A
 Legionella pneumophila
 Peptidyl-Prolyl
 cis
 -
 trans
 Isomerase Present in Culture Supernatants Is Necessary for Optimal Growth at Low Temperatures

Söderberg, Maria A.; Cianciotto, Nicholas P.

doi:10.1128/aem.02512-07

Cited by 38 publications

(47 citation statements)

References 44 publications

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“…For example, when 130b is grown in BYE broth at 37°C, the secretome encompasses more than 25 proteins, including many degradative enzymes as well as proteins with no similarity to known proteins (2-4, 6, 10, 11, 19, 20, 23, 31, 49-51). Also, 2D polyacrylamide gel electrophoresis analysis of supernatants produced during growth at 12 to 17°C revealed other exoproteins that are more pronounced at low temperatures (55). Although more work is needed to identify the critical secreted factors, the new data presented here significantly increase our appreciation for the role that type II secretion plays in Legionella ecology.…”

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confidence: 67%

Importance of Type II Secretion for Survival of Legionella pneumophila in Tap Water and in Amoebae at Low Temperatures

Söderberg

Dao

Starkenburg

et al. 2008

Appl Environ Microbiol

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Legionella pneumophila type II secretion mutants showed reduced survival in both tap water at 4 to 17°C and aquatic amoebae at 22 to 25°C. Wild-type supernatants stimulated the growth of these mutants, indicating that secreted factors promote low-temperature survival. There was a correlation between low-temperature survival and secretion function when 12 additional Legionella species were examined.Legionella pneumophila is widespread in natural and manmade water systems (8,21,29,39,41,47,53,64). In these habitats, L. pneumophila exists planktonically, within protozoa, and in biofilms (14,35,36,41,45). The ubiquity of L. pneumophila is also a result of the organism's ability to survive at many temperatures, including ones as low as 4°C (21,29,62,64). L. pneumophila is an important pathogen of humans, with the inhalation of contaminated water droplets originating from aerosol-generating devices resulting in Legionnaires' disease (16). Given the manner in which infection occurs, it is important to better understand how legionellae survive in water, in protozoa, and at low temperatures. Recently, we found that L. pneumophila type II protein secretion is critical for growth in rich broth or agar at 12 to 25°C but not in medium at 30 to 37°C (56). Operative in many gram-negatives (9), type II secretion is a multistep process in which proteins are translocated across the inner membrane in a Sec-or Tat-dependent manner, recognized in the periplasm, and then delivered to the T2S apparatus, whereupon a pilus-like structure "pushes" proteins through a dedicated outer membrane pore or secretin (28).To investigate the connection between type II secretion and low-temperature survival under conditions that more closely mimic natural habitats, we compared wild-type serogroup 1 strain 130b (Table 1) and its type II secretion mutants for persistence in tap water incubated at 37°C, 25°C, and 17°C. We used three mutants: NU258, containing a mutation in the genes encoding the type II outer membrane secretin (lspD) and the inner membrane ATPase (lspE); NU275, containing a mutation in the gene for the inner membrane platform protein (lspF); and NU272 mutated in the gene encoding the pseudopilin peptidase (pilD) (51). Tap water was obtained from laboratory sinks and filter sterilized. Following growth at 37°C in buffered yeast extract (BYE) broth to late log phase (56), wild types and mutants were inoculated into flasks containing 50 ml of the tap water, and then the cultures were incubated with shaking. As with other wild-type L. pneumophila (30,41,42,54,57), 130b persisted in low-temperature tap water for extended times (Fig. 1). Also similar to previous work (27), the recovery of CFU was maintained for a longer period at low temperatures below 37°C. But across the 17 to 37°C range, the secretion mutants behaved differently than their parent (Fig. 1). At 37°C, the mutants displayed a greater recoverability than 130b between days 7 and 20 (P Ͻ 0.05). In a similar vein, at 25°C, the mutants were recovered more than the wild type was be...

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confidence: 67%

Importance of Type II Secretion for Survival of Legionella pneumophila in Tap Water and in Amoebae at Low Temperatures

Söderberg

Dao

Starkenburg

et al. 2008

Appl Environ Microbiol

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“…The T2S mutants are not impaired for entry into the amoebae, indicating that T2S is promoting bacterial resistance to intracellular killing and/or facilitating replication itself (22). Others of our studies have shown that T2S also promotes the persistence of L. pneumophila in the environment by facilitating extracellular survival in low-temperature water samples (18,(22)(23)(24)(25). Furthermore, L. pneumophila T2S helps to mediate the secretion of a surfactant that confers both sliding motility and antibacterial activity (26,27).…”

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confidence: 87%

Multiple Legionella pneumophila Type II Secretion Substrates, Including a Novel Protein, Contribute to Differential Infection of the Amoebae Acanthamoeba castellanii, Hartmannella vermiformis, and Naegleria lovaniensis

et al. 2013

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Type II protein secretion (T2S) by Legionella pneumophila is required for intracellular infection of host cells, including macrophages and the amoebae Acanthamoeba castellanii and Hartmannella vermiformis. Previous proteomic analysis revealed that T2S by L. pneumophila 130b mediates the export of >25 proteins, including several that appeared to be novel. Following confirmation that they are unlike known proteins, T2S substrates NttA, NttB, and LegP were targeted for mutation. nttA mutants were impaired for intracellular multiplication in A. castellanii but not H. vermiformis or macrophages, suggesting that novel exoproteins which are specific to Legionella are especially important for infection. Because the importance of NttA was host cell dependent, we examined a panel of T2S substrate mutants that had not been tested before in more than one amoeba. As a result, RNase SrnA, acyltransferase PlaC, and metalloprotease ProA all proved to be required for optimal intracellular multiplication in H. vermiformis but not A. castellanii. Further examination of an lspF mutant lacking the T2S apparatus documented that T2S is also critical for infection of the amoeba Naegleria lovaniensis. Mutants lacking SrnA, PlaC, or ProA, but not those deficient for NttA, were defective in N. lovaniensis. Based upon analysis of a double mutant lacking PlaC and ProA, the role of ProA in H. vermiformis was connected to its ability to activate PlaC, whereas in N. lovaniensis, ProA appeared to have multiple functions. Together, these data document that the T2S system exports multiple effectors, including a novel one, which contribute in different ways to the broad host range of L. pneumophila.

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“…The Lsp system presumably secretes factors that aid L. pneumophila persistence at low temperatures, as the growth of lsp mutants was stimulated by the addition of culture supernatant from the wild-type strain (310). One of these factors is a secreted peptidyl-prolyl cis-trans isomerase present in the culture supernatant (308). Additional factors were recently identified from a transposon mutant screen for growth defects at low temperatures.…”

Section: The Lsp Type II Secretion Systemmentioning

confidence: 99%

Molecular Pathogenesis of Infections Caused byLegionella pneumophila

Newton¹,

et al. 2010

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SUMMARY The genus Legionella contains more than 50 species, of which at least 24 have been associated with human infection. The best-characterized member of the genus, Legionella pneumophila, is the major causative agent of Legionnaires' disease, a severe form of acute pneumonia. L. pneumophila is an intracellular pathogen, and as part of its pathogenesis, the bacteria avoid phagolysosome fusion and replicate within alveolar macrophages and epithelial cells in a vacuole that exhibits many characteristics of the endoplasmic reticulum (ER). The formation of the unusual L. pneumophila vacuole is a feature of its interaction with the host, yet the mechanisms by which the bacteria avoid classical endosome fusion and recruit markers of the ER are incompletely understood. Here we review the factors that contribute to the ability of L. pneumophila to infect and replicate in human cells and amoebae with an emphasis on proteins that are secreted by the bacteria into the Legionella vacuole and/or the host cell. Many of these factors undermine eukaryotic trafficking and signaling pathways by acting as functional and, in some cases, structural mimics of eukaryotic proteins. We discuss the consequences of this mimicry for the biology of the infected cell and also for immune responses to L. pneumophila infection.

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A Legionella pneumophila Peptidyl-Prolyl cis - trans Isomerase Present in Culture Supernatants Is Necessary for Optimal Growth at Low Temperatures

Cited by 38 publications

References 44 publications

Importance of Type II Secretion for Survival of Legionella pneumophila in Tap Water and in Amoebae at Low Temperatures

Importance of Type II Secretion for Survival of Legionella pneumophila in Tap Water and in Amoebae at Low Temperatures

Multiple Legionella pneumophila Type II Secretion Substrates, Including a Novel Protein, Contribute to Differential Infection of the Amoebae Acanthamoeba castellanii, Hartmannella vermiformis, and Naegleria lovaniensis

Molecular Pathogenesis of Infections Caused byLegionella pneumophila

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