Dermacentor andersoni transmission of Francisella tularensis subsp. novicida reflects bacterial colonization, dissemination, and replication coordinated with tick feeding

Kathryn E Reif; Guy H Palmer; Massaro W Ueti; Glen A Scoles; J J Margolis; D M Monack; Susan M Noh

doi:10.1128/IAI.05676-11

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Dermacentor andersoni transmission of Francisella tularensis subsp. novicida reflects bacterial colonization, dissemination, and replication coordinated with tick feeding

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Dermacentor andersoni transmission of Francisella tularensis subsp. novicida reflects bacterial colonization, dissemination, and replication coordinated with tick feeding

Kathryn E Reif, Guy H Palmer, Massaro W Ueti, Glen A Scoles, J J Margolis, D M Monack and Susan M Noh

Infection and immunity, Vol.79(12), pp.4941-4946

12/2011

DOI: https://doi.org/10.1128/IAI.05676-11

Handle:

https://hdl.handle.net/2376/109708

PMCID: PMC3232653

PMID: 21930762

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Abstract

Nymph - physiology

Rabbits

Mice, Inbred C57BL

Francisella tularensis - physiology

Male

Arachnid Vectors - microbiology

Feeding Behavior - physiology

Gene Expression Regulation, Bacterial - physiology

Chitinases - genetics

Dermacentor - physiology

Dermacentor - microbiology

Tularemia - microbiology

Animals

Tularemia - transmission

Francisella tularensis - growth & development

Nymph - microbiology

Arachnid Vectors - physiology

Female

Mice

Francisella tularensis - genetics

Mutation

Ticks serve as biological vectors for a wide variety of bacterial pathogens which must be able to efficiently colonize specific tick tissues prior to transmission. The bacterial determinants of tick colonization are largely unknown, a knowledge gap attributed in large part to the paucity of tools to genetically manipulate these pathogens. In this study, we demonstrated that Francisella tularensis subsp. novicida, for which a complete two-allele transposon mutant library has been constructed, initially infects the midguts of 100% of acquisition-fed Dermacentor andersoni nymphs, with stable colonization and replication during a subsequent molt. Increased dissemination to and marked replication within the salivary gland was closely linked to a second (transmission) feed and culminated in secretion of bacteria into the saliva and successful transmission. Simultaneous testing of multiple mutants resulted in total bacterial levels similar to those observed for single mutants. However, there was evidence of a bottleneck during colonization, resulting in a founder effect in which the most successful mutant varied when comparing individual ticks. Thus, it is essential to assess mutant success at the level of the tick population rather than in individual ticks. The ability of F. tularensis subsp. novicida to recapitulate the key physiological events by which bacteria colonize and are transmitted by ixodid ticks provides a new genome-wide approach to identify the required pathogen molecules and pathways. The identification of specific genes and, more importantly, conserved pathways that function at the tick-pathogen interface will accelerate the development of new methods to block transmission.

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Title: Dermacentor andersoni transmission of Francisella tularensis subsp. novicida reflects bacterial colonization, dissemination, and replication coordinated with tick feeding
Creators: Kathryn E Reif - Department of Veterinary Microbiology and Pathology, Washington State University, Pullman, WA 99164-7040, USA. kreif@vetmed.wsu.edu
Guy H Palmer
Massaro W Ueti
Glen A Scoles
J J Margolis
D M Monack
Susan M Noh
Publication Details: Infection and immunity, Vol.79(12), pp.4941-4946
Academic Unit: Paul G. Allen School for Global Animal Health
Publisher: United States
Grant note: T32 AI007025 / NIAID NIH HHS R01 AI044005 / NIAID NIH HHS AI065359 / NIAID NIH HHS R37 AI044005 / NIAID NIH HHS AI044005 / NIAID NIH HHS U54 AI065359 / NIAID NIH HHS T32AI007025 / NIAID NIH HHS AI093524 / NIAID NIH HHS R21 AI093524 / NIAID NIH HHS
Identifiers: 99900547161901842
Language: English
Resource Type: Journal article