1932

Abstract

Interest in arthropod-borne pathogens focuses primarily on how they cause disease in humans. How they produce a transmissible infection in their arthropod host is just as critical to their life cycle, however. adopts a unique life stage in the digestive tract of its flea vector, characterized by rapid formation of a bacterial biofilm that is enveloped in a complex extracellular polymeric substance. Localization and adherence of the biofilm to the flea foregut is essential for transmission. Here, we review the molecular and genetic mechanisms of these processes and present a comparative evaluation and updated model of two related transmission mechanisms.

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2017-09-08
2024-10-09
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Literature Cited

  1. Aoyagi KL, Brooks BD, Bearden SW, Montenieri JA, Gage KL, Fisher MA. 1.  2015. LPS modification promotes maintenance of Yersinia pestis in fleas. Microbiology 161:628–38 [Google Scholar]
  2. Bacot AW. 2.  1915. Further notes on the mechanism of the transmission of plague by fleas. J. Hyg. 14:774–76 [Google Scholar]
  3. Bacot AW, Martin CJ. 3.  1914. Observations on the mechanism of the transmission of plague by fleas. J. Hyg. 13:423–39 [Google Scholar]
  4. Bartra SS, Styer KL, O'Bryant DM, Nilles ML, Hinnebusch BJ. 4.  et al. 2008. Resistance of Yersinia pestis to complement-dependent killing is mediated by the Ail outer membrane protein. Infect. Immun. 76:612–22 [Google Scholar]
  5. Beard CB, Butler JF, Hall DW. 5.  1990. Prevalence and biology of endosymbionts of fleas (Siphonaptera: Pulicidae) from dogs and cats in Alachua County, Florida. J. Med. Entomol 27:1050–61 [Google Scholar]
  6. Bellows LE, Koestler BJ, Karaba SM, Waters CM, Lathem WW. 6.  2012. Hfq-dependent, co-ordinate control of cyclic diguanylate synthesis and catabolism in the plague pathogen Yersinia pestis. Mol. Microbiol. 86:661–74 [Google Scholar]
  7. Bland DM, Hinnebusch BJ. 7.  2016. Feeding behavior modulates biofilm-mediated transmission of Yersiniapestis by the cat flea, Ctenocephalides felis. PLOS Negl. Trop. Dis. 10:e0004413 [Google Scholar]
  8. Bobrov AG, Kirillina O, Forman S, Mack D, Perry RD. 8.  2008. Insights into Yersinia pestis biofilm development: topology and co-interaction of Hms inner membrane proteins involved in exopolysaccharide production. Environ. Microbiol. 10:1419–32 [Google Scholar]
  9. Bobrov AG, Kirillina O, Ryjenkov DA, Waters CM, Price PA. 9.  et al. 2011. Systematic analysis of cyclic di-GMP signalling enzymes and their role in biofilm formation and virulence in Yersinia pestis. Mol. Microbiol. 79:533–51 [Google Scholar]
  10. Bobrov AG, Kirillina O, Vadyvaloo V, Koestler BJ, Hinz AK. 10.  et al. 2015. The Yersinia pestis HmsCDE regulatory system is essential for blockage of the oriental rat flea (Xenopsylla cheopis), a classic plague vector. Environ. Microbiol 17:947–59 [Google Scholar]
  11. Boegler KA, Graham CB, Johnson TL, Montenieri JA, Eisen RJ. 11.  2016. Infection prevalence, bacterial loads, and transmission efficiency in Oropsylla montana (Siphonaptera: Ceratophyllidae) one day after exposure to varying concentrations of Yersinia pestis in blood. J. Med. Entomol 53:674–80 [Google Scholar]
  12. Buhnerkempe MG, Eisen RJ, Goodell B, Gage KL, Antolin MF, Webb CT. 12.  2011. Transmission shifts underlie variability in population responses to Yersinia pestis infection. PLOS ONE 6:e22498 [Google Scholar]
  13. Burroughs AL. 13.  1944. The flea Malaraeus telchinum a vector of P. pestis. Proc. Soc. Exp. Biol. Med. 55:10–11 [Google Scholar]
  14. Burroughs AL. 14.  1947. Sylvatic plague studies: the vector efficiency of nine species of fleas compared with Xenopsylla cheopis. J. Hyg. 45:371–96 [Google Scholar]
  15. Chouikha I, Hinnebusch BJ. 15.  2012. Yersinia–flea interactions and the evolution of the arthropod-borne transmission route of plague. Curr. Opin. Microbiol. 15:239–46 [Google Scholar]
  16. Cohen C, Toh E, Munro D, Dong QF, Hawlena H. 16.  2015. Similarities and seasonal variations in bacterial communities from the blood of rodents and from their flea vectors. ISME J 9:1662–76 [Google Scholar]
  17. Darby C, Ananth SL, Tan L, Hinnebusch BJ. 17.  2005. Identification of gmhA, a Yersinia pestis gene required for flea blockage, by using a Caenorhabditis elegans biofilm system. Infect. Immun 73:7236–42 [Google Scholar]
  18. Douglas AE. 18.  2011. Lessons from studying insect symbioses. Cell Host Microbe 10:359–67 [Google Scholar]
  19. Earl SC, Rogers MT, Keen J, Bland DM, Houppert AS. 19.  et al. 2015. Resistance to innate immunity contributes to colonization of the insect gut by Yersinia pestis. PLOS ONE 10:e0133318 [Google Scholar]
  20. Eisen RJ, Bearden SW, Wilder AP, Montenieri JA, Antolin MF, Gage KL. 20.  2006. Early-phase transmission of Yersinia pestis by unblocked fleas as a mechanism explaining rapidly spreading plague epizootics. PNAS 103:15380–85 [Google Scholar]
  21. Eisen RJ, Borchert JN, Holmes JL, Amatre G, Van Wyk K. 21.  et al. 2008. Early-phase transmission of Yersinia pestis by cat fleas (Ctenocephalides felis) and their potential role as vectors in a plague-endemic region of Uganda. Am. J. Trop. Med. Hyg 78:949–56 [Google Scholar]
  22. Eisen RJ, Eisen L, Gage KL. 22.  2009. Studies of vector competency and efficiency of North American fleas for Yersinia pestis: state of the field and future research needs. J. Med. Entomol 46:737–44 [Google Scholar]
  23. Eisen RJ, Holmes JL, Schotthoefer AM, Vetter SM, Montenieri JA, Gage KL. 23.  2008. Demonstration of early-phase transmission of Yersinia pestis by the mouse flea, Aetheca wagneri (Siphonaptera: Ceratophylidae), and implications for the role of deer mice as enzootic reservoirs. J. Med. Entomol 45:1160–64 [Google Scholar]
  24. Eisen RJ, Lowell JL, Montenieri JA, Bearden SW, Gage KL. 24.  2007. Temporal dynamics of early-phase transmission of Yersinia pestis by unblocked fleas: Secondary infectious feeds prolong efficient transmission by Oropsylla montana (Siphonaptera: Ceratophyllidae). J. Med. Entomol 44:672–77 [Google Scholar]
  25. Eisen RJ, Vetter SM, Holmes JL, Bearden SW, Montenieri JA, Gage KL. 25.  2008. Source of host blood affects prevalence of infection and bacterial loads of Yersinia pestis in fleas. J. Med. Entomol 45:933–38 [Google Scholar]
  26. Eisen RJ, Wilder AP, Bearden SW, Montenieri JA, Gage KL. 26.  2007. Early-phase transmission of Yersinia pestis by unblocked Xenopsylla cheopis (Siphonaptera: Pulicidae) is as efficient as transmission by blocked fleas. J. Med. Entomol 44:678–82 [Google Scholar]
  27. Engelthaler DM, Hinnebusch BJ, Rittner CM, Gage KL. 27.  2000. Quantitative competitive PCR as a technique for exploring flea-Yersina pestis dynamics. Am. J. Trop. Med. Hyg 62:552–60 [Google Scholar]
  28. Erickson DL, Anderson NE, Cromar LM, Jolley A. 28.  2009. Bacterial communities associated with flea vectors of plague. J. Med. Entomol 46:1532–36 [Google Scholar]
  29. Erickson DL, Jarrett CO, Callison JA, Fischer ER, Hinnebusch BJ. 29.  2008. Loss of a biofilm-inhibiting glycosyl hydrolase during the emergence of Yersinia pestis. J. Bacteriol. 190:8163–70 [Google Scholar]
  30. Erickson DL, Russell CW, Johnson KL, Hileman T, Stewart RM. 30.  2011. PhoP and OxyR transcriptional regulators contribute to Yersinia pestis virulence and survival within Galleria mellonella. Microb. Pathog 51:389–95 [Google Scholar]
  31. Eskey CR, Haas VH. 31.  1940. Plague in the Western Part of the United States Washington, DC: U.S. Public Health Serv [Google Scholar]
  32. Fang N, Qu S, Yang H, Fang H, Liu L. 32.  et al. 2014. HmsB enhances biofilm formation in Yersinia pestis. Front. Microbiol. 5:685 [Google Scholar]
  33. Fang N, Yang H, Fang H, Liu L, Zhang Y. 33.  et al. 2015. RcsAB is a major repressor of Yersinia biofilm development through directly acting on hmsCDE, hmsT, and hmsHFRS. Sci. Rep 5:9566 [Google Scholar]
  34. Felek S, Muszynski A, Carlson RW, Tsang TM, Hinnebusch BJ, Krukonis ES. 34.  2009. Phosphoglucomutase of Yersinia pestis is required for autoaggregation and polymyxin B resistance. Infect. Immun. 78:1163–75 [Google Scholar]
  35. Flemming HC, Wingender J. 35.  2010. The biofilm matrix. Nat. Rev. Microbiol. 8:623–33 [Google Scholar]
  36. Fong JNC, Yildiz FH. 36.  2015. Biofilm matrix proteins. Microbiol. Spectr. 3:MB–0004-2014 [Google Scholar]
  37. Graca-Souza AV, Maya-Monteiro C, Paiva-Silva GO, Braz GR, Paes MC. 37.  et al. 2006. Adaptations against heme toxicity in blood-feeding arthropods. Insect Biochem. Mol. Biol. 36:322–35 [Google Scholar]
  38. Hengge R. 38.  2009. Principles of c-di-GMP signalling in bacteria. Nat. Rev. Microbiol. 7:263–73 [Google Scholar]
  39. Heroven AK, Dersch P. 39.  2006. RovM, a novel LysR-type regulator of the virulence activator gene rovA, controls cell invasion, virulence and motility of Yersinia pseudotuberculosis. Mol. Microbiol. 62:1469–83 [Google Scholar]
  40. Hinnebusch BJ. 40.  2012. Biofilm-dependent and biofilm-independent mechanisms of transmission of Yersinia pestis by fleas. Adv. Exp. Med. Biol 954:237–43 [Google Scholar]
  41. Hinnebusch BJ, Bland DM, Bosio CF, Jarrett CO. 41.  2017. Comparative ability of Oropsylla montana and Xenopsylla cheopis fleas to transmit Yersinia pestis by two different mechanisms. PLOS Negl. Trop. Dis 11:e0005276 [Google Scholar]
  42. Hinnebusch BJ, Chouikha I, Sun YC. 42.  2016. Ecological opportunity, evolution, and the emergence of flea-borne plague. Infect. Immun. 84:1932–40 [Google Scholar]
  43. Hinnebusch BJ, Fischer ER, Schwan TG. 43.  1998. Evaluation of the role of the Yersinia pestis plasminogen activator and other plasmid-encoded factors in temperature-dependent blockage of the flea. J. Inf. Dis. 178:1406–15 [Google Scholar]
  44. Hinnebusch BJ, Jarrett CO, Callison JA, Gardner D, Buchanan SK, Plano GV. 44.  2011. Role of the Yersinia pestis Ail protein in preventing a protective polymorphonuclear leukocyte response during bubonic plague. Infect. Immun. 79:4984–89 [Google Scholar]
  45. Hinnebusch BJ, Perry RD, Schwan TG. 45.  1996. Role of the Yersinia pestis hemin storage (hms) locus in the transmission of plague by fleas. Science 273:367–70 [Google Scholar]
  46. Hinnebusch BJ, Rudolph AE, Cherepanov P, Dixon JE, Schwan TG, Forsberg Å. 46.  2002. Role of Yersinia murine toxin in survival of Yersinia pestis in the midgut of the flea vector. Science 296:733–35 [Google Scholar]
  47. Hinnebusch BJ, Sebbane F, Vadyvaloo V. 47.  2012. Transcriptional profiling of the Yersinia pestis life cycle. Yersinia: Systems Biology and Control E Carniel, BJ Hinnebusch 1–18 Norwich, UK: Horiz. Sci [Google Scholar]
  48. Hobley L, Harkins C, MacPhee CE, Stanley-Wall NR. 48.  2015. Giving structure to the biofilm matrix: an overview of individual strategies and emerging common themes. FEMS Microbiol. Rev. 39:649–69 [Google Scholar]
  49. Holdenried R. 49.  1952. Sylvatic plague studies: VIII. Notes on the alimentary and reproductive tracts of fleas, made during experimental studies of plague. J. Parasitol. 38:289–92 [Google Scholar]
  50. Holdenried R, Quan SF. 50.  1956. Susceptibility of New Mexico rodents to experimental plague. Public Health Rep 71:979–84 [Google Scholar]
  51. Jarrett CO, Deak E, Isherwood KE, Oyston PC, Fischer ER. 51.  et al. 2004. Transmission of Yersinia pestis from an infectious biofilm in the flea vector. J. Inf. Dis. 190:783–92 [Google Scholar]
  52. Johnson TL, Hinnebusch BJ, Boegler KA, Graham CB, MacMillan K. 52.  et al. 2014. Yersinia murine toxin is not required for early-phase transmission of Yersinia pestis by Oropsylla montana (Siphonaptera: Ceratophyllidae) or Xenopsylla cheopis (Siphonaptera: Pulicidae). Microbiology 160:2517–25 [Google Scholar]
  53. Jones RT, Bernhardt SA, Martin AP, Gage KL. 53.  2012. Interactions among symbionts of Oropsylla spp. (Siphonoptera: Ceratophyllidae). J. Med. Entomol 49:492–96 [Google Scholar]
  54. Jones RT, McCormick KF, Martin AP. 54.  2008. Bacterial communities of Bartonella-positive fleas: diversity and community assembly patterns. Appl. Environ. Microbiol. 74:1667–70 [Google Scholar]
  55. Jones RT, Sanchez LG, Fierer N. 55.  2013. A cross-taxon analysis of insect-associated bacterial diversity. PLOS ONE 8:e61218 [Google Scholar]
  56. Jones RT, Vetter SM, Montenieiri J, Holmes J, Bernhardt SA, Gage KL. 56.  2013. Yersinia pestis infection and laboratory conditions alter flea-associated bacterial communities. ISME J 7:224–28 [Google Scholar]
  57. Kartman L, Prince FM, Quan SF. 57.  1956. Studies on Pasteurella pestis in fleas. Comparative plague-vector efficiency of Xenopsylla vexabilis hawaiiensis and Xenopsylla cheopis. Bull. World Health Organ 14:681–704 [Google Scholar]
  58. Kartman L, Prince FM, Quan SF, Stark HE. 58.  1958. New knowledge on the ecology of sylvatic plague. Ann. N. Y. Acad. Sci. 70:668–711 [Google Scholar]
  59. Kirillina O, Fetherston JD, Bobrov AG, Abney J, Perry RD. 59.  2004. HmsP, a putative phosphodiesterase, and HmsT, a putative diguanylate cyclase, control Hms-dependent biofilm formation in Yersinia pestis. Mol. Microbiol. 54:75–88 [Google Scholar]
  60. Kolodziejek AM, Hovde CJ, Minnich SA. 60.  2012. Yersinia pestis Ail: multiple roles of a single protein. Front. Cell. Infect. Microbiol. 2: doi 10.3389 [Google Scholar]
  61. Kolodziejek AM, Sinclair DJ, Seo KS, Schnider DR, Deobald CF. 61.  et al. 2007. Phenotypic characterization of OmpX, an Ail homologue of Yersinia pestis KIM. Microbiology 153:2941–51 [Google Scholar]
  62. Krasnov BR. 62.  2008. Functional and Evolutionary Ecology of Fleas Cambridge, UK: Cambridge Univ. Press [Google Scholar]
  63. Lillard JW, Bearden SW, Fetherston JD, Perry RD. 63.  1999. The haemin storage (Hms+) phenotype of Yersinia pestis is not essential for the pathogenesis of bubonic plague in mammals. Microbiology 145:197–209 [Google Scholar]
  64. Liu L, Fang H, Yang H, Zhang Y, Han Y. 64.  et al. 2016. CRP is an activator of Yersinia pestis biofilm formation that operates via a mechanism Involving gmhA and waaAE-coaD. Front. Microbiol 7:295 [Google Scholar]
  65. Liu L, Fang H, Yang H, Zhang Y, Han Y. 65.  et al. 2016. Reciprocal regulation of Yersinia pestis biofilm formation and virulence by RovM and RovA. Open Biol 6:150198 [Google Scholar]
  66. Liu Z, Gao X, Wang H, Fang H, Yan Y. 66.  et al. 2016. Plasmid pPCP1-derived sRNA HmsA promotes biofilm formation of Yersinia pestis. BMC Microbiol. 16:176 [Google Scholar]
  67. Lorange EA, Race BL, Sebbane F, Hinnebusch BJ. 67.  2005. Poor vector competence of fleas and the evolution of hypervirulence in Yersinia pestis. J. Inf. Dis. 191:1907–12 [Google Scholar]
  68. Marchette NJ, Lundgren DL, Nicholes PS, Bushman JB, Vest D. 68.  1962. Studies on infectious diseases in wild animals in Utah: II. Susceptibility of wild mammals to experimental plague. Zoonoses Res 1:225–49 [Google Scholar]
  69. Otto M. 69.  2013. Staphylococcal infections: mechanisms of biofilm maturation and detachment as critical determinants of pathogenicity. Annu. Rev. Med. 64:175–88 [Google Scholar]
  70. Paskewitz SM. 70.  1997. Transmission factors for insect-vectored microorganisms. Trends Microbiol 5:171–73 [Google Scholar]
  71. Pennington JE, Wells MA. 71.  2005. The adult midgut: structure and function. Biology of Disease Vectors WC Marquardt 289–95 Amsterdam: Elsevier [Google Scholar]
  72. Perry RD, Fetherston JD. 72.  1997. Yersinia pestis—etiologic agent of plague. Clin. Microbiol. Rev. 10:35–66 [Google Scholar]
  73. Petrova OE, Sauer K. 73.  2012. Sticky situations: key components that control bacterial surface attachment. J. Bacteriol. 194:2413–25 [Google Scholar]
  74. 74. Plague Res. Commission. 1906. Experiments upon the transmission of plague by fleas. J. Hyg. 6:425–82 [Google Scholar]
  75. 75. Plague Res. Commission. 1907. Further observations on the transmission of plague by fleas, with special reference to the fate of the plague bacillus in the body of the rat flea (P. cheopis). J. Hyg. 7:395–420 [Google Scholar]
  76. 76. Plague Res. Commission. 1908. The mechanism by means of which the flea clears itself of plague bacilli. J. Hyg. 8:260–65 [Google Scholar]
  77. Podladchikova O, Antonenka U, Heesemann J, Rakin A. 77.  2011. Yersinia pestis autoagglutination factor is a component of the type six secretion system. Int. J. Med. Microbiol 301:562–69 [Google Scholar]
  78. Pollitzer R. 78.  1954. Plague Geneva: World Health Organ [Google Scholar]
  79. Pollitzer R, Meyer KF. 79.  1961. The ecology of plague. Studies in Disease Ecology JM May 433–501 New York: Hafner [Google Scholar]
  80. Quan SF, Burroughs AL, Holdenried R, Meyer KF. 80.  1953. Studies on the prevention of experimental plague epizootics instituted among mice by infected fleas Estratto Atti. Sesto Congr. Int. Microbiol., Sez. Lomb. Soc. Ital. Microbiol. Rome: [Google Scholar]
  81. Rebeil R, Jarrett CO, Driver JD, Ernst RK, Oyston PC, Hinnebusch BJ. 81.  2013. Induction of the Yersinia pestis PhoP-PhoQ regulatory system in the flea and its role in producing a transmissible infection. J. Bacteriol. 195:1920–30 [Google Scholar]
  82. Reinhardt CA. 82.  1976. Ultrastructural comparison of the midgut epithelia of fleas with different feeding behavior patterns (Xenopsylla cheopis, Echidnophaga gallinacea, Tungapenetrans, Siphonaptera Pulicidae). Acta Trop 33:105–32 [Google Scholar]
  83. Rempe KA, Hinz AK, Vadyvaloo V. 83.  2012. Hfq regulates biofilm gut blockage that facilitates flea-borne transmission of Yersinia pestis. J. Bacteriol. 194:2036–40 [Google Scholar]
  84. Ren GX, Fan S, Guo XP, Chen S, Sun YC. 84.  2016. Differential regulation of c-di-GMP metabolic enzymes by environmental signals modulates biofilm formation in Yersinia pestis. Front. Microbiol. 7:821 [Google Scholar]
  85. Ren GX, Yan HQ, Zhu H, Guo XP, Sun YC. 85.  2014. HmsC, a periplasmic protein, controls biofilm formation via repression of HmsD, a diguanylate cyclase in Yersinia pestis. Environ. Microbiol. 16:1202–16 [Google Scholar]
  86. Ribeiro JCM. 86.  1996. Common problems of arthropod vectors of disease. The Biology of Disease Vectors BJ Beaty, WC Marquardt 25–33 Niwot, CO: Univ. Press of Colo [Google Scholar]
  87. Schotthoefer AM, Bearden SW, Vetter SM, Holmes J, Montenieri JA. 87.  et al. 2011. Effects of temperature on early-phase transmission of Yersinapestis by the flea, Xenopsylla cheopis. J. Med. Entomol. 48:411–17 [Google Scholar]
  88. Sun Y-C, Guo XP, Hinnebusch BJ, Darby C. 88.  2012. The Yersinia pestis Rcs phosphorelay inhibits biofilm formation by repressing transcription of the diguanylate cyclase gene hmsT. J. Bacteriol 194:2020–26 [Google Scholar]
  89. Sun Y-C, Jarrett CO, Bosio CF, Hinnebusch BJ. 89.  2014. Retracing the evolutionary path that led to flea-borne transmission of Yersinia pestis. Cell Host Microbe 15:578–86 [Google Scholar]
  90. Sun Y-C, Koumoutsi A, Darby C. 90.  2009. The response regulator PhoP negatively regulates Yersinia pseudotuberculosis and Yersinia pestis biofilms. FEMS Microbiol. Lett 290:85–90 [Google Scholar]
  91. Sun Y-C, Koumoutsi A, Jarrett C, Lawrence K, Gherardini FC. 91.  et al. 2011. Differential control of Yersinia pestis biofilm formation in vitro and in the flea vector by two c-di-GMP diguanylate cyclases. PLOS ONE 6:e19267 [Google Scholar]
  92. Tam C, Demke O, Hermanas T, Mitchell A, Hendrickx AP, Schneewind O. 92.  2014. YfbA, a Yersinia pestis regulator required for colonization and biofilm formation in the gut of cat fleas. J. Bacteriol. 196:1165–73 [Google Scholar]
  93. Tan L, Darby C. 93.  2006. Yersinia pestis YrbH is a multifunctional protein required for both 3-deoxy-d-manno-oct-2-ulosonic acid biosynthesis and biofilm formation. Mol. Microbiol 61:861–70 [Google Scholar]
  94. Tolker-Nielsen T. 94.  2015. Biofilm development. Microbiol. Spectr. 3:MB–0001-2014 [Google Scholar]
  95. Vadyvaloo V, Hinz AK. 95.  2015. A LysR-type transcriptional regulator, RovM, senses nutritional cues suggesting that it is involved in metabolic adaptation of Yersinia pestis to the flea gut. PLOS ONE 10:e0137508 [Google Scholar]
  96. Vadyvaloo V, Jarrett C, Sturdevant DE, Sebbane F, Hinnebusch BJ. 96.  2010. Transit through the flea vector induces a pretransmission innate immunity resistance phenotype in Yersinia pestis. PLOS Pathog. 6:e10000783 [Google Scholar]
  97. Vaughan JA, Azad AF. 97.  1993. Patterns of erythrocyte digestion by bloodsucking insects: constraints on vector competence. J. Med. Entomol 30:214–16 [Google Scholar]
  98. Verjbitski DT. 98.  1908. The part played by insects in the epidemiology of plague. J. Hyg. 8:162–208 [Google Scholar]
  99. Vetter SM, Eisen RJ, Schotthoefer AM, Montenieri JA, Holmes JL. 99.  et al. 2010. Biofilm formation is not required for early-phase transmission of Yersinia pestis. Microbiology 156:2216–25 [Google Scholar]
  100. Webb CT, Brooks CP, Gage KL, Antolin MF. 100.  2006. Classic flea-borne transmission does not drive plague epizootics in prairie dogs. PNAS 103:6236–41 [Google Scholar]
  101. Wheeler CM, Douglas JR. 101.  1945. Sylvatic plague studies: V. The determination of vector efficiency. J. Infect. Dis. 77:1–12 [Google Scholar]
  102. Wilder AP, Eisen RJ, Bearden SW, Montenieri JA, Gage KL, Antolin MF. 102.  2008. Oropsylla hirsuta (Siphonaptera: Ceratophyllidae) can support plague epizootics in black-tailed prairie dogs (Cynomys ludovicianus) by early-phase transmission of Yersinia pestis. Vector Borne Zoonotic Dis 8:359–67 [Google Scholar]
  103. Wilder AP, Eisen RJ, Bearden SW, Montenieri JA, Tripp DW. 103.  et al. 2008. Transmission efficiency of two flea species (Oropsylla tuberculata cynomuris and Oropsylla hirsuta) involved in plague epizootics among prairie dogs. EcoHealth 5:205–12 [Google Scholar]
  104. Williams JE, Moussa MA, Cavanaugh DC. 104.  1979. Experimental plague in the California ground squirrel. J. Infect. Dis. 140:618–21 [Google Scholar]
  105. Willias SP, Chauhan S, Lo CC, Chain PS, Motin VL. 105.  2015. CRP-mediated carbon catabolite regulation of Yersinia pestis biofilm formation is enhanced by the carbon storage regulator protein, CsrA. PLOS ONE 10:e0135481 [Google Scholar]
  106. Zhang Y, Dai X, Wang Q, Chen H, Meng W. 106.  et al. 2015. Transmission efficiency of the plague pathogen (Y. pestis) by the flea, Xenopsylla skrjabini, to mice and great gerbils. Parasit. Vectors 8:256 [Google Scholar]
  107. Zhang Y, Dai X, Wang X, Maituohuti A, Cui Y. 107.  et al. 2012. Dynamics of Yersinia pestis and its antibody response in great gerbils (Rhombomys opimus) by subcutaneous infection. PLOS ONE 7:e46820 [Google Scholar]
  108. Zhou W, Russell CW, Johnson KL, Mortensen RD, Erickson DL. 108.  2012. Gene expression analysis of Xenopsylla cheopis (Siphonaptera: Pulicidae) suggests a role for reactive oxygen species in response to Yersinia pestis infection. J. Med. Entomol 49:364–70 [Google Scholar]
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