Comparative genomic characterization of Francisella tularensis strains belonging to low and high virulence subspecies

PLoS Pathogens

Volumn 5, Issue 5, 2009, Pages

  Champion, Mia D ^a   Zeng, Qiandong ^a   Nix, Eli B ^b   Nano, Francis E ^b   Keim, Paul ^c,d   Kodira, Chinnappa D ^a   Borowsky, Mark ^a   Young, Sarah ^a   Koehrsen, Michael ^a   Engels, Reinhard ^a   Pearson, Matthew ^a   Howarth, Clint ^a   Larson, Lisa ^a   White, Jared ^a   Alvarado, Lucia ^a   Forsman, Mats ^e   Bearden, Scott W ^f   Sjöstedt, Anders ^g   Titball, Richard ^h   Michell, Stephen L ^h   Birren, Bruce ^a   Galagan, James ^a,i   more..

^a BROAD INSTITUTE OF MIT AND HARVARD   (United States)

^b UNIVERSITY OF VICTORIA   (Canada)

^c NORTHERN ARIZONA UNIVERSITY   (United States)

^d TRANSLATIONAL GENOMICS RESEARCH INSTITUTE   (United States)

^e SWEDISH DEFENCE RESEARCH AGENCY   (Sweden)

^f NATIONAL CENTER FOR EMERGING AND ZOONOTIC INFECTIOUS DISEASES   (United States)

^g UMEÅ UNIVERSITY   (Sweden)

^h UNIVERSITY OF EXETER   (United Kingdom)

ⁱ BOSTON UNIVERSITY SCHOOL OF MEDICINE   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

REDUCED NICOTINAMIDE ADENINE DINUCLEOTIDE PHOSPHATE;

ARTICLE; BACTERIAL STRAIN; BACTERIAL SURVIVAL; BACTERIAL VIRULENCE; BACTERIUM ISOLATE; COMPARATIVE STUDY; FRANCISELLA TULARENSIS; GENE LOCUS; GENE LOSS; GENE SEQUENCE; GENOME ANALYSIS; NONHUMAN; NUCLEOTIDE SEQUENCE; OXIDATIVE STRESS; PATHOGENESIS; PHYLOGENY; PSEUDOGENE; BACTERIAL GENE; COMPARATIVE GENOMIC HYBRIDIZATION; GENETIC RECOMBINATION; GENETICS; ISOLATION AND PURIFICATION; PATHOGENICITY; VIRULENCE;

BACTERIA (MICROORGANISMS); FRANCISELLA; FRANCISELLA TULARENSIS; FRANCISELLA TULARENSIS SUBSP. HOLARCTICA; FRANCISELLA TULARENSIS SUBSP. MEDIASIATICA; FRANCISELLA TULARENSIS SUBSP. NOVICIDA; FRANCISELLA TULARENSIS SUBSP. TULARENSIS; NEGIBACTERIA;

BASE SEQUENCE; COMPARATIVE GENOMIC HYBRIDIZATION; FRANCISELLA TULARENSIS; GENES, BACTERIAL; PHYLOGENY; RECOMBINATION, GENETIC; VIRULENCE;

EID: 67249166181     PISSN: 15537366     EISSN: 15537374     Source Type: Journal    
DOI: 10.1371/journal.ppat.1000459     Document Type: Article

References (86)

1. CDC (2008) Tularemia http://www.cdc.gov/ncidod/diseases/submenus/sub- tularemia.htm.
2. Ellis J, Oyston PC, Green M, Titball RW (2002) Tularemia. Clin Microbiol Rev 15: 631-641.
3. Oyston PC, Sjostedt A, Titball RW (2004) Tularaemia: bioterrorism defence renews interest in Francisella tularensis. Nat Rev Microbiol 2: 967-978. (Pubitemid 39562535)
4. Svensson K, Larsson P, Johansson D, Byström M, Forsman M, et al. (2005) Evolution of Subspecies of Francisella tularensis. Journal of Bacteriology 187: 3903-3908. (Pubitemid 40705601)
5. Johansson A, Farlow J, Larsson P, Dukerich M, Chambers E, et al. (2004) Worldwide genetic relationships among Francisella tularensis isolates determined by multiple-locus variable-number tandem repeat analysis. J Bacteriol 186: 5808-5818. (Pubitemid 39128654)
6. Vogler AJ, Birdsell D, Price LB, Bowers JR, Beckstrom-Sternberg SM, et al. (2009) Phylogeography of Francisella tularensis: global expansion of a highly fit clone. J Bacteriol 191: 2474-2484.
7. Forsman M, Sandstrom G, Sjostedt A (1994) Analysis of 16S ribosomal DNA sequences of Francisella strains and utilization for determination of the phylogeny of the genus and for identification of strains by PCR. Int J Syst Bacteriol 44: 38-46. (Pubitemid 24023652)
8. Canback B, Tamas I, Andersson SG (2004) A phylogenomic study of endosymbiotic bacteria. Mol Biol Evol 6: 1110-1122. (Pubitemid 38658219)
9. Larsson P, Oyston PC, Chain P, Chu MC, Duffield M, et al. (2005) The complete genome sequence of Francisella tularensis, the causative agent of tularemia. Nat Genet 37: 153-159.
10. Beckstrom-Sternberg SM, Auerbach RK, Godbole S, Pearson JV, Beckstrom-Sternberg JS, et al. (2007) Complete Genomic Characterization of a Pathogenic A.II Strain of Francisella tularensis Subspecies tularensis. PLoS ONE 2: e947.
11. Farlow J, Wagner DM, Dukerich M, Stanley M, Chu M, et al. (2005) Francisella tularensis in the United States. Emerg Infect Dis 11: 1835-1841. (Pubitemid 43356077)
12. Keim P, Johansson A, Wagner DM (2007) Molecular epidemiology, evolution, and ecology of Francisella. Ann N Y Acad Sci 1105: 30-66. (Pubitemid 47507092)
13. Broekhuijsen M, Larsson P, Johansson A, Bystrom M, Eriksson U, et al. (2003) Genome-wide DNA microarray analysis of Francisella tularensis strains demonstrates extensive genetic conservation within the species but identifies regions that are unique to the highly virulent F. tularensis subsp. tularensis. J Clin Microbiol 41: 2924-2931. (Pubitemid 36842280)
14. Forsman M, Johansson A (2005) Tularemia. In Encyclopedia of Bioterrorism Defence. pp 483-488.
15. Rohmer L, Brittnacher M, Svensson K, Buckley D, Haugen E, et al. (2006) Potential source of Francisella tularensis live vaccine strain attenuation determined by genome comparison. Infect Immun 74: 6895-6906. (Pubitemid 44913165)
16. Nano FE, Zhang N, Cowley SC, Klose KE, Cheung KK, et al. (2004) A Francisella tularensis pathogenicity island required for intramacrophage growth. J Bacteriol 186: 6430-6436. (Pubitemid 39258124)
17. Rohmer L, Fong C, Abmayr S, Wasnick M, Larson Freeman TJ, et al. (2007) Comparison of Francisella tularensis genomes reveals evolutionary events associated with the emergence of human pathogenic strains. Genome Biol 8: R102. (Pubitemid 351903178)
18. Nano FE, Schmerk C (2007) The Francisella pathogenicity island. Ann N Y Acad Sci 1105: 122-137. (Pubitemid 47507082)
19. Maurelli AT (2007) Black holes, antivirulence genes, and gene inactivation in the evolution of bacterial pathogens. FEMS Microbiol Lett 267: 1-8. (Pubitemid 46066532)
20. Hacker J, Kaper JB (2000) Pathogenicity islands and the evolution of microbes. Annu Rev Microbiol 54: 641-679. (Pubitemid 30835922)
21. Li J, Ryder C, Mandal M, Ahmed F, Azadi P, et al. (2007) Attenuation and protective efficacy of an O-antigen-deficient mutant of Francisella tularensis LVS. Microbiology 153: 3141-3153. (Pubitemid 47517074)
22. Parkhill J, Sebaihia M, Preston A, Murphy LD, Thomson N, et al. (2003) Comparative analysis of the genome sequences of Bordetella pertussis, Bordetella parapertussis and Bordetella bronchiseptica. Nat Genet 35: 32-40.
23. Moore RA, Reckseidler-Zenteno S, Kim H, Nierman W, Yu Y, et al. (2004) Contribution of gene loss to the pathogenic evolution of Burkholderia pseudomallei and Burkholderia mallei. Infect Immun 72: 4172-4187. (Pubitemid 38821932)
24. Day WA, Jr Fernández RE, Maurelli AT (2001) Pathoadaptive mutations that enhance virulence: genetic organization of the cadA regions of Shigella spp. Infect Immun 69: 7471-7480. (Pubitemid 33086572)
25. Titball RW, Petrosino JF (2007) Francisella tularensis genomics and proteomics. Ann N Y Acad Sci 1105: 98-121. (Pubitemid 47507096)
26. Petrosino JF, Xiang Q, Karpathy SE, Jiang H, Yerrapragada S, et al. (2006) Chromosome rearrangement and diversification of Francisella tularensis revealed by the type B (OSU18) genome sequence. J Bacteriol 188: 6977-6985. (Pubitemid 44497910)
27. Tomaso H, Al Dahouk S, Hofer E, Splettstoesser WD, Treu TM, et al. (2005) Antimicrobial susceptibilities of Austrian Francisella tularensis holarctica biovar II strains. Int J Antimicrob Agents 26: 279-284. (Pubitemid 41338654)
28. Infectious Diseases Society of America IDSA (2008) Tularemia: Current, comprehensive information on pathogenesis, microbiology, epidemiology, diagnosis, treatment, and prophylaxis. http://www.cidrap.umn.edu/idsa/bt/ tularemia/biofacts/tularemiafactsheet.html.
29. Abd H, Johansson T, Golovliov I, Sandström G, Forsman M (2003) Survival and growth of Francisella tularensis in Acanthamoeba castellanii. Appl Environ Microbiol 69: 600-606. (Pubitemid 36077527)
30. Thelaus J, Andersson A, Mathisen P, Forslund AL, Noppa L, et al. (2009) Influence of nutrient status and grazing pressure on the fate of Francisella tularensis in lake water. FEMS Microbiol Ecol 67: 69-80.
31. Nübel U, Reissbrodt R, Weller A, Grunow R, Porsch- Ozcürümez M, et al. (2006) Population structure of Francisella tularensis. J Bacteriol 188: 5319-5324. (Pubitemid 44051502)
32. Gallagher LA, Ramage E, Jacobs MA, Kaul R, Brittnacher M, et al. (2007) A comprehensive transposon mutant library of Francisella novicida, a bioweapon surrogate. Proc Natl Acad Sci 104: 1009-1014. (Pubitemid 46154727)
33. Kraemer PS, Mitchell A, Pelletier MR, Gallagher LA, Wasnick M, et al. (2009) Genome-wide screen in Francisella novicida for genes required for pulmonary and systemic infection in mice. Infect Immun 77: 232-244.
34. Weiss DS, Brotcke A, Henry T, Margolis JJ, Chan K, et al. (2007) In vivo negative selection screen identifies genes required for Francisella virulence. Proc Natl Acad Sci U S A 104: 6037-6042.
35. Gallagher LA, McKevitt M, Ramage ER, Manoil C (2008) Genetic dissection of the Francisella novicida restriction barrier. J Bacteriol 190: 7830-7837.
36. Atkins HS, Dassa E, Walker NJ, Griffin KF, Harland DN, et al. (2006) The identification and evaluation of ATP binding cassette systems in the intracellular bacterium Francisella tularensis. Res Microbiol 157: 593-604. (Pubitemid 44067427)
37. Su J, Yang J, Zhao D, Kawula TH, Banas JA, et al. (2007) Genome-wide identification of Francisella tularensis virulence determinants. Infect Immun 75: 3089-3101. (Pubitemid 46870195)
38. Brett CL, Donowitz M, Rao R (2005) Evolutionary origins of eukaryotic sodium/proton exchangers. Am J Physiol Cell Physiol 288: C223-239. (Pubitemid 40105332)
39. Rubio MA, Pastar I, Gaston KW, Ragone FL, Janzen CJ, et al. (2007) An adenosine-to-inosine tRNA-editing enzyme that can perform C-to-U deamination of DNA. PNAS 104: 7821-7826. (Pubitemid 47185835)
40. Patel NJ, Zaborina O, Wu L, Wang Y, Wolfgeher DJ, et al. (2007) Recognition of intestinal epithelial HIF-1alpha activation by Pseudomonas aeruginosa. Am J Physiol Gastrointest Liver Physiol 292: G134-142. (Pubitemid 46090258)
41. Kukavica-Ibrulj I, Sanschagrin F, Peterson A, Whiteley M, Boyle B, et al. (2008) Functional genomics of PycR, a LysR family transcriptional regulator essential for maintenance of Pseudomonas aeruginosa in the rat lung. Microbiology 154: 2106-2118.
42. Waldron DE, Lindsay JA (2006) Sau1: a novel lineage-specific type I restriction-modification system that blocks horizontal gene transfer into Staphylococcus aureus and between S. aureus isolates of different lineages. J Bacteriol 188: 5578-5585. (Pubitemid 44157315)
43. Kostakioti M, Newman CL, Thanassi DG, Stathopoulos C (2005) Mechanisms of Protein Export across the Bacterial Outer Membrane. J Bacteriol 187: 4306-4314. (Pubitemid 40880940)
44. Winstanley C, Hart CA (2001) Type III secretion systems and pathogenicity islands. J Med Microbiol 50: 116-126. (Pubitemid 32113160)
45. Mecsas JJ, Strauss EJ (1996) Molecular mechanisms of bacterial virulence: type III secretion and pathogenicity islands. Emerg Infect Dis 2: 270-288.
46. Sugio A, Yang B, Zhu T, White FF (2007) Two type III effector genes of Xanthomonas oryzae pv. oryzae control the induction of the host genes OsTFIIAgamma1 and OsTFX1 during bacterial blight of rice. Proc Natl Acad Sci U S A 104: 10720-10725. (Pubitemid 47185731)
47. Gil H, Platz GJ, Forestal CA, Monfett M, Bakshi CS, et al. (2006) Deletion of TolC orthologs in Francisella tularensis identifies roles in multidrug resistance and virulence. Proc Natl Acad Sci 103: 12897-12902. (Pubitemid 44298658)
48. Tobe T, Beatson SA, Taniguchi H, Abe H, Bailey CM, et al. (2006) An extensive repertoire of type III secretion effectors in Escherichia coli O157 and the role of lambdoid phages in their dissemination. Proc Natl Acad Sci 103: 14941-14946. (Pubitemid 44527833)
49. Forsberg A, Guina T (2007) Type II secretion and type IV pili of Francisella. Ann N Y Acad Sci 1105: 187-201. (Pubitemid 47507097)
50. Urbanowski ML, Lykken GL, Yahr TL (2005) A secreted regulatory protein couples transcription to the secretory activity of the Pseudomonas aeruginosa type III secretion system. Proc Natl Acad Sci 102: 9930-9935. (Pubitemid 40993670)
51. Schröder G, Dehio C (2005) Virulence-associated type IV secretion systems of Bartonella. Trends Microbiol 13: 336-342. (Pubitemid 40884469)
52. Goodner B, Hinkle G, Gattung S, Miller N, Blanchard M, et al. (2001) Genome sequence of the plant pathogen and biotechnology agent Agrobacterium tumefaciens C58. Science 294: 2323-2328. (Pubitemid 33140550)
53. Wood DW, Setubal JC, Kaul R, Monks DE, Kitajima JP, et al. (2001) The Genome of the Natural Genetic Engineer Agrobacterium tumefaciens C58. Science 294: 2317-2323. (Pubitemid 33140549)
54. Koo JT, Choe J, Moseley SL (2004) HrpA, a DEAH-box RNA helicase, is involved in mRNA processing of a fimbrial operon in Escherichia coli. Mol Microbiol 52: 1813-1826. (Pubitemid 38822687)
55. Chakraborty S, Monfett M, Maier TM, Benach JL, Frank DW, et al. (2008) Type IV pili in Francisella tularensis: roles of pilF and pilT in fiber assembly, host cell adherence and virulence. Infect Immun: Epub.
56. Forsberg A, Guina T (2007) Type II secretion and type IV pili of Francisella. Ann N Y Acad Sci 1105: 187-201. (Pubitemid 47507097)
57. Rossier O, Cianciotto NP (2001) Type II protein secretion is a subset of the PilD-dependent processes that facilitate intracellular infection by Legionella pneumophila. Infect Immun 69: 2092-2098. (Pubitemid 32239673)
58. Twine S, Byström M, Chen W, Forsman M, Golovliov I, et al. (2005) A mutant of Francisella tularensis strain SCHU S4 lacking the ability to express a 58-kilodalton protein is attenuated for virulence and is an effective live vaccine. Infect Immun 73: 8345-8352. (Pubitemid 41740325)
59. Gil H, Benach JL, Thanassi DG (2004) Presence of pili on the surface of Francisella tularensis. Infect Immun 72: 3042-3047. (Pubitemid 38542436)
60. Zogaj X, Chakraborty S, Liu J, Thanassi DG, Klose KE (2008) Characterization of the Francisella tularensis subsp. novicida type IV pilus. Microbiology 154: 2139-2150.
61. Sasindran SJ, Saikolappan S, Dhandayuthapani S (2007) Methionine sulfoxide reductases and virulence of bacterial pathogens. Future Microbiol 2: 619-630.
62. Cameron ADS, Redfield R (2006) Non-canonical CRP sites control competence regulons in Escherichia coli and many other gamma-proteobacteria. Nucleic Acids Res 34: 6001-6014. (Pubitemid 44941178)
63. Ludu JS, de Bruin OM, Duplantis BN, Schmerk CL, Chou AY, et al. (2008) The Francisella pathogenicity island protein PdpD is required for full virulence and associates with homologues of the type VI secretion system. J Bacteriol 190: 4584-4595. (Pubitemid 351898975)
64. Lewinson O, Adler J, Sigal N, Bibi E (2006) Promiscuity in multidrug recognition and transport: the bacterial MFS Mdr transporters. Mol Microbiol 61: 277-284. (Pubitemid 44356562)
65. Roohparvar R, De Waard MA, Kema GH, Zwiers LH (2007) MgMfs1, a major facilitator superfamily transporter from the fungal wheat pathogen Mycosphaerella graminicola, is a strong protectant against natural toxic compounds and fungicides. Fungal Genet Biol 44: 378-388. (Pubitemid 46483138)
66. Kanehisa M, Araki M, Goto S, Hattori M, Hirakawa M, et al. (Dec 12 2007 Epub) KEGG for linking genomes to life and the environment. Nucleic Acids Res.
67. Ren Q, Chen K, Paulsen IT (2007) TransportDB: a comprehensive database resource for cytoplasmic membrane transport systems and outer membrane channels. Nucleic Acids Res. pp D274-279. (Pubitemid 46056214)
68. Lee EM, Ahn SH, Park JH, Lee JH, Ahn SC, et al. (2004) Identification of oligopeptide permease (opp) gene cluster in Vibrio fluvialis and characterization of biofilm production by oppA knockout mutation. FEMS Microbiol Lett 240: 21-30. (Pubitemid 39421786)
69. Parish T, Smith DA, Kendall S, Casali N, Bancroft GJ, et al. (2003) Deletion of Two-Component Regulatory Systems Increases the Virulence of Mycobacterium tuberculosis. Infection and Immunity 71: 1134-1140. (Pubitemid 36254293)
70. Flamez C, Ricard I, Arafah S, Simonet M, Marceau M (2007) Two-component system regulon plasticity in bacteria: a concept emerging from phenotypic analysis of Yersinia pseudotuberculosis response regulator mutants. Adv Exp Med Biol 603: 145-155.
71. Ng W, Ho-Ching, Tsui T, Winkler ME (2005) Regulation of the pspA Virulence Factor and Essential pcsB Murein Biosynthetic Genes by the Phosphorylated VicR (YycF) Response Regulator in Streptococcus pneumoniae. Journal of Bacteriology 187: 7444-7459. (Pubitemid 41507801)
72. Liu M, Hanks TS, Zhang J, McClure MJ, Siemsen DW, et al. (2006) Defects in ex vivo and in vivo growth and sensitivity to osmotic stress of group A Streptococcus caused by interruption of response regulator gene vicR. Microbiology 152: 967-978.
73. Ludu JS, Nix EB, Duplantis BN, de Bruin OM, Gallagher LA, et al. (2008) Genetic elements for selection, deletion mutagenesis and complementation in Francisella spp. FEMS Microbiol Lett 278: 86-93. (Pubitemid 350215885)
74. Bar-Haim E, Gat O, Markel G, Cohen H, Shafferman A, et al. (2008) Interrelationship between dendritic cell trafficking and Francisella tularensis dissemination following airway infection. PLoS Pathog 4: e1000211. doi:1000210.1001371/journal.ppat.1000211.
75. Hollis DG, Weaver RE, Steigerwalt AG, Wenger JD, Moss CW, et al. (1989) Francisella philomiragia comb. nov. (formerly Yersinia philomiragia) and Francisella tularensis biogroup novicida (formerly Francisella novicida) associated with human disease. J Clin Microbiol 27: 1601-1608. (Pubitemid 19170170)
76. Batzoglou S, Jaffe DB, Stanley K, Butler J, Gnerre S, et al. (2002) ARACHNE: a whole-genome shotgun assembler. Genome Res 12: 177-189. (Pubitemid 34070592)
77. Grant JR, Stothard P (2008) The CGView Server: a comparative genomics tool for circular genomes. Nucleic Acids Res 36: W181-W184.
78. Darling AC, Mau B, Blattner FR, Perna NT (2004) Mauve: multiple alignment of conserved genomic sequence with rearrangements. Genome Res 14: 1394-1403. (Pubitemid 39029237)
79. Li M, Ma B, Kisman D, Tromp J (2003) PatternHunter II: highly sensitive and fast homology search. Genome Inform 14: 164-175.
80. Tamura K, Dudley J, Nei M, Kumar S (2007) MEGA4: Molecular Evolutionary Genetics Analysis (MEGA) software version 4.0. . Molecular Biology and Evolution 24: 1596-1599. (Pubitemid 47236692)
81. Moriya Y, Itoh M, Okuda S, Yoshizawa A, Kanehisa M (2007) KAAS: an automatic genome annotation and pathway reconstruction server. Nucleic Acids Res 35: W182-W185.
82. Ren Q, Paulsen IT (2005) Comparative Analyses of Fundamental Differences in Membrane Transport Capabilities in Prokaryotes and Eukaryotes. PLoS Comput Biol 1: e27.
83. TransportDB (2008) http://www.membranetransport.org.
84. Kiil K, Ferchaud JB, David C, Binnewies TT, Wu H, et al. (2005) Genome update: distribution of two-component transduction systems in 250 bacterial genomes. Microbiology 151: 3447-3452. (Pubitemid 41632057)
85. Gertz EM, Yu YK, Agarwala R, Schäffer AA, Altschul SF (2006) Composition-based statistics and translated nucleotide searches: improving the TBLASTN module of BLAST. BMC Biol 4. (Pubitemid 46195777)
86. Microbial Genome Projects BCM-HGSC (2008) http://www.hgsc.bcm.tmc.edu/ projects/microbial/microbial-index.xsp.