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Restriction of Francisella novicida genetic diversity during infection of the vector midgut.

Reif KE, Palmer GH, Crowder DW, Ueti MW, Noh SM - PLoS Pathog. (2014)

Bottom Line: Here we show using Francisella novicida and a natural tick vector of Francisella spp. (Dermacentor andersoni), that the tick vector acted as a stronger ecological filter for pathogen diversity compared to the mammalian host.We incorporated our experimental results into a model to demonstrate how vector population dynamics, especially vector-to-host ratio, strongly affected pathogen genotypic diversity in a population over time.Understanding pathogen genotypic population dynamics will aid in identification of the variables that most strongly affect pathogen transmission and disease ecology.

View Article: PubMed Central - PubMed

Affiliation: Department of Veterinary Microbiology and Pathology, Washington State University, Pullman, Washington, and Paul G. Allen School for Global Animal Health, Washington State University, Pullman, Washington, United States of America; Animal Disease Research Unit, Agricultural Research Service, U.S. Department of Agriculture, Pullman, Washington, United States of America.

ABSTRACT
The genetic diversity of pathogens, and interactions between genotypes, can strongly influence pathogen phenotypes such as transmissibility and virulence. For vector-borne pathogens, both mammalian hosts and arthropod vectors may limit pathogen genotypic diversity (number of unique genotypes circulating in an area) by preventing infection or transmission of particular genotypes. Mammalian hosts often act as "ecological filters" for pathogen diversity, where novel variants are frequently eliminated because of stochastic events or fitness costs. However, whether vectors can serve a similar role in limiting pathogen diversity is less clear. Here we show using Francisella novicida and a natural tick vector of Francisella spp. (Dermacentor andersoni), that the tick vector acted as a stronger ecological filter for pathogen diversity compared to the mammalian host. When both mice and ticks were exposed to mixtures of F. novicida genotypes, significantly fewer genotypes co-colonized ticks compared to mice. In both ticks and mice, increased genotypic diversity negatively affected the recovery of available genotypes. Competition among genotypes contributed to the reduction of diversity during infection of the tick midgut, as genotypes not recovered from tick midguts during mixed genotype infections were recovered from tick midguts during individual genotype infection. Mediated by stochastic and selective forces, pathogen genotype diversity was markedly reduced in the tick. We incorporated our experimental results into a model to demonstrate how vector population dynamics, especially vector-to-host ratio, strongly affected pathogen genotypic diversity in a population over time. Understanding pathogen genotypic population dynamics will aid in identification of the variables that most strongly affect pathogen transmission and disease ecology.

No MeSH data available.


Related in: MedlinePlus

Genotype prevalence and bacterial levels during single-genotype infections.Six genotypes were investigated for their ability to colonize mice and ticks in the absence of other genotypes. A) Bacterial infection level in mouse blood. B) Bacterial infection level in tick midgut. C) Prevalence of genotype colonization in tick midguts. Error bars represent ±SEM.
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ppat-1004499-g002: Genotype prevalence and bacterial levels during single-genotype infections.Six genotypes were investigated for their ability to colonize mice and ticks in the absence of other genotypes. A) Bacterial infection level in mouse blood. B) Bacterial infection level in tick midgut. C) Prevalence of genotype colonization in tick midguts. Error bars represent ±SEM.

Mentions: The reduction in F. novicida genotypic diversity upon infection of ticks at both the population and individual level may reflect competition among genotypes. Alternatively, this reduction in diversity may be due to the inability of specific genotypes to infect the tick. To test these hypotheses, the only six genotypes (Genotype 1–6, Table S4) that were consistently recovered from mice but absent from ticks in pooled genotype experiments were further explored. First, we determined if each of these six genotypes, when inoculated individually into mice, were able to colonize feeding ticks. All six genotypes colonized both mice and ticks at infection levels (CFU/ml mouse blood or tick midgut) similar to wild-type with the exception of Genotype 3 that failed to colonize infect ticks (Figure 2A, B) (F5,40 = 0.88, P = 0.50). Moreover, with the exception of Genotypes 3, the other genotypes were recovered from a similar proportion of ticks as wild-type (P>0.30 for all comparisons) (Figure 2C).


Restriction of Francisella novicida genetic diversity during infection of the vector midgut.

Reif KE, Palmer GH, Crowder DW, Ueti MW, Noh SM - PLoS Pathog. (2014)

Genotype prevalence and bacterial levels during single-genotype infections.Six genotypes were investigated for their ability to colonize mice and ticks in the absence of other genotypes. A) Bacterial infection level in mouse blood. B) Bacterial infection level in tick midgut. C) Prevalence of genotype colonization in tick midguts. Error bars represent ±SEM.
© Copyright Policy
Related In: Results  -  Collection

Show All Figures
getmorefigures.php?uid=PMC4231110&req=5

ppat-1004499-g002: Genotype prevalence and bacterial levels during single-genotype infections.Six genotypes were investigated for their ability to colonize mice and ticks in the absence of other genotypes. A) Bacterial infection level in mouse blood. B) Bacterial infection level in tick midgut. C) Prevalence of genotype colonization in tick midguts. Error bars represent ±SEM.
Mentions: The reduction in F. novicida genotypic diversity upon infection of ticks at both the population and individual level may reflect competition among genotypes. Alternatively, this reduction in diversity may be due to the inability of specific genotypes to infect the tick. To test these hypotheses, the only six genotypes (Genotype 1–6, Table S4) that were consistently recovered from mice but absent from ticks in pooled genotype experiments were further explored. First, we determined if each of these six genotypes, when inoculated individually into mice, were able to colonize feeding ticks. All six genotypes colonized both mice and ticks at infection levels (CFU/ml mouse blood or tick midgut) similar to wild-type with the exception of Genotype 3 that failed to colonize infect ticks (Figure 2A, B) (F5,40 = 0.88, P = 0.50). Moreover, with the exception of Genotypes 3, the other genotypes were recovered from a similar proportion of ticks as wild-type (P>0.30 for all comparisons) (Figure 2C).

Bottom Line: Here we show using Francisella novicida and a natural tick vector of Francisella spp. (Dermacentor andersoni), that the tick vector acted as a stronger ecological filter for pathogen diversity compared to the mammalian host.We incorporated our experimental results into a model to demonstrate how vector population dynamics, especially vector-to-host ratio, strongly affected pathogen genotypic diversity in a population over time.Understanding pathogen genotypic population dynamics will aid in identification of the variables that most strongly affect pathogen transmission and disease ecology.

View Article: PubMed Central - PubMed

Affiliation: Department of Veterinary Microbiology and Pathology, Washington State University, Pullman, Washington, and Paul G. Allen School for Global Animal Health, Washington State University, Pullman, Washington, United States of America; Animal Disease Research Unit, Agricultural Research Service, U.S. Department of Agriculture, Pullman, Washington, United States of America.

ABSTRACT
The genetic diversity of pathogens, and interactions between genotypes, can strongly influence pathogen phenotypes such as transmissibility and virulence. For vector-borne pathogens, both mammalian hosts and arthropod vectors may limit pathogen genotypic diversity (number of unique genotypes circulating in an area) by preventing infection or transmission of particular genotypes. Mammalian hosts often act as "ecological filters" for pathogen diversity, where novel variants are frequently eliminated because of stochastic events or fitness costs. However, whether vectors can serve a similar role in limiting pathogen diversity is less clear. Here we show using Francisella novicida and a natural tick vector of Francisella spp. (Dermacentor andersoni), that the tick vector acted as a stronger ecological filter for pathogen diversity compared to the mammalian host. When both mice and ticks were exposed to mixtures of F. novicida genotypes, significantly fewer genotypes co-colonized ticks compared to mice. In both ticks and mice, increased genotypic diversity negatively affected the recovery of available genotypes. Competition among genotypes contributed to the reduction of diversity during infection of the tick midgut, as genotypes not recovered from tick midguts during mixed genotype infections were recovered from tick midguts during individual genotype infection. Mediated by stochastic and selective forces, pathogen genotype diversity was markedly reduced in the tick. We incorporated our experimental results into a model to demonstrate how vector population dynamics, especially vector-to-host ratio, strongly affected pathogen genotypic diversity in a population over time. Understanding pathogen genotypic population dynamics will aid in identification of the variables that most strongly affect pathogen transmission and disease ecology.

No MeSH data available.


Related in: MedlinePlus