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Link to original content: https://pubmed.ncbi.nlm.nih.gov/16428415
Serotype differences and lack of biofilm formation characterize Yersinia pseudotuberculosis infection of the Xenopsylla cheopis flea vector of Yersinia pestis - PubMed Skip to main page content
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. 2006 Feb;188(3):1113-9.
doi: 10.1128/JB.188.3.1113-1119.2006.

Serotype differences and lack of biofilm formation characterize Yersinia pseudotuberculosis infection of the Xenopsylla cheopis flea vector of Yersinia pestis

David L Erickson  1 , Clayton O Jarrett, Brendan W Wren, B Joseph Hinnebusch
Affiliations

Serotype differences and lack of biofilm formation characterize Yersinia pseudotuberculosis infection of the Xenopsylla cheopis flea vector of Yersinia pestis

David L Erickson et al. J Bacteriol. 2006 Feb.

Abstract

Yersinia pestis, the agent of plague, is usually transmitted by fleas. To produce a transmissible infection, Y. pestis colonizes the flea midgut and forms a biofilm in the proventricular valve, which blocks normal blood feeding. The enteropathogen Yersinia pseudotuberculosis, from which Y. pestis recently evolved, is not transmitted by fleas. However, both Y. pestis and Y. pseudotuberculosis form biofilms that adhere to the external mouthparts and block feeding of Caenorhabditis elegans nematodes, which has been proposed as a model of Y. pestis-flea interactions. We compared the ability of Y. pestis and Y. pseudotuberculosis to infect the rat flea Xenopsylla cheopis and to produce biofilms in the flea and in vitro. Five of 18 Y. pseudotuberculosis strains, encompassing seven serotypes, including all three serotype O3 strains tested, were unable to stably colonize the flea midgut. The other strains persisted in the flea midgut for 4 weeks but did not increase in numbers, and none of the 18 strains colonized the proventriculus or produced a biofilm in the flea. Y. pseudotuberculosis strains also varied greatly in their ability to produce biofilms in vitro, but there was no correlation between biofilm phenotype in vitro or on the surface of C. elegans and the ability to colonize or block fleas. Our results support a model in which a genetic change in the Y. pseudotuberculosis progenitor of Y. pestis extended its pre-existing ex vivo biofilm-forming ability to the flea gut environment, thus enabling proventricular blockage and efficient flea-borne transmission.

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Figures

FIG. 1.
FIG. 1.
The number of Y. pseudotuberculosis in infected fleas decreases over time. The change (n-fold) in CFU/flea (mean CFU/flea on day 28 divided by mean CFU/flea immediately after infection) was determined separately for Y. pseudotuberculosis strains K163, K174, and K177 (A) and IP32953, PB1, PB1 ΔddhD-wzz, PB1 ΔddhD-wzz(pHMS1.2), IP32951, K170, K175, K177, K186, and K199 (B) and for Y. pestis KIM6+ (C). The mean and standard error of the mean of the change (n-fold) in CFU are shown for each group; the mean CFU/flea for each time point was determined from samples of 20 fleas per strain except where noted in Table 1.
FIG. 2.
FIG. 2.
Effect of the Y. pestis ymt gene on the ability of serotype O3 Y. pseudotuberculosis strains to persist in the flea digestive tract. Percentages of fleas that remained infected during a 4-week period following a single infectious blood meal containing the YPIII (□), K171 (▵), YPIII(pCH16) (▪), or K171(pCH16) (▴) strain of serotype O3. The average and standard deviation of the results of three independent infection experiments for each strain are shown.
FIG. 3.
FIG. 3.
Y. pseudotuberculosis does not form a biofilm in the flea digestive tract. The digestive tracts of fleas infected with Y. pestis KIM6+(pGFP) (A) or Y. pseudotuberculosis PB1 (B) were dissected, and the bacteria were visualized with fluorescence microscopy, either directly (Y. pestis) or after indirect fluorescent antibody (Y. pseudotuberculosis). The bar corresponds to 100 μm.
FIG. 4.
FIG. 4.
Y. pseudotuberculosis biofilms in glass flow cells. Confocal scanning laser microscopy images of biofilms produced after 48 h at 21°C for Y. pseudotuberculosis serotype O3 strain YPIII (A), serotype O1b strain K163 (B), serotype O2c strain K170 (C), serotype O3 strain K171 (D), serotype O4a strain K174 (E), serotype O4b strain K175 (F), serotype O5a strain K177 (G), serotype O9 strain K186 (H), and strain K199 (serotype unknown) (I). The right side and top of each panel are reconstructed vertical cross sections of the biofilm. The bar corresponds to 100 μm.
FIG. 5.
FIG. 5.
The Pgm+ phenotype correlates with enhanced biofilm formation by Y. pseudotuberculosis in vitro. Confocal scanning laser microscopy images of 48-h, 21°C biofilms produced by the Hms− strain Y. pseudotuberculosis PB1 ΔddhD-wzz (A), the Hms+ strain PB1 ΔddhD-wzz(pHMS1.2) (B), and the Hms+ strain Y. pestis KIM6+ (C). The bar corresponds to 100 μm.
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