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      Genome Stability of Lyme Disease Spirochetes: Comparative Genomics of Borrelia burgdorferi Plasmids

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          Abstract

          Lyme disease is the most common tick-borne human illness in North America. In order to understand the molecular pathogenesis, natural diversity, population structure and epizootic spread of the North American Lyme agent, Borrelia burgdorferi sensu stricto, a much better understanding of the natural diversity of its genome will be required. Towards this end we present a comparative analysis of the nucleotide sequences of the numerous plasmids of B. burgdorferi isolates B31, N40, JD1 and 297. These strains were chosen because they include the three most commonly studied laboratory strains, and because they represent different major genetic lineages and so are informative regarding the genetic diversity and evolution of this organism. A unique feature of Borrelia genomes is that they carry a large number of linear and circular plasmids, and this work shows that strains N40, JD1, 297 and B31 carry related but non-identical sets of 16, 20, 19 and 21 plasmids, respectively, that comprise 33–40% of their genomes. We deduce that there are at least 28 plasmid compatibility types among the four strains. The B. burgdorferi ∼900 Kbp linear chromosomes are evolutionarily exceptionally stable, except for a short ≤20 Kbp plasmid-like section at the right end. A few of the plasmids, including the linear lp54 and circular cp26, are also very stable. We show here that the other plasmids, especially the linear ones, are considerably more variable. Nearly all of the linear plasmids have undergone one or more substantial inter-plasmid rearrangements since their last common ancestor. In spite of these rearrangements and differences in plasmid contents, the overall gene complement of the different isolates has remained relatively constant.

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          Most cited references221

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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?

              A treponema-like spirochete was detected in and isolated from adult Ixodes dammini, the incriminated tick vector of Lyme disease. Causally related to the spirochetes may be long-lasting cutaneous lesions that appeared on New Zealand White rabbits 10 to 12 weeks after infected ticks fed on them. Samples of serum from patients with Lyme disease were shown by indirect immunofluorescence to contain antibodies to this agent. It is suggested that the newly discovered spirochete is involved in the etiology of Lyme disease.
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                Author and article information

                Contributors
                Role: Editor
                Journal
                PLoS One
                plos
                plosone
                PLoS ONE
                Public Library of Science (San Francisco, USA )
                1932-6203
                2012
                14 March 2012
                : 7
                : 3
                : e33280
                Affiliations
                [1 ]Department of Pathology, University of Utah School of Medicine, Salt Lake City, Utah, United States of America
                [2 ]Department of Medicine and Institute for Genome Sciences, University of Maryland School of Medicine, Baltimore, Maryland, United States of America
                [3 ]Department of Biological Sciences, Hunter College of the City University of New York, New York City, New York, United States of America
                [4 ]Department of Medicine, Health Science Center, Stony Brook University, Stony Brook, New York, United States of America
                [5 ]Department of Medicine, New Jersey Medical School, Newark, New Jersey, United States of America
                [6 ]J. Craig Venter Institute, Rockville, Maryland, United States of America
                [7 ]Biology Department, Brookhaven National Laboratory, Upton, New York, United States of America
                University of Kentucky College of Medicine, United States of America
                Author notes

                Conceived and designed the experiments: SRC WMH WGQ BJL JJD SES CMF. Performed the experiments: EFM EBG MV DR JKA LCV SF JFW GID HMK JES RAH SRC. Analyzed the data: SRC EBG MV LCV SF WGQ EFM. Contributed reagents/materials/analysis tools: SRC BJL WGQ EFM CMF. Wrote the paper: SRC.

                [¤a]

                Current address: Virginia, United States of America

                [¤b]

                Current address: Center for Genomic Sciences, United States Army Medical Research Institute of Infectious Diseases, Ft. Detrick, Maryland, United States of America

                [¤c]

                Current address: Bethesda, Maryland, United States of America

                Article
                PONE-D-11-25819
                10.1371/journal.pone.0033280
                3303823
                22432010
                23ed9249-7cd4-45fc-9c73-5f75c44e6637
                Casjens et al. This is an open-access article distributed under the terms of the Creative Commons Attribution License, which permits unrestricted use, distribution, and reproduction in any medium, provided the original author and source are credited.
                History
                : 16 December 2011
                : 6 February 2012
                Page count
                Pages: 24
                Categories
                Research Article
                Biology
                Evolutionary Biology
                Genetics
                Molecular Genetics
                Genomics
                Microbiology
                Bacteriology
                Medicine
                Infectious Diseases
                Bacterial Diseases

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                Uncategorized

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