Passage through Tetrahymena tropicalis enhances the resistance to stress and the infectivity of Legionella pneumophila

Koubar, Mohamad; Rodier, Marie‐Hélène; Garduño, Rafael A.; Frère, Jacques

doi:10.1111/j.1574-6968.2011.02402.x

Cited by 38 publications

(37 citation statements)

References 20 publications

(42 reference statements)

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“…Increased resistance to antibiotics was also described after incubation of L. pneumophila in Acanthamoeba castellanii buffer for 16 h (12). MIFs are able to resist starvation better than stationary-phase forms in encystment buffer (11), but both forms show similar levels of resistance in distilled water (8).…”

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confidence: 96%

“…Infection of HeLa cells and Tetrahymena tropicalis leads to the differentiation of L. pneumophila into mature infectious forms (MIFs), characterized by ultrastructural changes and accumulation of poly-␤-hydroxybutyrate (8)(9)(10). MIFs are highly infectious and are more resistant to antibiotics and detergent than other forms (9,11). Increased resistance to antibiotics was also described after incubation of L. pneumophila in Acanthamoeba castellanii buffer for 16 h (12).…”

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confidence: 98%

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A Regulatory Feedback Loop between RpoS and SpoT Supports the Survival of Legionella pneumophila in Water

Trigui

Dudyk

et al. 2015

Appl Environ Microbiol

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bLegionella pneumophila is a waterborne pathogen, and survival in the aquatic environment is central to its transmission to humans. Therefore, identifying genes required for its survival in water could help prevent Legionnaires' disease outbreaks. In the present study, we investigate the role of the sigma factor RpoS in promoting survival in water, where L. pneumophila experiences severe nutrient deprivation. The rpoS mutant showed a strong survival defect compared to the wild-type strain in defined water medium. The transcriptome of the rpoS mutant during exposure to water revealed that RpoS represses genes associated with replication, translation, and transcription, suggesting that the mutant fails to shut down major metabolic programs. In addition, the rpoS mutant is transcriptionally more active than the wild-type strain after water exposure. This could be explained by a misregulation of the stringent response in the rpoS mutant. Indeed, the rpoS mutant shows an increased expression of spoT and a corresponding decrease in the level of (p)ppGpp, which is due to the presence of a negative feedback loop between RpoS and SpoT. Therefore, the lack of RpoS causes an aberrant regulation of the stringent response, which prevents the induction of a successful response to starvation. L egionella pneumophila is the causative agent of Legionnaires' disease. It is widely distributed in natural freshwater systems (1) and readily colonizes man-made water systems such as cooling towers and water distribution systems (2). L. pneumophila persists in aquatic environments thanks to its ability to adapt to a variety of different ecological niches, either as an intracellular parasite of amoebae or ciliate protozoans, as a free-living member of complex biofilm communities, or as planktonic cells (3, 4). Amoebae support intracellular multiplication of L. pneumophila, and protect against suboptimal growth conditions and exposure to chlorine (5-7). Infection of HeLa cells and Tetrahymena tropicalis leads to the differentiation of L. pneumophila into mature infectious forms (MIFs), characterized by ultrastructural changes and accumulation of poly-␤-hydroxybutyrate (8-10). MIFs are highly infectious and are more resistant to antibiotics and detergent than other forms (9, 11). Increased resistance to antibiotics was also described after incubation of L. pneumophila in Acanthamoeba castellanii buffer for 16 h (12). MIFs are able to resist starvation better than stationary-phase forms in encystment buffer (11), but both forms show similar levels of resistance in distilled water (8).In the free-living state outside the amoebal host, L. pneumophila encounters stressful conditions, such as limited nutrient availability in aquatic systems (1, 13). Nevertheless, previous studies have shown that L. pneumophila is able to survive for long periods (up to 1.5 years) in sterilized tap, surface and estuarine waters (14-17). The genetic determinants underlying the ability of L. pneumophila to survive in its natural habitat of low-nutrient water for a...

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confidence: 96%

mentioning

confidence: 98%

A Regulatory Feedback Loop between RpoS and SpoT Supports the Survival of Legionella pneumophila in Water

Trigui

Dudyk

et al. 2015

Appl Environ Microbiol

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“…was reported for E. coli O157:H7 (44,45), L. pneumophila (35), S. enterica (33,46), and E. coli K-12 (47). A few dead cells were observed after 24 h of coincubation (Fig.…”

Section: Discussionmentioning

confidence: 94%

“…Bacteria packaged and excreted in MLBs have greater resistance to unfavorable conditions (32)(33)(34). For example, it was shown that L. pneumophila packaged in MLBs by the ciliate Tetrahymena tropicalis was more infectious and displayed greater resistance to gentamicin and longer survival in a nutrient-poor environment, compared to the planktonic state (35).…”

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confidence: 99%

Packaging of Campylobacter jejuni into Multilamellar Bodies by the Ciliate Tetrahymena pyriformis

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Paquet

Charette

et al. 2016

Appl Environ Microbiol

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dCampylobacter jejuni is the leading cause of bacterial gastroenteritis worldwide. Transmission to humans occurs through consumption of contaminated food or water. The conditions affecting the persistence of C. jejuni in the environment are poorly understood. Some protozoa package and excrete bacteria into multilamellar bodies (MLBs). Packaged bacteria are protected from deleterious conditions, which increases their survival. We hypothesized that C. jejuni could be packaged under aerobic conditions by the amoeba Acanthamoeba castellanii or the ciliate Tetrahymena pyriformis, both of which are able to package other pathogenic bacteria. A. castellanii did not produce MLBs containing C. jejuni. In contrast, when incubated with T. pyriformis, C. jejuni was ingested, packaged in MLBs, and then expelled into the milieu. The viability of the bacteria inside MLBs was confirmed by microscopic analyses. The kinetics of C. jejuni culturability showed that packaging increased the survival of C. jejuni up to 60 h, in contrast to the strong survival defect seen in ciliate-free culture. This study suggests that T. pyriformis may increase the risk of persistence of C. jejuni in the environment and its possible transmission between different reservoirs in food and potable water through packaging. Campylobacter jejuni is a leading cause of human gastroenteritis worldwide and a major public health problem (1-3). Severe symptoms of C. jejuni infection include high fever, watery to bloody diarrhea, nausea, and vomiting (4). In severe cases, C. jejuni is associated with serious postinfectious complications, such as Guillain-Barré syndrome (5, 6).Despite causing a serious disease in humans, C. jejuni is usually viewed as commensal in chickens (7) and livestock animals such as cattle (8) and pigs (9). Once these animals are colonized with Campylobacter spp., they excrete large numbers of the microorganisms in their feces and commonly contaminate different aquatic habitats, such as surface waters close to farming activities, agricultural runoff, wastewater effluent, sewage, and marine environments (10). Numerous epidemiological studies have demonstrated that water is not only a significant reservoir of C. jejuni but also an important factor for the spread of C. jejuni in farms, throughout flocks, and in slaughterhouses (11-15).C. jejuni requires a microaerobic environment (80% N 2 , 10% CO 2 , 5% H 2 , and 5% O 2 ) (16) and a narrow range of temperatures (37 to 43°C) for optimal growth (17). Because of the constraints imposed by its sensitivity to oxygen, C. jejuni is considered less able to tolerate environmental stress than other foodborne pathogens (18). Once outside the host, however, the interaction of C. jejuni with other microorganisms could help it survive high concentrations of oxygen and other environmental stresses.Since the study by Snelling et al. (19), in which Campylobacter and protozoa were isolated from the same broiler drinking water systems, the potential interactions between these microorganisms have been investigate...

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“…This is why Tetrahymena infection is very dangerous to many fish species [69]. However, not only fishes but also mammals, including human, are touched by different infections, as by a similar way, the L. pneumophila [70,71] and Salmonella enterica [72], causing diseases, are transported. In addition, in some cases, the microbes during their stay in the phagocytic vesicles can be transformed to more pathogenic 284 CSABA and hypervirulent forms [73].…”

Section: Discussionmentioning

confidence: 99%

Lectins and Tetrahymena – A review

Csaba

2016

Acta Microbiologica et Immunologica Hungarica

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The unicellular ciliate Tetrahymena is a complete organism, one of the most highly developed protozoans, which has specialized organelles performing each of the functions characteristic to the cells of higher ranked animals. It is also able to produce, store, and secrete hormones of higher ranked animals and also react to them. It produces lectins that can bind them and has functions, which are influenced by exogenous lectins. The review lists the observations on the relationship between lectins and Tetrahymena and try to construe them on the basis of the data, which are at our disposal. Considering the data, lectins can be used by Tetrahymena as materials for influencing conjugation, for stimulating hormone receptors, and by this, mimic the hormonal functions. Lectins can influence phagocytosis and movement of the cells as well as the cell division. As Tetrahymena can recognize both related and hostile cells by the help of lectins and surface sugars, it could be surmised a complex predator-prey system. This could determine the survival of the population as well as the nourishment conditions. When Tetrahymena is pathogenic, it can use lectins as virulence factors.

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Passage through Tetrahymena tropicalis enhances the resistance to stress and the infectivity of Legionella pneumophila

Cited by 38 publications

References 20 publications

A Regulatory Feedback Loop between RpoS and SpoT Supports the Survival of Legionella pneumophila in Water

A Regulatory Feedback Loop between RpoS and SpoT Supports the Survival of Legionella pneumophila in Water

Packaging of Campylobacter jejuni into Multilamellar Bodies by the Ciliate Tetrahymena pyriformis

Lectins and Tetrahymena – A review

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