Developmental Changes During the Formation and Breaking of the Dormant State in Bacteria

Halvorson, H. O.; Vary, James C.; Steinberg, William M.

doi:10.1146/annurev.mi.20.100166.001125

Cited by 76 publications

(28 citation statements)

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“…It is known, however, that persister cells revert to a susceptible state, or to an awakened state, upon reinoculation into fresh medium (2,28), in the presence of sugar metabolites (18), in the presence of environmental signals (97,98), by stochastic exit from dormancy (99, 100), or upon the addition of spent medium to preformed persister cells (17). Under these conditions, reversion to a susceptible state correlates with a sudden burst of transcription and translation (55) and the production of proteins necessary to perform cell repair (101). However, no reports have demonstrated that persister cells awake due to the presence of a specific signaling molecule.…”

Section: Discussionmentioning

confidence: 99%

The Fatty Acid Signaling Molecule cis -2-Decenoic Acid Increases Metabolic Activity and Reverts Persister Cells to an Antimicrobial-Susceptible State

Marques

Morozov

Planzos

et al. 2014

Appl Environ Microbiol

125

112

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bPersister cells, which are tolerant to antimicrobials, contribute to biofilm recalcitrance to therapeutic agents. In turn, the ability to kill persister cells is believed to significantly improve efforts in eradicating biofilm-related, chronic infections. While much research has focused on elucidating the mechanism(s) by which persister cells form, little is known about the mechanism or factors that enable persister cells to revert to an active and susceptible state. Here, we demonstrate that cis-2-decenoic acid (cis-DA), a fatty acid signaling molecule, is able to change the status of Pseudomonas aeruginosa and Escherichia coli persister cells from a dormant to a metabolically active state without an increase in cell number. This cell awakening is supported by an increase of the persister cells' respiratory activity together with changes in protein abundance and increases of the transcript expression levels of several metabolic markers, including acpP, 16S rRNA, atpH, and ppx. Given that most antimicrobials target actively growing cells, we also explored the effect of cis-DA on enhancing antibiotic efficacy in killing persister cells due to their inability to keep a persister cell state. Compared to antimicrobial treatment alone, combinational treatments of persister cell subpopulations with antimicrobials and cis-DA resulted in a significantly greater decrease in cell viability. In addition, the presence of cis-DA led to a decrease in the number of persister cells isolated. We thus demonstrate the ability of a fatty acid signaling molecule to revert bacterial cells from a tolerant phenotype to a metabolically active, antimicrobial-sensitive state. P ersister cells are considered to be a subpopulation of stochastically produced, nongrowing (dormant) cells present in biofilm and planktonic bacterial cultures. Persister cells account for 10 Ϫ6 to 10 Ϫ4 of the total cell population of mid-exponential-phase cells and up to 1% of the total cell population of stationary-phase cells and biofilms, a pattern resembling that of a quorum-sensing mechanism (1-3). Tolerance to antimicrobials is one of the key characteristics of this subpopulation, as persisters escape killing by antimicrobials such as fluoroquinolones, which can kill slowgrowing bacteria but not dormant cells (4). It is therefore not surprising that persister cells are considered to play a major role in the resilience of bacterial populations and have recently been isolated from patients with candidiasis, from cystic fibrosis patients with chronic lung infections, and from Mycobacterium tuberculosis biofilms responsible for chronic tuberculosis (5-8).Several mechanisms have been described to contribute to persister cell formation. For instance, several genes involved in energy generation and cell maintenance have been shown to be downregulated in persister cells, further indicating that persisters are nongrowing, dormant cells (1). Among these genes were members of several operons involved in oxidative phosphorylation, including NADH dehydrogenase, ATP syn...

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Section: Discussionmentioning

confidence: 99%

The Fatty Acid Signaling Molecule cis -2-Decenoic Acid Increases Metabolic Activity and Reverts Persister Cells to an Antimicrobial-Susceptible State

Marques

Morozov

Planzos

et al. 2014

Appl Environ Microbiol

125

112

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“…Controls with no CA addition germinated, as confirmed by lack of growth in TG broth after heat shocking. Although bacterial spores may remain viable under extreme environmental conditions, germination may be inhibited by minor physical or chemical changes (Gould et al, 1970;Halvorson et al, 1966). Relatively small amounts of a chemical agent can be sporostatic, yet considerably higher concentrations are required to render spores non-viable or to inhibit vegetative cell growth (Bowles, 1991;Bowles and Miller 1993a,b;Smith and Dawes, 1989).…”

Section: Resultsmentioning

confidence: 99%

“…Unsupplemented cultures contained 80 and 152.7 pgDPA/mL after 9 and 24 hr at 32"C, respectively. During initial germination phases, degradative processes of cortex embedded lytic en- zymes alter spore permeability with concomitant DPA release (Gould et al, 1970;Halvorson et al, 1966). Reduced DPA release suggested that CA precluded changes in spore coat permeability (Halvorson et al, 1966).…”

Section: Resultsmentioning

confidence: 99%

“…CA inhibitions may be attributed to its reactivity at 80°C and changes in the tertiary structure or spore coat proteins. Mild heating activates bacterial spores by inducing spore coat structural changes (Gould et al, 1970;Halvorson, et al, 1966). Thus, spore core incorporation of CA may be enhanced with subsequent structural damage that render spores non-viable.…”

Section: Resultsmentioning

confidence: 99%

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Caffeic Acid Activity Against Clostridium botulinum Spores

Bowles

Miller

1994

Journal of Food Science

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Caffeic acid (CA) is widely distributed among higher fruits and vegetables. While CA has antimicrobial activity, little information exists on its utility as a food additive. As such, CA was tested for activity against Clostridium botulinum spores. At 0.78 and 3.25 mM, CA inhibited germination for 6 and 24 hr, respectively, with >lOO mM required to render spores nonviable. CA concentrations 5: 50mM reduced 80°C spore thermal resistance. Sporostatic activity was retained when tested in commercial meat broths, and 5.0 mM CA delayed toxigenesis. Caffeic acid has potential as a food additive to inhibit growth of C. botulinurn, and reduce thermal processing requirements of heat sensitive foods.

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“…In Bacillus cspeies, messenger RNA (mRNA) wass ynthesized de novo after the activation of spores and no stored mRNA appears to exist in spores (Halvorson et al 1966;Rodenberg et al 1968). Therefore, mRNA synthesis necessary for germination of bacterial spores should be induced after the initiation of germination, and then protein synthesis may be initiated.…”

Section: Discussionmentioning

confidence: 99%

MACROMOLECULE SYNTHESIS AND GERMINATION OF CONIDIA IN TEMPERATURE SENSITIVE MUTANTS OF <i>NEUROSPORA CRASSA</i>

Inoue

Ishikawa

1970

The Japanese journal of genetics

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Developmental Changes During the Formation and Breaking of the Dormant State in Bacteria

Cited by 76 publications

References 0 publications

The Fatty Acid Signaling Molecule cis -2-Decenoic Acid Increases Metabolic Activity and Reverts Persister Cells to an Antimicrobial-Susceptible State

The Fatty Acid Signaling Molecule cis -2-Decenoic Acid Increases Metabolic Activity and Reverts Persister Cells to an Antimicrobial-Susceptible State

Caffeic Acid Activity Against Clostridium botulinum Spores

MACROMOLECULE SYNTHESIS AND GERMINATION OF CONIDIA IN TEMPERATURE SENSITIVE MUTANTS OF <i>NEUROSPORA CRASSA</i>

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