Comparative review of Francisella tularensis and Francisella novicida

Abstract

Francisella tularensis is the causative agent of the acute disease tularemia. Due to its extreme infectivity and ability to cause disease upon inhalation, F. tularensis has been classified as a biothreat agent. Two subspecies of F. tularensis, tularensis and holarctica, are responsible for tularemia in humans. In comparison, the closely related species F. novicida very rarely causes human illness and cases that do occur are associated with patients who are immune compromised or have other underlying health problems. Virulence between F. tularensis and F. novicida also differs in laboratory animals. Despite this varying capacity to cause disease, the two species share ~97% nucleotide identity, with F. novicida commonly used as a laboratory surrogate for F. tularensis. As the F. novicida U112 strain is exempt from U.S. select agent regulations, research studies can be carried out in non-registered laboratories lacking specialized containment facilities required for work with virulent F. tularensis strains. This review is designed to highlight phenotypic (clinical, ecological, virulence, and pathogenic) and genomic differences between F. tularensis and F. novicida that warrant maintaining F. novicida and F. tularensis as separate species. Standardized nomenclature for F. novicida is critical for accurate interpretation of experimental results, limiting clinical confusion between F. novicida and F. tularensis and ensuring treatment efficacy studies utilize virulent F. tularensis strains.

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    Meibom K. L. Charbit A. (2010 ). Francisella tularensis metabolism and its relation to virulence. Front. Microbiol. 1:140

    Not in our library10.3389/fmicb.2010.00140

90. 90.

    Meric M. Willke A. Finke E. J. Grunow R. Sayan M. Erdogan S. (2008 ). Evaluation of clinical, laboratory, and therapeutic features of 145 tularemia cases: the role of quinolones in oropharyngeal tularemia. APMIS 116, 66–73

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91. 91.

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93. 93.

    Molins C. R. Delorey M. J. Yockey B. M. Young J. W. Sheldon S. W. Reese S. M. (2010 ). Virulence differences among Francisella tularensis subsp. tularensis clades in mice. PLoS ONE 5:e10205

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    Moran N. A. (2002 ). Microbial minimalism: genome reduction in bacterial pathogens. Cell 108, 583–586

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95. 95.

    Mortensen B. L. Fuller J. R. Taft-Benz S. Kijek T. M. Miller C. N. Huang M. T. (2010 ). Effects of the putative transcriptional regulator IclR on Francisella tularensis pathogenesis. Infect. Immun. 78, 5022–5032

    Not in our library10.1128/iai.00544-10

96. 96.

    Nano F. E. Schmerk C. (2007 ). The Francisella pathogenicity island. Ann. N.Y. Acad. Sci. 1105, 122–137

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97. 97.

    Nano F. E. Zhang N. Cowley S. C. Klose K. E. Cheung K. K. Roberts M. J. (2004 ). A Francisella tularensis pathogenicity island required for intramacrophage growth. J. Bacteriol. 186, 6430–6436

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98. 98.

    Nelson M. Lever M. S. Dean R. E. Pearce P. C. Stevens D. J. Simpson A. J. (2010 ). Bioavailability and efficacy of levofloxacin against Francisella tularensis in the common marmoset (Callithrix jacchus). Antimicrob. Agents Chemother. 54, 3922–3926

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99. 99.

    Okan N. A. Chalabaev S. Kim T. H. Fink A. Ross R. A. Kasper D. L. (2013 ). Kdo hydrolase is required for Francisella tularensis virulence and evasion of TLR2-mediated innate immunity. MBio 4, e00638–e00612

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100. 100.

     Okan N. A. Kasper D. L. (2013 ). The atypical lipopolysaccharide of Francisella. Carbohydr. Res. 378, 79–83

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     Ong C. Ooi C. H. Wang D. Chong H. Ng K. C. Rodrigues F. (2004 ). Patterns of large-scale genomic variation in virulent and avirulent Burkholderia species. Genome Res. 14, 2295–2307

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103. 103.

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104. 104.

     Pammit M. A. Budhavarapu V. N. Raulie E. K. Klose K. E. Teale J. M. Arulanandam B. P. (2004 ). Intranasal interleukin-12 treatment promotes antimicrobial clearance and survival in pulmonary Francisella tularensis subsp. novicida infection. Antimicrob. Agents Chemother. 48, 4513–4519

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105. 105.

     Pechous R. D. McCarthy T. R. Mohapatra N. P. Soni S. Penoske R. M. Salzman N. H. (2008 ). A Francisella tularensis Schu S4 purine auxotroph is highly attenuated in mice but offers limited protection against homologous intranasal challenge. PLoS ONE 3:e2487

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106. 106.

     Petersen J. M. Carlson J. Yockey B. Pillai S. Kuske C. Garbalena G. (2009a ). Direct isolation of Francisella spp. from environmental samples. Lett. Appl. Microbiol. 48, 663–667

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107. 107.

     Petersen J. M. Mead P. S. Schriefer M. E. (2009b ). Francisella tularensis: an arthropod-borne pathogen. Vet. Res. 40, 7

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108. 108.

     Petersen J. M. Molins C. R. (2010 ). Subpopulations of Francisella tularensis ssp. tularensis and holarctica: identification and associated epidemiology. Future Microbiol. 5, 649–661

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109. 109.

     Qin A. Scott D. W. Mann B. J. (2008 ). Francisella tularensis subsp. tularensis Schu S4 disulfide bond formation protein B, but not an RND-type efflux pump, is required for virulence. Infect. Immun. 76, 3086–3092

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110. 110.
     The Fischer 344 rat reflects human susceptibility to francisella pulmonary challenge and provides a new platform for virulence and protection studies. · 2010

     Not checked
111. 111.

     Respicio-Kingry L. B. Yockey M. Yendell B. Ratard S. Hand R. Balsamo J. (2012 ). Laboratory analysis of a Francisella novicida outbreak among prisoners at a Louisiana correctional facility, 2011, in 7th International Conference on Tularemia (Breckenridge, CO).

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     Richard K. Mann B. J. Stocker L. Barry E. M. Qin A. Cole L. E. (2014 ). Novel catanionic surfactant vesicle vaccines protect against Francisella tularensis LVS and confer significant partial protection against F. tularensis Schu S4 strain. Clin. Vaccine Immunol. 21, 212–226

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113. 113.
     Comparison of Francisella tularensis genomes reveals evolutionary events associated with the emergence of human pathogenic strains · 2007

     No notice
114. 114.

     Sampson T. R. Saroj S. D. Llewellyn A. C. Tzeng Y. L. Weiss D. S. (2013 ). A CRISPR/Cas system mediates bacterial innate immune evasion and virulence. Nature 497, 254–257

     Not in our library10.1038/nature12048

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     Sampson T. R. Weiss D. S. (2013a ). Alternative roles for CRISPR/Cas systems in bacterial pathogenesis. PLoS Pathog. 9:e1003621

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     Schmerk C. L. Duplantis B. N. Howard P. L. Nano F. E. (2009 ). A Francisella novicida pdpA mutant exhibits limited intracellular replication and remains associated with the lysosomal marker LAMP-1. Microbiology 155, 1498–1504

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     Schunder E. Rydzewski K. Grunow R. Heuner K. (2013 ). First indication for a functional CRISPR/Cas system in Francisella tularensis. Int. J. Med. Microbiol. 303, 51–60

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     Scoles G. A. (2004 ). Phylogenetic analysis of the Francisella-like endosymbionts of Dermacentor ticks. J. Med. Entomol. 41, 277–286

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120. 120.

     Sharma J. Li Q. Mishra B. B. Pena C. Teale J. M. (2009 ). Lethal pulmonary infection with Francisella novicida is associated with severe sepsis. J. Leukoc. Biol. 86, 491–504

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121. 121.

     Sjödin A. Svensson K. Ohrman C. Ahlinder J. Lindgren P. Duodu S. (2012 ). Genome characterisation of the genus Francisella reveals insight into similar evolutionary paths in pathogens of mammals and fish. BMC Genomics 13:268

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122. 122.

     Skerman V. B. D. McGowan V. Sneath P. H. A. (eds.). (1980 ). Approved lists of bacterial names. Int. J. Syst. Bacteriol. 30, 225–420

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     Stackebrandt E. Frederiksen W. Garrity G. M. Grimont P. A. Kampfer P. Maiden M. C. (2002 ). Report of the ad hoc committee for the re-evaluation of the species definition in bacteriology. Int. J. Syst. Evol. Microbiol. 52, 1043–1047

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124. 124.

     Steward J. Piercy T. Lever M. S. Simpson A. J. Brooks T. J. (2006 ). Treatment of murine pneumonic Francisella tularensis infection with gatifloxacin, moxifloxacin or ciprofloxacin. Int. J. Antimicrob. Agents 27, 439–443

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125. 125.

     Sutera V. Levert M. Burmeister W. P. Schneider D. Maurin M. (2014 ). Evolution toward high-level fluoroquinolone resistance in Francisella species. J. Antimicrob. Chemother. 69, 101–110

     Not in our library10.1093/jac/dkt321

126. 126.

     Svensson K. Sjödin A. Bystrom M. Granberg M. Brittnacher M. J. Rohmer L. (2012 ). Genome sequence of Francisella tularensis subspecies holarctica strain FSC200, isolated from a child with tularemia. J. Bacteriol. 194, 6965–6966

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127. 127.

     Tärnvik A. Berglund L. (2003 ). Tularaemia. Eur. Respir. J. 21, 361–373

     Not in our library10.1183/09031936.03.00088903

128. 128.

     Telepnev M. Golovliov I. Grundström T. Tärnvik A. Sjöstedt A. (2003 ). Francisella tularensis inhibits Toll-like receptor-mediated activation of intracellular signalling and secretion of TNF-alpha and IL-1 from murine macrophages. Cell. Microbiol. 5, 41–51

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129. 129.

     Tempel R. Lai X. H. Crosa L. Kozlowicz B. Heffron F. (2006 ). Attenuated Francisella novicida transposon mutants protect mice against wild-type challenge. Infect. Immun. 74, 5095–5105

     Not in our library10.1128/iai.00598-06

130. 130.

     Thomas R. M. Titball R. W. Oyston P. C. Griffin K. Waters E. Hitchen P. G. (2007 ). The immunologically distinct O antigens from Francisella tularensis subspecies tularensis and Francisella novicida are both virulence determinants and protective antigens. Infect. Immun. 75, 371–378

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131. 131.

     Thomas R. M. Twine S. M. Fulton K. M. Tessier L. Kilmury S. L. Ding W. (2011 ). Glycosylation of DsbA in Francisella tularensis subsp. tularensis. J. Bacteriol. 193, 5498–5509

     Not in our library10.1128/jb.00438-11

132. 132.

     Tindall B. J. Kampfer P. Euzeby J. P. Oren A. (2006 ). Valid publication of names of prokaryotes according to the rules of nomenclature: past history and current practice. Int. J. Syst. Evol. Microbiol. 56, 2715–2720

     Not in our library10.1099/ijs.0.64780-0

133. 133.

     Tomaso H. Al Dahouk S. Hofer E. Splettstoesser W. D. Treu T. M. Dierich M. P. (2005 ). Antimicrobial susceptibilities of Austrian Francisella tularensis holarctica biovar II strains. Int. J. Antimicrob. Agents 26, 279–284

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     Urich S. K. Petersen J. M. (2008 ). In vitro susceptibility of isolates of Francisella tularensis types A and B from North America. Antimicrob. Agents Chemother. 52, 2276–2278

     Not in our library10.1128/aac.01584-07

135. 135.

     Valade E. Vaissaire J. Merens A. Hernandez E. Gros C. Le Doujet C. (2008 ). Susceptibility of 71 French isolates of Francisella tularensis subsp. holarctica to eight antibiotics and accuracy of the Etest method. J. Antimicrob. Chemother. 62, 208–210

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136. 136.

     Vinogradov E. Conlan W. J. Gunn J. S. Perry M. B. (2004 ). Characterization of the lipopolysaccharide O-antigen of Francisella novicida (U112). Carbohydr. Res. 339, 649–654

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137. 137.

     Vinogradov E. Perry M. B. (2004 ). Characterisation of the core part of the lipopolysaccharide O-antigen of Francisella novicida (U112). Carbohydr. Res. 339, 1643–1648

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138. 138.

     Vinogradov E. Perry M. B. Conlan J. W. (2002 ). Structural analysis of Francisella tularensis lipopolysaccharide. Eur. J. Biochem. 269, 6112–6118

     Not in our library10.1046/j.1432-1033.2002.03321.x

139. 139.

     Weber I. B. Turabelidze G. Patrick S. Griffith K. S. Kugeler K. J. Mead P. S. (2012 ). Clinical recognition and management of tularemia in Missouri: a retrospective records review of 121 cases. Clin. Infect. Dis. 55, 1283–1290

     Not in our library10.1093/cid/cis706

140. 140.

     Weiss D. S. Brotcke A. Henry T. Margolis J. J. Chan K. Monack D. M. (2007a ). In vivo negative selection screen identifies genes required for Francisella virulence. Proc. Natl. Acad. Sci. U.S.A. 104, 6037–6042

     Not in our library10.1073/pnas.0609675104

141. 141.

     Weiss D. S. Henry T. Monack D. M. (2007b ). Francisella tularensis: activation of the inflammasome. Ann. N.Y. Acad. Sci. 1105, 219–237

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142. 142.

     Whipp M. J. Davis J. M. Lum G. De Boer J. Zhou Y. Bearden S. W. (2003 ). Characterization of a novicida-like subspecies of Francisella tularensis isolated in Australia. J. Med. Microbiol. 52, 839–842

     Not in our library10.1099/jmm.0.05245-0

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     Whitehouse C. A. Kesterson K. E. Duncan D. D. Eshoo M. W. Wolcott M. (2012 ). Identification and characterization of Francisella species from natural warm springs in Utah, USA. Lett. Appl. Microbiol. 54, 313–324

     Not in our library10.1111/j.1472-765x.2012.03214.x

144. 144.

     WHO. (2007 ). WHO Guidelines on Tularaemia. Geneva: World Health Organization

     Not in our library

145. 145.

     Zarrella T. M. Singh A. Bitsaktsis C. Rahman T. Sahay B. Feustel P. J. (2011 ). Host-adaptation of Francisella tularensis alters the bacterium's surface-carbohydrates to hinder effectors of innate and adaptive immunity. PLoS ONE 6:e22335

     Not in our library10.1371/journal.pone.0022335

146. 146.

     Zimmer A. L. Thoden J. B. Holden H. M. (2013 ). Three-dimensional structure of a sugar N-formyltransferase from Francisella tularensis. Protein Sci. [Epub ahead of print].

     Not in our library10.1002/pro.2409

147. 147.

     Zogaj X. Wyatt G. C. Klose K. E. (2012 ). Cyclic di-GMP stimulates biofilm formation and inhibits virulence of Francisella novicida. Infect. Immun. 80, 4239–4247

     Not in our library10.1128/iai.00702-12

Cited by papers we hold 2

• Using affinity propagation clustering for identifying bacterial clades and subclades with whole-genome sequences of Francisella tularensis. · 2020
  Not checked
• An Immature Myeloid/Myeloid-Suppressor Cell Response Associated with Necrotizing Inflammation Mediates Lethal Pulmonary Tularemia. · 2016
  Not checked

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