Analysis of the transcriptome of Legionella pneumophila hfq mutant reveals a new mobile genetic element

Microbiology (United Kingdom)

Volumn 159, Issue 8, 2013, Pages 1649-1660

  Trigui, Hana ^a   Dudyk, Paulina ^a   Sum, Janet ^b   Shuman, Howard A ^b,c   Faucher, Sebastien P ^a  

^a MCGILL UNIVERSITY   (Canada)

^b NewYork Presbyterian Hospital   (United States)

^c UNIVERSITY OF CHICAGO   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

COPPER; COPPER EXPORTING ADENOSINE TRIPHOSPHATASE; HFQ PROTEIN; RNA BINDING PROTEIN; TRANSCRIPTOME; UNCLASSIFIED DRUG;

ARTICLE; BACTERIAL STRAIN; DELETION MUTANT; GENE DOSAGE; GENE MUTATION; GENE OVEREXPRESSION; GENOMIC ISLAND; LEGIONELLA PNEUMOPHILA; MICROARRAY ANALYSIS; NONHUMAN; NUCLEOTIDE SEQUENCE; POLYMERASE CHAIN REACTION; PRIORITY JOURNAL;

GENE DELETION; GENOME, BACTERIAL; HOST FACTOR 1 PROTEIN; INTERSPERSED REPETITIVE SEQUENCES; LEGIONELLA PNEUMOPHILA; PLASMIDS; POLYMERASE CHAIN REACTION; RECOMBINATION, GENETIC; TRANSCRIPTOME;

EID: 84881236876     PISSN: 13500872     EISSN: 14652080     Source Type: Journal    
DOI: 10.1099/mic.0.067983-0     Document Type: Article

References (48)

1. Aiba, H. (2007). Mechanism of RNA silencing by Hfq-binding small RNAs. Curr Opin Microbiol 10, 134-139.
2. Altman, E. & Segal, G. (2008). The response regulator CpxR directly regulates expression of several Legionella pneumophila icm/dot components as well as new translocated substrates. J Bacteriol 190, 1985-1996.
3. Amaro, F., Gilbert, J. A., Owens, S., Trimble, W. & Shuman, H. A. (2012). Whole-genome sequence of the human pathogen Legionella pneumophila serogroup 12 strain 570-CO-H. J Bacteriol 194, 1613-1614.
4. Beaber, J. W., Hochhut, B. & Waldor, M. K. (2004). SOS response promotes horizontal dissemination of antibiotic resistance genes. Nature 427, 72-74.
5. Brassinga, A. K. C., Hiltz, M. F., Sisson, G. R., Morash, M. G., Hill, N., Garduno, E., Edelstein, P. H., Garduno, R. A. & Hoffman, P. S. (2003). A 65-kilobase pathogenicity island is unique to Philadelphia-1 strains of Legionella pneumophila. J Bacteriol 185, 4630-4637.
6. Cazalet, C., Rusniok, C., Bruggemann, H., Zidane, N., Magnier, A., Ma, L., Tichit, M., Jarraud, S., Bouchier, C. & other authors (2004). Evidence in the Legionella pneumophila genome for exploitation of host cell functions and high genome plasticity. Nat Genet 36, 1165-1173.
7. Charpentier, X., Faucher, S. P., Kalachikov, S. & Shuman, H. A. (2008). Loss of RNase R induces competence development in Legionella pneumophila. J Bacteriol 190, 8126-8136.
8. Chen, D.-Q., Huang, S.-S. & Lu, Y.-J. (2006). Efficient transformation of Legionella pneumophila by high-voltage electroporation. Microbiol Res 161, 246-251.
9. Chien, M., Morozova, I., Shi, S., Sheng, H., Chen, J., Gomez, S. M., Asamani, G., Hill, K., Nuara, J. & other authors (2004). The genomic sequence of the accidental pathogen Legionella pneumophila. Science 305, 1966-1968.
10. D'Auria, G., Jimenez-Hernandez, N., Peris-Bondia, F., Moya, A. & Latorre, A. (2010). Legionella pneumophila pangenome reveals strainspecific virulence factors. BMC Genomics 11, 181.
11. Dagan, T., Artzy-Randrup, Y. & Martin, W. (2008). Modular networks and cumulative impact of lateral transfer in prokaryote genome evolution. Proc Natl Acad Sci U S A 105, 10039-10044.
12. de Felipe, K. S., Glover, R. T., Charpentier, X., Anderson, O. R., Reyes, M., Pericone, C. D. & Shuman, H. A. (2008). Legionella eukaryotic-like type IV substrates interfere with organelle trafficking. PLoS Pathog 4, e1000117.
13. Doleans-Jordheim, A., Akermi, M., Ginevra, C., Cazalet, C., Kay, E., Schneider, D., Buchrieser, C., Atlan, D., Vandenesch, F. & other authors (2006). Growth-phase-dependent mobility of the lvhencoding region in Legionella pneumophila strain Paris. Microbiology 152, 3561-3568.
14. Drolet, M. (2006). Growth inhibition mediated by excess negative supercoiling: the interplay between transcription elongation, R-loop formation and DNA topology. Mol Microbiol 59, 723-730.
15. Faucher, S. P. & Shuman, H. A. (2011). Small regulatory RNA and Legionella pneumophila. Front Microbiol 2, 98.
16. Faucher, S. P. & Shuman, H. A. (2012). Methods to study Legionella transcriptome in vitro and in vivo. Methods in Molecular Biology 954, 567-582.
17. Faucher, S. P., Porwollik, S., Dozois, C. M., McClelland, M. & Daigle, F. (2006). Transcriptome of Salmonella enterica serovar Typhi within macrophages revealed through the selective capture of transcribed sequences. Proc Natl Acad Sci U S A 103, 1906-1911.
18. Faucher, S. P., Friedlander, G., Livny, J., Margalit, H. & Shuman, H. A. (2010). Legionella pneumophila 6S RNA optimizes intracellular multiplication. Proc Natl Acad Sci U S A 107, 7533-7538.
19. Faucher, S., Mueller, C. & Shuman, H. (2011). Legionella pneumophila transcriptome during intracellular multiplication in human macrophages 2, 60.
20. Franco, I. S., Shuman, H. A. & Charpentier, X. (2009). The perplexing functions and surprising origins of Legionella pneumophila type IV secretion effectors. Cell Microbiol 11, 1435-1443.
21. Franze de Fernandez, M. T., Eoyang, L. & August, J. T. (1968). Factor fraction required for the synthesis of bacteriophage Qbeta-RNA. Nature 219, 588-590.
22. Gal-Mor, O. & Segal, G. (2003). The Legionella pneumophila GacA homolog (LetA) is involved in the regulation of icm virulence genes and is required for intracellular multiplication in Acanthamoeba castellanii. Microb Pathog 34, 187-194.
23. Glockner, G., Albert-Weissenberger, C., Weinmann, E., Jacobi, S., Schunder, E., Steinert, M., Hacker, J. & Heuner, K. (2008). Identification and characterization of a new conjugation/type IVA secretion system (trb/tra) of Legionella pneumophila Corby localized on two mobile genomic islands. Int J Med Microbiol 298, 411-428.
24. Gomez-Valero, L., Rusniok, C., Jarraud, S., Vacherie, B., Rouy, Z., Barbe, V., Medigue, C., Etienne, J. & Buchrieser, C. (2011). Extensive recombination events and horizontal gene transfer shaped the Legionella pneumophila genomes. BMC Genomics 12, 536.
25. Hovel-Miner, G., Pampou, S., Faucher, S. P., Clarke, M., Morozova, I., Morozov, P., Russo, J. J., Shuman, H. A. & Kalachikov, S. (2009). SigmaS controls multiple pathways associated with intracellular multiplication of Legionella pneumophila. J Bacteriol 191, 2461-2473.
26. Jayakumar, D., Early, J. V. & Steinman, H. M. (2012). Virulence phenotypes of Legionella pneumophila associated with noncoding RNA lpr0035. Infect Immun 80, 4143-4153.
27. Kessler, A., Schell, U., Sahr, T., Tiaden, A., Harrison, C., Buchrieser, C. & Hilbi, H. (2013). The Legionella pneumophila orphan sensor kinase LqsT regulates competence and pathogen-host interactions as a component of the LAI-1 circuit. Environ Microbiol 15, 646-662.
28. Kim, E.-H., Charpentier, X., Torres-Urquidy, O., McEvoy, M. M. & Rensing, C. (2009). The metal efflux island of Legionella pneumophila is not required for survival in macrophages and amoebas. FEMS Microbiol Lett 301, 164-170.
29. Kovach, M. E., Elzer, P. H., Hill, D. S., Robertson, G. T., Farris, M. A., Roop, R. M., II & Peterson, K. M. (1995). Four new derivatives of the broad-host-range cloning vector pBBR1MCS, carrying different antibiotic-resistance cassettes. Gene 166, 175-176.
30. Lin, Y. E., Stout, J. E. & Yu, V. L. (2011). Controlling Legionella in hospital drinking water: an evidence-based review of disinfection methods. Infect Control Hosp Epidemiol 32, 166-173.
31. Livak, K. J. & Schmittgen, T. D. (2001). Analysis of relative gene expression data using real-time quantitative PCR and the 2-DDCT method. Methods 25, 402-408.
32. Lu, J., Struewing, I., Buse, H. Y., Kou, J., Shuman, H. A., Faucher, S. P. & Ashbolt, N. J. (2013). Legionella pneumophila transcriptional response following exposure to CuO nanoparticles. Appl Environ Microbiol 79, 2713-2720.
33. Luneberg, E., Mayer, B., Daryab, N., Kooistra, O., Zahringer, U., Rohde, M., Swanson, J. & Frosch, M. (2001). Chromosomal insertion and excision of a 30 kb unstable genetic element is responsible for phase variation of lipopolysaccharide and other virulence determinants in Legionella pneumophila. Mol Microbiol 39, 1259-1271.
34. McNealy, T. L., Forsbach-Birk, V., Shi, C. & Marre, R. (2005). The Hfq homolog in Legionella pneumophila demonstrates regulation by LetA and RpoS and interacts with the global regulator CsrA. J Bacteriol 187, 1527-1532.
35. Molofsky, A. B. & Swanson, M. S. (2003). Legionella pneumophila CsrA is a pivotal repressor of transmission traits and activator of replication. Mol Microbiol 50, 445-461.
36. Morales, V. M., Backman, A. & Bagdasarian, M. (1991). A series of wide-host-range low-copy-number vectors that allow direct screening for recombinants. Gene 97, 39-47.
37. Rasis, M. & Segal, G. (2009). The LetA-RsmYZ-CsrA regulatory cascade, together with RpoS and PmrA, post-transcriptionally regulates stationary phase activation of Legionella pneumophila Icm/ Dot effectors. Mol Microbiol 72, 995-1010.
38. Reva, O. & Bezuidt, O. (2012). Distribution of horizontally transferred heavy metal resistance operons in recent outbreak bacteria. Mobile Genet Elements 2, 96-100.
39. Ross, J. A., Wardle, S. J. & Haniford, D. B. (2010). Tn10/IS10 transposition is downregulated at the level of transposase expression by the RNA-binding protein Hfq. Mol Microbiol 78, 607-621.
40. Sadosky, A. B., Wiater, L. A. & Shuman, H. A. (1993). Identification of Legionella pneumophila genes required for growth within and killing of human macrophages. Infect Immun 61, 5361-5373.
41. Sahr, T., Bruggemann, H., Jules, M., Lomma, M., Albert- Weissenberger, C., Cazalet, C. & Buchrieser, C. (2009). Two small ncRNAs jointly govern virulence and transmission in Legionella pneumophila. Mol Microbiol 72, 741-762.
42. Segal, G., Russo, J. J. & Shuman, H. A. (1999). Relationships between a new type IV secretion system and the icm/dot virulence system of Legionella pneumophila. Mol Microbiol 34, 799-809.
43. Tiaden, A., Spirig, T., Sahr, T., Walti, M. A., Boucke, K., Buchrieser, C. & Hilbi, H. (2010). The autoinducer synthase LqsA and putative sensor kinase LqsS regulate phagocyte interactions, extracellular filaments and a genomic island of Legionella pneumophila. Environ Microbiol 12, 1243-1259.
44. Tsui, H. C., Leung, H. C. & Winkler, M. E. (1994). Characterization of broadly pleiotropic phenotypes caused by an hfq insertion mutation in Escherichia coli K-12. Mol Microbiol 13, 35-49.
45. Vogel, J. P., Andrews, H. L., Wong, S. K. & Isberg, R. R. (1998). Conjugative transfer by the virulence system of Legionella pneumophila. Science 279, 873-876.
46. Weissenmayer, B. A., Prendergast, J. G. D., Lohan, A. J. & Loftus, B. J. (2011). Sequencing illustrates the transcriptional response of Legionella pneumophila during infection and identifies seventy novel small non-coding RNAs. PLoS ONE 6, e17570.
47. Wozniak, R. A. F. & Waldor, M. K. (2010). Integrative and conjugative elements: mosaic mobile genetic elements enabling dynamic lateral gene flow. Nat Rev Microbiol 8, 552-563.
48. Zusman, T., Aloni, G., Halperin, E., Kotzer, H., Degtyar, E., Feldman, M. & Segal, G. (2007). The response regulator PmrA is a major regulator of the icm/dot type IV secretion system in Legionella pneumophila and Coxiella burnetii. Mol Microbiol 63, 1508-1523.