(24)(25). As with ospC, erp transcription is repressed during tick colonization and induced during tick feedin...

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“…monocytogenes, where BCFAs comprise 75 to 98% of the membrane (13, 14, 16, 21, 142). BCFA-deficient strains have increased susceptibility to antimicrobial peptide killing and lysozyme digestion and decreased production of the virulence factor listeriolysin O (143), all of which likely contribute to the decreased intracellular growth and virulence of a strain deficient of BCFAs (143, 144). In S.…”

Section: Bcaas At the Crossroads Of Metabolism And Virulencementioning

confidence: 99%

Branching Out: Alterations in Bacterial Physiology and Virulence Due to Branched-Chain Amino Acid Deprivation

Kaiser

Heinrichs

2018

mBio

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The branched-chain amino acids (BCAAs [Ile, Leu, and Val]) represent important nutrients in bacterial physiology, with roles that range from supporting protein synthesis to signaling and fine-tuning the adaptation to amino acid starvation. In some pathogenic bacteria, the adaptation to amino acid starvation includes induction of virulence gene expression: thus, BCAAs support not only proliferation during infection, but also the evasion of host defenses.

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Fatty Acids Regulate Stress Resistance and Virulence Factor Production for Listeria monocytogenes

Cited by 98 publications

References 64 publications

Short branched-chain C6 carboxylic acids result in increased growth, novel ‘unnatural’ fatty acids and increased membrane fluidity in a Listeria monocytogenes branched-chain fatty acid-deficient mutant

Short branched-chain C6 carboxylic acids result in increased growth, novel ‘unnatural’ fatty acids and increased membrane fluidity in a Listeria monocytogenes branched-chain fatty acid-deficient mutant

Changes in Bacterial Growth Rate Govern Expression of the Borrelia burgdorferi OspC and Erp Infection-Associated Surface Proteins

Branching Out: Alterations in Bacterial Physiology and Virulence Due to Branched-Chain Amino Acid Deprivation

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