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Yersinia pestis Survival and Replication in Potential Ameba Reservoir.

ABSTRACT: Plague ecology is characterized by sporadic epizootics, then periods of dormancy. Building evidence suggests environmentally ubiquitous amebae act as feral macrophages and hosts to many intracellular pathogens. We conducted environmental genetic surveys and laboratory co-culture infection experiments to assess whether plague bacteria were resistant to digestion by 5 environmental ameba species. First, we demonstrated that Yersinia pestis is resistant or transiently resistant to various ameba species. Second, we showed that Y. pestis survives and replicates intracellularly within Dictyostelium discoideum amebae for ˃48 hours postinfection, whereas control bacteria were destroyed in <1 hour. Finally, we found that Y. pestis resides within ameba structures synonymous with those found in infected human macrophages, for which Y. pestis is a competent pathogen. Evidence supporting amebae as potential plague reservoirs stresses the importance of recognizing pathogen-harboring amebae as threats to public health, agriculture, conservation, and biodefense.

SUBMITTER: Markman DW

PROVIDER: S-EPMC5782900 | biostudies-literature | 2018 Feb

REPOSITORIES: biostudies-literature

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Yersinia pestis Survival and Replication in Potential Ameba Reservoir.

Markman David W DW Antolin Michael F MF Bowen Richard A RA Wheat William H WH Woods Michael M Gonzalez-Juarrero Mercedes M Jackson Mary M

Emerging infectious diseases 20180201 2

Plague ecology is characterized by sporadic epizootics, then periods of dormancy. Building evidence suggests environmentally ubiquitous amebae act as feral macrophages and hosts to many intracellular pathogens. We conducted environmental genetic surveys and laboratory co-culture infection experiments to assess whether plague bacteria were resistant to digestion by 5 environmental ameba species. First, we demonstrated that Yersinia pestis is resistant or transiently resistant to various ameba spe ...[more]

PMID: 29350155

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Project description:BackgroundPlague is a bacterial zoonotic disease, caused by Yersinia pestis. Rodents are the natural hosts with fleas as the vehicle of disease transmission. Domestic and wild dogs and cats have also been identified as possible disease hosts. In Zambia, plague outbreaks have been reported in the Southern and Eastern regions in the last 20 years. Based on these observations, Y. pestis could possibly be endemically present in the area.MethodsTo substantiate such possibility, sera samples were collected from rodents, shrews, dogs and cats for detection of antibodies against Fraction 1 gene (Fra1) of Y. pestis while organs from rodents and shrews, and fleas from both dogs and rodents were collected to investigate plasminogen activator gene (pla gene) of Y. pestis using ELISA and PCR respectively.ResultsA total of 369 blood samples were collected from domestic carnivores, shrews and domestic and peri-domestic rodents while 199 organs were collected from the rodents and shrews. Blood samples were tested for antibodies against Fra1 antigen using ELISA and 3% (5/165) (95% CI 0.99-6.93%) dogs were positive while all cats were negative. Of 199 sera from rodents and shrews, 12.6% (95% CI 8.30-17.98%) were positive for antibodies against Fra1 using anti-rat IgG secondary antibody while using anti-mouse IgG secondary antibody, 17.6% (95% CI 12.57-23.60%) were positive. PCR was run on the organs and 2.5% (95% CI 0.82-5.77%) were positive for plasminogen activator gene of Y. pestis and the amplicons were sequenced and showed 99% identity with Y. pestis reference sequences. All 82 fleas collected from animals subjected to PCR, were negative for pla gene. The specific rat-flea and dog-flea indices were 0.19 and 0.27 respectively, which were lower than the level required to enhance chances of the disease outbreak.ConclusionsWe concluded that plague was still endemic in the area and the disease may infect human beings if contact is enhanced between reservoir hosts and flea vectors. The lower specific rodent-flea Indices and absence of Y. pestis in the potential vectors were considered to be partly responsible for the current absence of plague outbreaks despite its presence in the sylvatic cycle.

Project description:Plague is a flea-borne rodent-associated zoonotic disease caused by Yersinia pestis The disease is characterized by epizootics with high rodent mortalities, punctuated by interepizootic periods when the bacterium persists in an unknown reservoir. This study investigates the interaction between Y. pestis and the ubiquitous soil free-living amoeba (FLA) Acanthamoeba castellanii to assess if the bacterium can survive within soil amoebae and whether intracellular mechanisms are conserved between infection of mammalian macrophages and soil amoebae. The results demonstrate that during coculture with amoebae, representative Y. pestis strains of epidemic biovars Medievalis, Orientalis, and Antiqua are phagocytized and able to survive within amoebae for at least 5 days. Key Y. pestis determinants of the intracellular interaction of Y. pestis and phagocytic macrophages, PhoP and the type three secretion system (T3SS), were then tested for their roles in the Y. pestis-amoeba interaction. Consistent with a requirement for the PhoP transcriptional activator in the intracellular survival of Y. pestis in macrophages, a PhoP mutant is unable to survive when cocultured with amoebae. Additionally, induction of the T3SS blocks phagocytic uptake of Y. pestis by amoebae, similar to that which occurs during macrophage infection. Electron microscopy revealed that in A. castellanii, Y. pestis resides intact within spacious vacuoles which were characterized using lysosomal trackers as being separated from the lysosomal compartment. This evidence for prolonged survival and subversion of intracellular digestion of Y. pestis within FLA suggests that protozoa may serve as a protective soil reservoir for Y. pestisIMPORTANCEYersinia pestis is a reemerging flea-borne zoonotic disease. Sylvatic plague cycles are characterized by an epizootic period during which the disease spreads rapidly, causing high rodent mortality, and an interepizootic period when the bacterium quiescently persists in an unknown reservoir. An understanding of the ecology of Y. pestis in the context of its persistence in the environment and its reactivation to initiate a new epizootic cycle is key to implementing novel surveillance strategies to more effectively predict and prevent new disease outbreaks. Here, we demonstrate prolonged survival and subversion of intracellular digestion of Y. pestis within a soil free-living amoeba. This suggests the potential role for protozoa as a protective soil reservoir for Y. pestis, which may help explain the recrudescence of plague epizootics.

Project description:BACKGROUND: Whole genome sequencing allowed the development of a number of high resolution sequence based typing tools for Yersinia (Y.) pestis. The application of these methods on isolates from most known foci worldwide and in particular from China and the Former Soviet Union has dramatically improved our understanding of the population structure of this species. In the current view, Y. pestis including the non or moderate human pathogen Y. pestis subspecies microtus emerged from Yersinia pseudotuberculosis about 2,600 to 28,600 years ago in central Asia. The majority of central Asia natural foci have been investigated. However these investigations included only few strains from Mongolia. METHODOLOGY/PRINCIPAL FINDINGS: Clustered Regularly Interspaced Short Prokaryotic Repeats (CRISPR) analysis and Multiple-locus variable number of tandem repeats (VNTR) analysis (MLVA) with 25 loci was performed on 100 Y. pestis strains, isolated from 37 sampling areas in Mongolia. The resulting data were compared with previously published data from more than 500 plague strains, 130 of which had also been previously genotyped by single nucleotide polymorphism (SNP) analysis. The comparison revealed six main clusters including the three microtus biovars Ulegeica, Altaica, and Xilingolensis. The largest cluster comprises 78 isolates, with unique and new genotypes seen so far in Mongolia only. Typing of selected isolates by key SNPs was used to robustly assign the corresponding clusters to previously defined SNP branches. CONCLUSIONS/SIGNIFICANCE: We show that Mongolia hosts the most recent microtus clade (Ulegeica). Interestingly no representatives of the ancestral Y. pestis subspecies pestis nodes previously identified in North-western China were identified in this study. This observation suggests that the subsequent evolution steps within Y. pestis pestis did not occur in Mongolia. Rather, Mongolia was most likely re-colonized by more recent clades coming back from China contemporary of the black death pandemic, or more recently in the past 600 years.

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Yersinia pestis Survival and Replication in Potential Ameba Reservoir.

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Yersinia pestis Survival and Replication in Potential Ameba Reservoir.

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