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      Virulence of the Lyme disease spirochete before and after the tick bloodmeal: a quantitative assessment

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          Abstract

          Background

          Borrelia burgdorferi, the tick-transmitted agent of Lyme disease, adapts to different environments as it cycles between an arthropod vector and vertebrate host. Signals encountered during nymphal tick feeding prior to transmission activate a regulon that is controlled by the alternative sigma factors RpoN and RpoS, which are required for mammalian infection. The ingested bloodmeal also provides nutrients that stimulate spirochete replication. Although the influence of tick feeding on spirochete growth and gene expression is well documented, a quantitative assessment of spirochete virulence before and after tick feeding has not been made.

          Methods

          Homogenates were prepared from unfed and fed infected Ixodes scapularis nymphs that had acquired B. burgdorferi as larvae. Serially diluted tick homogenates were needle-inoculated into mice to determine the infectious dose of tick-derived spirochetes before and after the bloodmeal. Mouse infection was assessed by sero-reactivity with B. burgdorferi whole cell lysates on immunoblots and attempted isolation of spirochetes from mouse tissues. Viable spirochetes in tick-derived inocula were quantified by colony formation in solid media.

          Results

          We found that an inoculum containing as many as 10 4 B. burgdorferi from unfed ticks is largely non-infectious, while the calculated ID 50 for spirochetes from fed ticks is ~30 organisms. Engineered constitutive production of the essential virulence factor OspC by spirochetes within unfed ticks did not confer an infectious phenotype.

          Conclusion

          Conditional priming of B. burgdorferi during tick feeding induces changes in addition to OspC that are required for infection of the mammalian host.

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          Most cited references65

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          Genomic sequence of a Lyme disease spirochaete, Borrelia burgdorferi.

          The genome of the bacterium Borrelia burgdorferi B31, the aetiologic agent of Lyme disease, contains a linear chromosome of 910,725 base pairs and at least 17 linear and circular plasmids with a combined size of more than 533,000 base pairs. The chromosome contains 853 genes encoding a basic set of proteins for DNA replication, transcription, translation, solute transport and energy metabolism, but, like Mycoplasma genitalium, it contains no genes for cellular biosynthetic reactions. Because B. burgdorferi and M. genitalium are distantly related eubacteria, we suggest that their limited metabolic capacities reflect convergent evolution by gene loss from more metabolically competent progenitors. Of 430 genes on 11 plasmids, most have no known biological function; 39% of plasmid genes are paralogues that form 47 gene families. The biological significance of the multiple plasmid-encoded genes is not clear, although they may be involved in antigenic variation or immune evasion.
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            Of ticks, mice and men: understanding the dual-host lifestyle of Lyme disease spirochaetes.

            In little more than 30 years, Lyme disease, which is caused by the spirochaete Borrelia burgdorferi, has risen from relative obscurity to become a global public health problem and a prototype of an emerging infection. During this period, there has been an extraordinary accumulation of knowledge on the phylogenetic diversity, molecular biology, genetics and host interactions of B. burgdorferi. In this Review, we integrate this large body of information into a cohesive picture of the molecular and cellular events that transpire as Lyme disease spirochaetes transit between their arthropod and vertebrate hosts during the enzootic cycle.
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              Lyme disease-a tick-borne spirochetosis?

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                Author and article information

                Contributors
                ikasumba@medicine.umaryland.edu
                bestora@niaid.nih.gov
                ktilly@niaid.nih.gov
                prosa@niaid.nih.gov
                Journal
                Parasit Vectors
                Parasit Vectors
                Parasites & Vectors
                BioMed Central (London )
                1756-3305
                7 March 2016
                7 March 2016
                2016
                : 9
                : 129
                Affiliations
                [ ]Laboratory of Zoonotic Pathogens, Rocky Mountain Laboratories, National Institute of Allergy and Infectious Diseases, National Institutes of Health, Hamilton, MT 59840 USA
                [ ]Current address: Center for Vaccine Development, Department of Geographic Medicine, University of Maryland School of Medicine, Baltimore, MD 21201 USA
                Article
                1380
                10.1186/s13071-016-1380-1
                4780146
                26951688
                100e92a2-b3b8-47ac-9e8d-ce15eb9a8989
                © Kasumba et al. 2016

                Open AccessThe article is a work of the United States Government; Title 17 U.S.C 105 provides that copyright protection is not available for any work of the United States government in the United States. Additionally, this is an open access article distributed under the terms of the Creative Commons Public Domain Dedication waiver ( http://creativecommons.org/publicdomain/zero/1.0), which permits worldwide unrestricted use, distribution, and reproduction in any medium for any lawful purpose.

                History
                : 14 December 2015
                : 12 February 2016
                Funding
                Funded by: Division of Intramural Research, National Institute of Allergy and Infectious Diseases, National Institutes of Health (US)
                Categories
                Research
                Custom metadata
                © The Author(s) 2016

                Parasitology
                borrelia burgdorferi,ixodes ticks,conditional priming,lyme disease spirochete
                Parasitology
                borrelia burgdorferi, ixodes ticks, conditional priming, lyme disease spirochete

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