Biofilm formation is not required for early-phase transmission of Yersinia pestis.
Early-phase transmission (EPT) is a recently described model of plague transmission that explains the rapid spread of disease from flea to mammal host during an epizootic. Unlike the traditional blockage-dependent model of plague transmission, EPT can occur when a flea takes its first blood meal after initially becoming infected by feeding on a bacteraemic host. Blockage of the flea gut results from biofilm formation in the proventriculus, mediated by the gene products found in the haemin storage (hms) locus of the Yersinia pestis chromosome. Although biofilms are required for blockage-dependent transmission, the role of biofilms in EPT has yet to be determined. An artificial feeding system was used to feed Xenopsylla cheopis and Oropsylla montana rat blood spiked with the parental Y. pestis strain KIM5(pCD1)+, two different biofilm-deficient mutants (Delta hmsT, Delta hmsR), or a biofilm-overproducer mutant (Delta hmsP). Infected fleas were then allowed to feed on naïve Swiss Webster mice for 1-4 days after infection, and the mice were monitored for signs of infection. We also determined the bacterial loads of each flea that fed upon naïve mice. Biofilm-defective mutants transmitted from X. cheopis and O. montana as efficiently as the parent strain, whereas the EPT efficiency of fleas fed the biofilm-overproducing strain was significantly less than that of fleas fed either the parent or a biofilm-deficient strain. Fleas infected with a biofilm-deficient strain harboured lower bacterial loads 4 days post-infection than fleas infected with the parent strain. Thus, defects in biofilm formation did not prevent flea-borne transmission of Y. pestis in our EPT model, although biofilm overproduction inhibited efficient EPT. Our results also indicate, however, that biofilms may play a role in infection persistence in the flea.
Vetter
Sara M
SM
Bacterial Diseases Branch, Division of Vector Borne Diseases, National Center for Enteric and Zoonotic Infectious Diseases, Centers for Disease Control and Prevention, 3150 Rampart Rd, Fort Collins, CO 80521, USA.
Eisen
Rebecca J
RJ
Bacterial Diseases Branch, Division of Vector Borne Diseases, National Center for Enteric and Zoonotic Infectious Diseases, Centers for Disease Control and Prevention, 3150 Rampart Rd, Fort Collins, CO 80521, USA.
Schotthoefer
Anna M
AM
Bacterial Diseases Branch, Division of Vector Borne Diseases, National Center for Enteric and Zoonotic Infectious Diseases, Centers for Disease Control and Prevention, 3150 Rampart Rd, Fort Collins, CO 80521, USA.
Montenieri
John A
JA
Bacterial Diseases Branch, Division of Vector Borne Diseases, National Center for Enteric and Zoonotic Infectious Diseases, Centers for Disease Control and Prevention, 3150 Rampart Rd, Fort Collins, CO 80521, USA.
Holmes
Jennifer L
JL
Bacterial Diseases Branch, Division of Vector Borne Diseases, National Center for Enteric and Zoonotic Infectious Diseases, Centers for Disease Control and Prevention, 3150 Rampart Rd, Fort Collins, CO 80521, USA.
Bobrov
Alexander G
AG
Department of Microbiology, Immunology and Molecular Genetics, University of Kentucky, MS415 Medical Center, Lexington, KY 40536, USA.
Bearden
Scott W
SW
Bacterial Diseases Branch, Division of Vector Borne Diseases, National Center for Enteric and Zoonotic Infectious Diseases, Centers for Disease Control and Prevention, 3150 Rampart Rd, Fort Collins, CO 80521, USA.
Perry
Robert D
RD
Department of Microbiology, Immunology and Molecular Genetics, University of Kentucky, MS415 Medical Center, Lexington, KY 40536, USA.
Gage
Kenneth L
KL
Bacterial Diseases Branch, Division of Vector Borne Diseases, National Center for Enteric and Zoonotic Infectious Diseases, Centers for Disease Control and Prevention, 3150 Rampart Rd, Fort Collins, CO 80521, USA.
D000818:Animals; D001426:Bacterial Proteins / Q000235:genetics / Q000378:metabolism; D018441:Biofilms; D006801:Humans; D007303:Insect Vectors / Q000382:microbiology; D051379:Mice; D010930:Plague / Q000382:microbiology / Q000635:transmission*; D051381:Rats; D017207:Rats, Sprague-Dawley; D005423:Siphonaptera / Q000382:microbiology; D015010:Yersinia pestis / Q000235:genetics / Q000502:physiology*
D001426:Bacterial Proteins
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