Advances in genetic manipulation of obligate intracellular bacterial pathogens

Frontiers in Microbiology

Volumn 2, Issue MAY, 2011, Pages

  Beare, Paul A ^a   Sandoz, Kelsi M ^b   Omsland, Anders ^a   Rockey, Daniel D ^b   Heinzen, Robert A ^a  

^a NATIONAL INSTITUTES OF HEALTH   (United States)

^b OREGON STATE UNIVERSITY   (United States)

Author keywords

Allelic exchange; Antibiotic selection; Complementation; Electroporation; Genetic transformation; Shuttle vector; Transposon mutagenesis; Virulence factor

Indexed keywords

EID: 80052627663     PISSN: None     EISSN: 1664302X     Source Type: Journal    
DOI: 10.3389/fmicb.2011.00097     Document Type: Article

References (82)

1. Andersson, J. O., and Andersson, S. G. (1999). Insights into the evolutionary process of genome degradation. Curr. Opin. Genet. Dev. 9, 664-671.
2. Andersson, S. G., Zomorodipour, A., Andersson, J. O., Sicheritz-Ponten, T., Alsmark, U. C., Podowski, R. M., Naslund, A. K., Eriksson, A. S., Winkler, H. H., and Kurland, C. G. (1998). The genome sequence of Rickettsia prowazekii and the origin of mitochondria. Nature 396, 133-140.
3. Atlas, R. M. (2003). Bioterrorism and biodefence research: changing the focus of microbiology. Nat. Rev. Microbiol. 1, 70-74.
4. Baldridge, G. D., Burkhardt, N., Herron, M. J., Kurtti, T. J., and Munderloh, U. G. (2005). Analysis of fluorescent protein expression in transformants of Rickettsia monacensis, an obligate intracellular tick symbiont. Appl. Environ. Microbiol. 71, 2095-2105.
5. Baldridge, G. D., Burkhardt, N. Y., Felsheim, R. F., Kurtti, T. J., and Munderloh, U. G. (2007a). Transposon insertion reveals pRM, a plasmid of Rickettsia monacensis. Appl. Environ. Microbiol. 73, 4984-4995.
6. Baldridge, G. D., Kurtti, T. J., Burkhardt, N., Baldridge, A. S., Nelson, C. M., Oliva, A. S., and Munderloh, U. G. (2007b). Infection of Ixodes scapularis ticks with Rickettsia monacensis expressing green fluorescent protein: a model system. J. Invertebr. Pathol. 94, 163-174.
7. Baldridge, G. D., Burkhardt, N. Y., Labruna, M. B., Pacheco, R. C., Paddock, C. D., Williamson, P. C., Billingsley, P. M., Felsheim, R. F., Kurtti, T. J., and Munderloh, U. G. (2010a). Wide dispersal and possible multiple origins of low-copy-number plasmids in Rickettsia species associated with blood-feeding arthropods. Appl. Environ. Microbiol. 76, 1718-1731.
8. Baldridge, G. D., Burkhardt, N. Y., Oliva, A. S., Kurtti, T. J., and Munderloh, U. G. (2010b). Rickettsial ompB promoter regulated expression of GFPuv in transformed Rickettsia montanensis. PLoS ONE 5, e8965. doi: 10.1371/ journal.pone.0008965
9. Barbet, A. F., Agnes, J. T., Moreland, A. L., Lundgren, A. M., Alleman, A. R., Noh, S. M., Brayton, K. A., Munderloh, U. G., and Palmer, G. H. (2005). Identification of functional promoters in the msp2 expression loci of Anaplasma marginale and Anaplasma phagocytophilum. Gene 353, 89-97.
10. Bardill, J. P., Miller, J. L., and Vogel, J. P. (2005). IcmS-dependent translocation of SdeA into macrophages by the Legionella pneumophila type IV secretion system. Mol. Microbiol. 56, 90-103.
11. Barysheva, O. V., Fujii, J., Takaesu, G., and Yoshida, S. (2008). Application of unstable Gfp variants to the kinetic study of Legionella pneumophila icm gene expression during infection. Microbiology 154, 1015-1025.
12. Bavoil, P. M., Hsia, R., and Ojcius, D. M. (2000). Closing in on Chlamydia and its intracellular bag of tricks. Microbiology 146, 2723-2731.
13. Beare, P. A., Howe, D., Cockrell, D. C., and Heinzen, R. A. (2007). Efficient method of cloning the obligate intracellular bacterium Coxiella burnetii. Appl. Environ. Microbiol. 73, 4048-4054.
14. Beare, P. A., Howe, D., Cockrell, D. C., Omsland, A., Hansen, B., and Heinzen, R. A. (2009). Characterization of a Coxiella burnetii ftsZ mutant generated by Himar1 transposon mutagenesis. J. Bacteriol. 191, 1369-1381.
15. Beare, P. A., Omsland, A., Cockrell, D. C., Howe, D., and Heinzen, R. A. (2010). Expansion of the Coxiella burnetii genetics tool box using axenic culture. Abstr. 24th Meet. Am. Soc. Rickettsiol. Abstr. 94.
16. Binet, R., and Maurelli, A. T. (2009). Transformation and isolation of allelic exchange mutants of Chlamydia psittaci using recombinant DNA introduced by electroporation. Proc. Natl. Acad. Sci. U.S.A. 106, 292-297.
17. Caldwell, H. D., Wood, H., Crane, D., Bailey, R., Jones, R. B., Mabey, D., Maclean, I., Mohammed, Z., Peeling, R., Roshick, C., Schachter, J., Solomon, A. W., Stamm, W. E., Suchland, R. J., Taylor, L., West, S. K., Quinn, T. C., Belland, R. J., and McClarty, G. (2003). Polymorphisms in Chlamydia trachomatis tryptophan synthase genes differentiate between genital and ocular isolates. J. Clin. Invest. 111, 1757-1769.
18. Campbell, R. E. (2004). Realization of beta-lactamase as a versatile fluorogenic reporter. Trends Biotechnol. 22, 208-211.
19. Chen, C., Banga, S., Mertens, K., Weber, M. M., Gorbaslieva, I., Tan, Y., Luo, Z. Q., and Samuel, J. E. (2010). Large-scale identification and translocation of type IV secretion substrates by Coxiella burnetii. Proc. Natl. Acad. Sci. U.S.A. 107, 21755-21760.
20. Choi, K. H., Gaynor, J. B., White, K. G., Lopez, C., Bosio, C. M., Karkhoff-Schweizer, R. R., and Schweizer, H. P. (2005). A Tn7-based broad-range bacterial cloning and expression system. Nat. Methods 2, 443-448.
21. Clark, T. R., Ellison, D. W., Kleba, B., and Hackstadt, T. (2011). Complementation of Rickettsia rickettsii RelA/SpoT restores a non-lytic plaque phenotype. Infect. Immun. 79, 1631-1637.
22. Coleman, S. A., Fischer, E. R., Howe, D., Mead, D. J., and Heinzen, R. A. (2004). Temporal analysis of Coxiella burnetii morphological differentiation. J. Bacteriol. 186, 7344-7352.
23. de Felipe, K. S., Glover, R. T., Charpentier, X., Anderson, O. R., Reyes, M., Pericone, C. D., and Shuman, H. A. (2008). Legionella eukaryotic-like type IV substrates interfere with organelle trafficking. PLoS Pathog. 4, e1000117. doi: 10.1371/journal. ppat.1000117
24. DeMars, R., and Weinfurter, J. (2008). Interstrain gene transfer in Chlamydia trachomatis in vitro: mechanism and significance. J. Bacteriol. 190, 1605-1614.
25. DeMars, R., Weinfurter, J., Guex, E., Lin, J., and Potucek, Y. (2007). Lateral gene transfer in vitro in the intracellular pathogen Chlamydia trachomatis. J. Bacteriol. 189, 991-1003.
26. Driskell, L. O., Yu, X. J., Zhang, L., Liu, Y., Popov, V. L., Walker, D. H., Tucker, A. M., and Wood, D. O. (2009). Directed mutagenesis of the Rickettsia prowazekii pld gene encoding phospholipase D. Infect. Immun. 77, 3244-3248.
27. Falkow, S. (2004). Molecular Koch's postulates applied to bacterial pathogenicity - a personal recollection 15 years later. Nat. Rev. Microbiol. 2, 67-72.
28. Felsheim, R. F., Chavez, A. S., Palmer, G. H., Crosby, L., Barbet, A. F., Kurtti, T. J., and Munderloh, U. G. (2010). Transformation of Anaplasma marginale. Vet. Parasitol. 167, 161-174.
29. Felsheim, R. F., Herron, M. J., Nelson, C. M., Burkhardt, N. Y., Barbet, A. F., Kurtti, T. J., and Munderloh, U. G. (2006). Transformation of Anaplasma phagocytophilum. BMC Biotechnol. 6, 42. doi: 10.1186/1472-6750-6-42
30. Gawronski, J. D., Wong, S. M., Giannoukos, G., Ward, D. V., and Akerley, B. J. (2009). Tracking insertion mutants within libraries by deep sequencing and a genome-wide screen for Haemophilus genes required in the lung. Proc. Natl. Acad. Sci. U.S.A. 106, 16422-16427.
31. Gomes, J. P., Bruno, W. J., Nunes, A., Santos, N., Florindo, C., Borrego, M. J., and Dean, D. (2007). Evolution of Chlamydia trachomatis diversity occurs by widespread interstrain recombination involving hotspots. Genome Res. 17, 50-60.
32. Hackstadt, T. (1996). The biology of Rickettsiae. Infect. Agents Dis. 5, 127-143.
33. Haglund, C. M., Choe, J. E., Skau, C. T., Kovar, D. R., and Welch, M. D. (2010). Rickettsia Sca2 is a bacterial forminlike mediator of actin-based motility. Nat. Cell Biol. 12, 1057-1063.
34. Heinzen, R. A., Hayes, S. F., Peacock, M. G., and Hackstadt, T. (1993). Directional actin polymerization associated with spotted fever group Rickettsia infection of Vero cells. Infect. Immun. 61, 1926-1935.
35. Karberg, M., Guo, H., Zhong, J., Coon, R., Perutka, J., and Lambowitz, A. M. (2001). Group II introns as controllable gene targeting vectors for genetic manipulation of bacteria. Nat. Biotechnol. 19, 1162-1167.
36. Kari, L., Goheen, M. M., Randall, L. B., Taylor, L. D., Carlson, J. H., Whitmire, W. M., Virok, D., Rajaram, K., Endresz, V., McClarty, G., Nelson, D. E., and Caldwell, H. D. (2011). Generation of targeted Chlamydia trachomatis null mutants. Proc. Natl. Acad. Sci. U.S.A. (in press).
37. Kleba, B., Clark, T. R., Lutter, E. I., Ellison, D. W., and Hackstadt, T. (2010). Disruption of the Rickettsia rickettsii Sca2 autotransporter inhibits actinbased motility. Infect. Immun. 78, 2240-2247.
38. Lampe, D. J., Akerley, B. J., Rubin, E. J., Mekalanos, J. J., and Robertson, H. M. (1999). Hyperactive transposase mutants of the Himar1 mariner transposon. Proc. Natl. Acad. Sci. U.S.A. 96, 11428-11433.
39. Lampe, M. F., Suchland, R. J., and Stamm, W. E. (1993). Nucleotide sequence of the variable domains within the major outer membrane protein gene from serovariants of Chlamydia trachomatis. Infect. Immun. 61, 213-219.
40. Li, C. H., Cheng, Y. W., Liao, P. L., Yang, Y. T., and Kang, J. J. (2010). Chloramphenicol causes mitochondrial stress, decreases ATP biosynthesis, induces matrix metalloproteinase-13 expression, and solid-tumor cell invasion. Toxicol. Sci. 116, 140-150.
41. Liu, Z. M., Tucker, A. M., Driskell, L. O., and Wood, D. O. (2007). Marinerbased transposon mutagenesis of Rickettsia prowazekii. Appl. Environ. Microbiol. 73, 6644-6649.
42. Lukacova, M., Valkova, D., Quevedo Diaz, M., Perecko, D., and Barak, I. (1999). Green fluorescent protein as a detection marker for Coxiella burnetii transformation. FEMS Microbiol. Lett. 175, 255-260.
43. Matsumoto, A., Izutsu, H., Miyashita, N., and Ohuchi, M. (1998). Plaque formation by and plaque cloning of Chlamydia trachomatis biovar trachoma. J. Clin. Microbiol. 36, 3013-3019.
44. Maurin, M., Benoliel, A. M., Bongrand, P., and Raoult, D. (1992). Phagolysosomal alkalinization and the bactericidal effect of antibiotics: the Coxiella burnetii paradigm. J. Infect. Dis. 166, 1097-1102.
45. Maurin, M., and Raoult, D. (1999). Q fever. Clin. Microbiol. Rev. 12, 518-553.
46. McCallum, C. M., Comai, L., Greene, E. A., and Henikoff, S. (2000). Targeted screening for induced mutations. Nat. Biotechnol. 18, 455-457.
47. Millman, K. L., Tavare, S., and Dean, D. (2001). Recombination in the ompA gene but not the omcB gene of Chlamydia contributes to serovarspecific differences in tissue tropism, immune surveillance, and persistence of the organism. J. Bacteriol. 183, 5997-6008.
48. Molofsky, A. B., and Swanson, M. S. (2003). Legionella pneumophila CsrA is a pivotal repressor of transmission traits and activator of replication. Mol. Microbiol. 50, 445-461.
49. Noh, S. M., Ueti, M. W., Palmer, G. H., Munderloh, U. G., Felsheim, R. F., and Brayton, K. A. (2011). Stability and tick transmission phenotype of gfp-transformed Anaplasma marginale through a complete in vivo infection cycle. Appl. Environ. Microbiol. 77, 330-334.
50. Nunes, A., Nogueira, P. J., Borrego, M. J., and Gomes, J. P. (2010). Adaptive evolution of the Chlamydia trachomatis dominant antigen reveals distinct evolutionary scenarios for B- and T-cell epitopes: worldwide survey. PLoS ONE 5, e13171. doi: 10.1371/journal. pone.0013171
51. Ogata, H., Renesto, P., Audic, S., Robert, C., Blanc, G., Fournier, P. E., Parinello, H., Claverie, J. M., and Raoult, D. (2005). The genome sequence of Rickettsia felis identifies the first putative conjugative plasmid in an obligate intracellular parasite. PLoS Biol. 3, e248. doi: 10.1371/journal. pbio.0030248
52. Omsland, A., Beare, P. A., Hill, J., Cockrell, D. C., Howe, D., Hansen, B., Samuel, J. E., and Heinzen, R. A. (2011). Isolation from animal tissue and genetic transformation of Coxiella burnetii facilitated by an improved axenic growth medium. Appl. Environ. Microbiol. (in press).
53. Omsland, A., Cockrell, D. C., Howe, D., Fischer, E. R., Virtaneva, K., Sturdevant, D. E., Porcella, S. F., and Heinzen, R. A. (2009). Host cell-free growth of the Q fever bacterium Coxiella burnetii. Proc. Natl. Acad. Sci. U.S.A. 106, 4430-4434.
54. Pallen, M. J., and Wren, B. W. (2007). Bacterial pathogenomics. Nature 449, 835-842.
55. Policastro, P. F., and Hackstadt, T. (1994). Differential activity of Rickettsia rickettsii ompA and ompB promoter regions in a heterologous reporter gene system. Microbiology 140, 2941-2949.
56. Qin, A., Tucker, A. M., Hines, A., and Wood, D. O. (2004). Transposon mutagenesis of the obligate intracellular pathogen Rickettsia prowazekii. Appl. Environ. Microbiol. 70, 2816-2822.
57. Rachek, L. I., Hines, A., Tucker, A. M., Winkler, H. H., and Wood, D. O. (2000). Transformation of Rickettsia prowazekii to erythromycin resistance encoded by the Escherichia coli ereB gene. J. Bacteriol. 182, 3289-3291.
58. Rachek, L. I., Tucker, A. M., Winkler, H. H., and Wood, D. O. (1998). Transformation of Rickettsia prowazekii to rifampin resistance. J. Bacteriol. 180, 2118-2124.
59. Raghavan, R., Hicks, L. D., and Minnick, M. F. (2008). Toxic introns and parasitic intein in Coxiella burnetii: legacies of a promiscuous past. J. Bacteriol. 190, 5934-5943.
60. Renesto, P., Gouin, E., and Raoult, D. (2002). Expression of green fluorescent protein in Rickettsia conorii. Microb. Pathog. 33, 17-21.
61. Reyrat, J. M., Pelicic, V., Gicquel, B., and Rappuoli, R. (1998). Counterselectable markers: untapped tools for bacterial genetics and pathogenesis. Infect. Immun. 66, 4011-4017.
62. Rodriguez, S. A., Yu, J. J., Davis, G., Arulanandam, B. P., and Klose, K. E. (2008). Targeted inactivation of Francisella tularensis genes by group II introns. Appl. Environ. Microbiol. 74, 2619-2626.
63. Roy, C. R., Berger, K. H., and Isberg, R. R. (1998). Legionella pneumophila DotA protein is required for early phagosome trafficking decisions that occur within minutes of bacterial uptake. Mol. Microbiol. 28, 663-674.
64. Seshadri, R., Paulsen, I. T., Eisen, J. A., Read, T. D., Nelson, K. E., Nelson, W. C., Ward, N. L., Tettelin, H., Davidsen, T. M., Beanan, M. J., Deboy, R. T., Daugherty, S. C., Brinkac, L. M., Madupu, R., Dodson, R. J., Khouri, H. M., Lee, K. H., Carty, H. A., Scanlan, D., Heinzen, R. A., Thompson, H. A., Samuel, J. E., Fraser, C. M., and Heidelberg, J. F. (2003). Complete genome sequence of the Q-fever pathogen Coxiella burnetii. Proc. Natl. Acad. Sci. U.S.A. 100, 5455-5460.
65. Sexton, J. A., Miller, J. L., Yoneda, A., Kehl-Fie, T. E., and Vogel, J. P. (2004). Legionella pneumophila DotU and IcmF are required for stability of the Dot/Icm complex. Infect. Immun. 72, 5983-5992.
66. Shannon, J. G., and Heinzen, R. A. (2007). Infection of human monocytederived macrophages with Coxiella burnetii. Methods Mol. Biol. 431, 189-200.
67. Sory, M. P., and Cornelis, G. R. (1994). Translocation of a hybrid YopEadenylate cyclase from Yersinia enterocolitica into HeLa cells. Mol. Microbiol. 14, 583-594.
68. Suchland, R. J., Eckert, L. O., Hawes, S. E., and Stamm, W. E. (2003). Longitudinal assessment of infecting serovars of Chlamydia trachomatis in Seattle public health clinics: 1988-1996. Sex. Transm. Dis. 30, 357-361.
69. Suchland, R. J., Sandoz, K. M., Jeffrey, B. M., Stamm, W. E., and Rockey, D. D. (2009). Horizontal transfer of tetracycline resistance among Chlamydia spp. in vitro. Antimicrob. Agents Chemother. 53, 4604-4611.
70. Suhan, M., Chen, S. Y., Thompson, H. A., Hoover, T. A., Hill, A., and Williams, J. C. (1994). Cloning and characterization of an autonomous replication sequence from Coxiella burnetii. J. Bacteriol. 176, 5233-5243.
71. Suhan, M. L., Chen, S. Y., and Thompson, H. A. (1996). Transformation of Coxiella burnetii to ampicillin resistance. J. Bacteriol. 178, 2701-2708.
72. Suhan, M. L., and Thompson, H. A. (2000). Expression of beta-lactamase in Coxiella burnetii transformants. FEMS Microbiol. Lett. 184, 303-306.
73. Tam, J. E., Davis, C. H., and Wyrick, P. B. (1994). Expression of recombinant DNA introduced into Chlamydia trachomatis by electroporation. Can. J. Microbiol. 40, 583-591.
74. Thomason, L. C., Costantino, N., Shaw, D. V., and Court, D. L. (2007). Multicopy plasmid modification with phage lambda Red recombineering. Plasmid 58, 148-158.
75. Troese, M. J., and Carlyon, J. A. (2009). Anaplasma phagocytophilum densecored organisms mediate cellular adherence through recognition of human P-selectin glycoprotein ligand 1. Infect. Immun. 77, 4018-4027.
76. Troyer, J. M., Radulovic, S., and Azad, A. F. (1999). Green fluorescent protein as a marker in Rickettsia typhi transformation. Infect. Immun. 67, 3308-3311.
77. Voth, D. E., Beare, P. A., Howe, D., Sharma, U. M., Samoilis, G., Cockrell, D. C., Omsland, A., and Heinzen, R. A. (2011). The Coxiella burnetii cryptic plasmid is enriched in genes encoding type IV secretion system substrates. J. Bacteriol. 193, 1493-1503.
78. Voth, D. E., Howe, D., Beare, P. A., Vogel, J. P., Unsworth, N., Samuel, J. E., and Heinzen, R. A. (2009). The Coxiella burnetii ankyrin repeat domain-containing protein family is heterogeneous, with C-terminal truncations that influence Dot/Icm-mediated secretion. J. Bacteriol. 191, 4232-4242.
79. Walker, D. H. (1989). Rocky Mountain spotted fever: a disease in need of microbiological concern. Clin. Microbiol. Rev. 2, 227-240.
80. Whitworth, T., Popov, V. L., Yu, X. J., Walker, D. H., and Bouyer, D. H. (2005). Expression of the Rickettsia prowazekii pld or tlyC gene in Salmonella enterica serovar Typhimurium mediates phagosomal escape. Infect. Immun. 73, 6668-6673.
81. Wike, D. A., Tallent, G., Peacock, M. G., and Ormsbee, R. A. (1972). Studies of the rickettsial plaque assay technique. Infect. Immun. 5, 715-722.
82. Wood, D. O., and Azad, A. F. (2000). Genetic manipulation of rickettsiae: a preview. Infect. Immun. 68, 6091-6093.