Isolation of protozoa from water associated with a legionellosis outbreak and demonstration of intracellular multiplication of Legionella pneumophila

Barbaree, James M.; Fields, Barry S.; Feeley, James C.; Gorman, George W.; Martin, W. J.

doi:10.1128/aem.51.2.422-424.1986

Cited by 198 publications

(95 citation statements)

References 13 publications

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“…For instance, coculture experiments in liquid media have shown that amoebae exert an important growth-promoting effect on L. pneumophila. During outbreaks of Legionnaire's disease, the water bodies concerned are usually found to contain significant numbers of free-living amoebae; furthermore, high numbers of Legionella species are found when concentrations of amoebae are high (Barbaree et al, 1986). Moreover, the isolation of L. pneumophila from water is more successful if amoebae are added (Sanden et al, 1992).…”

Section: Introductionmentioning

confidence: 99%

Free-living freshwater amoebae differ in their susceptibility to the pathogenic bacteriumLegionella pneumophila

Dey

Bodennec

Mameri

et al. 2009

FEMS Microbiology Letters

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Legionella pneumophila is known as a facultative intracellular parasite of free-living soil and freshwater amoebae, of which several species have been shown to support the growth of the pathogenic bacteria. We report for the first time the behaviour of two strains (c2c and Z503) of the amoeba Willaertia magna towards different strains of L. pneumophila serogroup 1 and compared it with Acanthamoeba castellanii and Hartmannella vermiformis, known to be L. pneumophila permissive. In contrast to the results seen with other amoebae, W. magna c2c inhibited the growth of one strain of Legionella (L. pneumophila, Paris), but not of others belonging to the same serogroup (L. pneumophila, Philadelphia and L. pneumophila, Lens). Also, the different L. pneumophila inhibited cell growth and induced cell death in A. castellanii, H. vermiformis and W. magna Z503 within 3-4 days while W. magna c2c strain remained unaffected even up to 7 days. Electron microscopy demonstrated that the formation of numerous replicative phagosomes observed within Acanthamoeba and Hartmannella is rarely seen in W. magna c2c cocultured with L. pneumophila. Moreover, the morphological differences were observed between L. pneumophila cultured either with Willaertia or other amoebae. These observations show that amoebae are not all equally permissive to L. pneumophila and highlight W. magna c2c as particularly resistant towards some strains of this bacterium.

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Section: Introductionmentioning

confidence: 99%

Free-living freshwater amoebae differ in their susceptibility to the pathogenic bacteriumLegionella pneumophila

Dey

Bodennec

Mameri

et al. 2009

FEMS Microbiology Letters

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“…Grazing by heterotrophic protists is a major source of bacterial mortality in soil (Clarholm, 1981;Ekelund et al, 2002), marine (Barbaree et al, 1986;Epstein & Shiaris, 1992) and freshwater (Sanders et al, 1989;Iriberri et al, 1995) systems and is considered to be a major trophic pathway whereby the biomass produced by bacteria, cyanobacteria and algae re-enters the food web (Azam et al, 1983).…”

Section: Introductionmentioning

confidence: 99%

“…Nonetheless, not all bacteria are ingested and digested by protozoa, some escape protozoan ingestion for a number of reasons, including their cell size (Šimek & Chrzanowski, 1992;Jürgens & DeMott, 1995;Kinner et al, 1998;Posch et al, 1999). Some are ingested but have evolved strategies of evading digestion and even multiplying within protozoa, the prototypical example being Legionella pneumphila (Rowbotham, 1980;Barbaree et al, 1986;Brown & Barker, 1994;Molmeret et al, 2005). It is also frequently reported that L. pneumophila uses similar mechanisms to invade protozoan and mammalian cell lines (Segal & Shuman, 1999;Molmeret et al, 2005); thus protozoa have been termed as 'trojan horses' (Brown & Barker, 1994) or 'biological gymnasia' whereby intraprotozoan cells train for their encounter with the more evolved mammalian cells (Harb et al, 2000).…”

Section: Introductionmentioning

confidence: 99%

Interactions of some common pathogenic bacteria with Acanthamoeba polyphaga

Huws

Morley

Jones

et al. 2008

FEMS Microbiology Letters

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Protozoan grazing is a major trophic pathway whereby the biomass re-enters the food web. Nonetheless, not all bacteria are digested by protozoa and the number known to evade digestion, resulting in their environmental augmentation, is increasing. We investigated the interactions of Bacillus cereus, Enterococcus faecalis, Enteropathogenic Escherichia coli (EPEC), Listeria monocytogenes, Salmonella enterica serovar Typhimurium, and methicillin-sensitive Staphylococcus aureus (MSSA), with the amoeba, Acanthamoeba polyphaga. There was evidence of predation of all bacterial species except L. monocytogenes and S. aureus, where extracellular numbers were significantly higher when cultured with amoebae compared with growth in the absence of amoebae. Intracellular growth kinetic experiments and fluorescent confocal microscopy suggest that S. aureus survived and may even multiply within A. polyphaga, whereas there was no apparent intra-amoebal replication of L. monocytogenes and higher numbers were likely sustained on metabolic waste products released during coculture.

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“…Tetrahymena spp. are ciliated protozoa that, depending on the incubation temperature, can support the growth of Legionella (Fields et al, 1984;Barbaree et al, 1986;Berk et al, 2008). In the species Tetrahymena tropicalis, L. pneumophila is efficiently ingested but does not replicate inside food vacuoles, in spite of resisting digestion.…”

Section: Introductionmentioning

confidence: 99%

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

Koubar

Rodier

Garduño

et al. 2011

FEMS Microbiol Lett

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Legionella pneumophila is a gram-negative bacterium prevalent in fresh water which accidentally infects humans and is responsible for the disease called legionellosis. Intracellular growth of L. pneumophila in Tetrahymena is inconsistent; in the species Tetrahymena tropicalis stationary-phase forms (SPFs) of L. pneumophila differentiate into mature intracellular forms (MIFs) without apparent bacterial replication and are expelled from the ciliate as pellets containing numerous MIFS. In the present work, we tested the impact of L. pneumophila passage through T. tropicalis. We observed that MIFs released from T. tropicalis are more resistant to various stresses than SPFs. Under our conditions, MIFs harboured a higher gentamicin resistance, maintained even after 3 months as pellets. Long-term survival essays revealed that MIFs survived better in a nutrient-poor environment than SFPs, as a reduction of only about 3 logs was observed after 4 months in the MIF population, whereas no cultivable SPFs were detected after 3 months in the same medium, corresponding to a loss of about 7 logs. We have also observed that MIFs are significantly more infectious in human pneumocyte cells compared with SPFs. These results strongly suggest a potential role of ciliates in increasing the risk of legionellosis.

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Isolation of protozoa from water associated with a legionellosis outbreak and demonstration of intracellular multiplication of Legionella pneumophila

Cited by 198 publications

References 13 publications

Free-living freshwater amoebae differ in their susceptibility to the pathogenic bacteriumLegionella pneumophila

Free-living freshwater amoebae differ in their susceptibility to the pathogenic bacteriumLegionella pneumophila

Interactions of some common pathogenic bacteria with Acanthamoeba polyphaga

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

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