A Widefield Light Microscopy-Based Approach Provides Further Insights into the Colonization of the Flea Proventriculus by Yersinia pestis
- PMID: 36939324
- PMCID: PMC10132112
- DOI: 10.1128/aem.02091-22
A Widefield Light Microscopy-Based Approach Provides Further Insights into the Colonization of the Flea Proventriculus by Yersinia pestis
Abstract
Yersinia pestis (the agent of flea-borne plague) must obstruct the flea's proventriculus to maintain transmission to a mammalian host. To this end, Y. pestis must consolidate a mass that entrapped Y. pestis within the proventriculus very early after its ingestion. We developed a semiautomated fluorescent image analysis method and used it to monitor and compare colonization of the flea proventriculus by a fully competent flea-blocking Y. pestis strain, a partially competent strain, and a noncompetent strain. Our data suggested that flea blockage results primarily from the replication of Y. pestis trapped in the anterior half of the proventriculus. However, consolidation of the bacteria-entrapping mass and colonization of the entire proventricular lumen increased the likelihood of flea blockage. The data also showed that consolidation of the bacterial mass is not a prerequisite for colonization of the proventriculus but allowed Y. pestis to maintain itself in a large flea population for an extended period of time. Taken as the whole, the data suggest that a strategy targeting bacterial mass consolidation could significantly reduce the likelihood of Y. pestis being transmitted by fleas (due to gut blockage), but also the possibility of using fleas as a long-term reservoir. IMPORTANCE Yersinia pestis (the causative agent of plague) is one of the deadliest bacterial pathogens. It circulates primarily among rodent populations and their fleas. Better knowledge of the mechanisms leading to the flea-borne transmission of Y. pestis is likely to generate strategies for controlling or even eradicating this bacillus. It is known that Y. pestis obstructs the flea's foregut so that the insect starves, frantically bites its mammalian host, and regurgitates Y. pestis at the bite site. Here, we developed a semiautomated fluorescent image analysis method and used it to document and compare foregut colonization and disease progression in fleas infected with a fully competent flea-blocking Y. pestis strain, a partially competent strain, and a noncompetent strain. Overall, our data provided new insights into Y. pestis' obstruction of the proventriculus for transmission but also the ecology of plague.
Keywords: HmsHFRS; OmpR-envZ; Yersinia pestis; bacteria; flea; plague; vector-borne diseases.
Conflict of interest statement
The authors declare no conflict of interest.
Figures
![FIG 1](https://www.ncbi.nlm.nih.gov/pmc/articles/instance/10132112/bin/aem.02091-22-f001.gif)
![FIG 2](https://www.ncbi.nlm.nih.gov/pmc/articles/instance/10132112/bin/aem.02091-22-f002.gif)
![FIG 3](https://www.ncbi.nlm.nih.gov/pmc/articles/instance/10132112/bin/aem.02091-22-f003.gif)
Similar articles
-
Role of the Yersinia pestis phospholipase D (Ymt) in the initial aggregation step of biofilm formation in the flea.mBio. 2024 Jun 12;15(6):e0012424. doi: 10.1128/mbio.00124-24. Epub 2024 May 9. mBio. 2024. PMID: 38722159 Free PMC article.
-
Molecular and Genetic Mechanisms That Mediate Transmission of Yersinia pestis by Fleas.Biomolecules. 2021 Feb 3;11(2):210. doi: 10.3390/biom11020210. Biomolecules. 2021. PMID: 33546271 Free PMC article. Review.
-
Biovar-related differences apparent in the flea foregut colonization phenotype of distinct Yersinia pestis strains do not impact transmission efficiency.Parasit Vectors. 2020 Jul 1;13(1):335. doi: 10.1186/s13071-020-04207-x. Parasit Vectors. 2020. PMID: 32611387 Free PMC article.
-
A refined model of how Yersinia pestis produces a transmissible infection in its flea vector.PLoS Pathog. 2020 Apr 15;16(4):e1008440. doi: 10.1371/journal.ppat.1008440. eCollection 2020 Apr. PLoS Pathog. 2020. PMID: 32294143 Free PMC article.
-
Yersinia--flea interactions and the evolution of the arthropod-borne transmission route of plague.Curr Opin Microbiol. 2012 Jun;15(3):239-46. doi: 10.1016/j.mib.2012.02.003. Epub 2012 Mar 7. Curr Opin Microbiol. 2012. PMID: 22406208 Free PMC article. Review.
References
-
- Bertherat E. 2019. Plague around the world in 2019. Weekly Epidemiological Record = Relevé épidémiologique hebdomadaire 94:289–292. https://apps.who.int/iris/handle/10665/325482.
-
- Gauthier JC, Raybaud A. 1903. Recherches expérimentales sur le rôle des parasites du rat dans la transmission de la peste. Revue D’Hygiène XXV 1903:426–438.
-
- Hinnebusch BJ. 2005. The evolution of flea-borne transmission in Yersinia pestis. Curr Issues Mol Biol 7:197–212. - PubMed
Publication types
MeSH terms
LinkOut - more resources
Full Text Sources
Medical