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      Phylogenetic diversity and historical patterns of pandemic spread of Yersinia pestis

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          Abstract

          Pandemic infectious diseases have accompanied humans since their origins 1, and have shaped the form of civilizations 2. Of these, plague is possibly historically the most dramatic. We reconstructed historical patterns of plague transmission through sequence variation in 17 complete genome sequences and 933 single nucleotide polymorphisms (SNPs) within a global collection of 286 Yersinia pestis isolates. Y. pestis evolved in or near China, and has been transmitted via multiple epidemics that followed various routes, probably including transmissions to West Asia via the Silk Road and to Africa by Chinese marine voyages. In 1894, Y. pestis spread to India and radiated to diverse parts of the globe, leading to country-specific lineages that can be traced by lineage-specific SNPs. All 626 current isolates from the U.S.A. reflect one radiation and 82 isolates from Madagascar represent a second. Subsequent local microevolution of Y. pestis is marked by sequential, geographically-specific SNPs.

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          Genome sequence of Yersinia pestis, the causative agent of plague.

          The Gram-negative bacterium Yersinia pestis is the causative agent of the systemic invasive infectious disease classically referred to as plague, and has been responsible for three human pandemics: the Justinian plague (sixth to eighth centuries), the Black Death (fourteenth to nineteenth centuries) and modern plague (nineteenth century to the present day). The recent identification of strains resistant to multiple drugs and the potential use of Y. pestis as an agent of biological warfare mean that plague still poses a threat to human health. Here we report the complete genome sequence of Y. pestis strain CO92, consisting of a 4.65-megabase (Mb) chromosome and three plasmids of 96.2 kilobases (kb), 70.3 kb and 9.6 kb. The genome is unusually rich in insertion sequences and displays anomalies in GC base-composition bias, indicating frequent intragenomic recombination. Many genes seem to have been acquired from other bacteria and viruses (including adhesins, secretion systems and insecticidal toxins). The genome contains around 150 pseudogenes, many of which are remnants of a redundant enteropathogenic lifestyle. The evidence of ongoing genome fluidity, expansion and decay suggests Y. pestis is a pathogen that has undergone large-scale genetic flux and provides a unique insight into the ways in which new and highly virulent pathogens evolve.
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            Evidence for lateral gene transfer between Archaea and bacteria from genome sequence of Thermotoga maritima.

            The 1,860,725-base-pair genome of Thermotoga maritima MSB8 contains 1,877 predicted coding regions, 1,014 (54%) of which have functional assignments and 863 (46%) of which are of unknown function. Genome analysis reveals numerous pathways involved in degradation of sugars and plant polysaccharides, and 108 genes that have orthologues only in the genomes of other thermophilic Eubacteria and Archaea. Of the Eubacteria sequenced to date, T. maritima has the highest percentage (24%) of genes that are most similar to archaeal genes. Eighty-one archaeal-like genes are clustered in 15 regions of the T. maritima genome that range in size from 4 to 20 kilobases. Conservation of gene order between T. maritima and Archaea in many of the clustered regions suggests that lateral gene transfer may have occurred between thermophilic Eubacteria and Archaea.
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              Insights into the evolution of Yersinia pestis through whole-genome comparison with Yersinia pseudotuberculosis.

              Yersinia pestis, the causative agent of plague, is a highly uniform clone that diverged recently from the enteric pathogen Yersinia pseudotuberculosis. Despite their close genetic relationship, they differ radically in their pathogenicity and transmission. Here, we report the complete genomic sequence of Y. pseudotuberculosis IP32953 and its use for detailed genome comparisons with available Y. pestis sequences. Analyses of identified differences across a panel of Yersinia isolates from around the world reveal 32 Y. pestis chromosomal genes that, together with the two Y. pestis-specific plasmids, to our knowledge, represent the only new genetic material in Y. pestis acquired since the the divergence from Y. pseudotuberculosis. In contrast, 149 other pseudogenes (doubling the previous estimate) and 317 genes absent from Y. pestis were detected, indicating that as many as 13% of Y. pseudotuberculosis genes no longer function in Y. pestis. Extensive insertion sequence-mediated genome rearrangements and reductive evolution through massive gene loss, resulting in elimination and modification of preexisting gene expression pathways, appear to be more important than acquisition of genes in the evolution of Y. pestis. These results provide a sobering example of how a highly virulent epidemic clone can suddenly emerge from a less virulent, closely related progenitor.
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                Author and article information

                Journal
                9216904
                2419
                Nat Genet
                Nat. Genet.
                Nature genetics
                1061-4036
                1546-1718
                18 October 2010
                31 October 2010
                December 2010
                01 June 2011
                : 42
                : 12
                : 1140-1143
                Affiliations
                [1 ] Max-Planck-Institut für Infektionsbiologie, Dept. of Molecular Biology, Charitéplatz 1, 10117 Berlin, Germany
                [2 ] State Key Laboratory of Pathogen and Biosecurity, Beijing Institute of Microbiology and Epidemiology, Beijing 100071, China
                [3 ] Environmental Research Institute, University College Cork, Cork, Ireland
                [4 ] Institute for Genome Sciences, University of Maryland School of Medicine, Baltimore, MD 21201, U.S.A.
                [5 ] Centre de Coopération Internationale en Recherche Agronomique pour le Développement, UMR BGPI, 34398 Montpellier Cedex 5, France
                [6 ] Department of Biological Sciences, Northern Arizona University, Flagstaff, AZ 86011-5640, U.S.A.
                [7 ] The Wellcome Trust Sanger Institute, The Wellcome Trust Genome Campus, Hinxton, Cambridge CB101SA, UK
                [8 ] MRC Centre for Outbreak Analysis and Modelling, Imperial College Faculty of Medicine, London W21PG, UK
                [9 ] Muséum National d'Histoire Naturelle - EPHE Department of Systematics and Evolution UMR-CNRS 7205, 75231 Paris, France
                [10 ] Institute of Human Genetics, German Research Center for Environmental Health, D-85764 Neuherberg, Germany
                [11 ] Unité Peste, Institut Pasteur de Madagascar, BP 1274 - 101, Madagascar
                [12 ] Division of Vector-Borne Infectious Diseases, Centers for Disease Control and Prevention, Fort Collins, CO, 80521, U.S.A.
                [13 ] Pathogen Genomics Division, Translational Genomics Research Institute, Phoenix, AZ 85404, U.S.A.
                [14 ] Institut Pasteur, Yersinia Research Unit, 28 rue du Dr. Roux, Paris, France.
                [15 ] Dept. of Microbiology, University College Cork, Cork, Ireland
                Author notes

                Author Contributions M.A., T.W., D.W., P.R., J.R., R.Y., D.M.W., P.K. designed the study; L.R., J.M.P., R.Y., E.C. contributed Y. pestis DNA and demographic information; G.M., Y.S., M.E., P.R., M.F., B.K., A.J.V., Y.L., Y.C., P.L., N.T. performed sequencing, SNP discovery, MassArray, and SNP testing; G.M., Y.S., C.J.M., M.E., P.R., D.M.W., P.L. performed bioinformatic analyses of the data; C.J.M., T.J., R.L., F.B., T.W. performed population genetic analyses; M.A., C.J.M., M.E., P.R., D.M.W., T.J., F.B., P.K., T.W., J.R., R.Y., E.C. wrote the manuscript.

                Correspondence and requests for materials should be addressed to M.A ( m.achtman@ 123456ucc.ie ), E.C. ( elisabeth.carniel@ 123456pasteur.fr ) or R.Y. ( ruifuyang@ 123456gmail.com )
                [*]

                These authors contributed equally to this work

                [†]

                Present addresses: G.M. & B.K: Max-Planck-Institut für molekulare Genetik, Ihnestraße 63/73,14195 Berlin, Germany; C.J.M.: Berlin Center for Genomics in Biodiversity Research (BeGenDiv), Altensteinstr. 6, 14195 Berlin, Germany; M.F.: Max-Delbrück-Centrum für molekulare Medizin (MDC) Berlin-Buch, Germany.

                Article
                UKMS32492
                10.1038/ng.705
                2999892
                21037571
                5b724884-5c3c-4a4c-ae15-5b5d8f5a52ec

                Users may view, print, copy, download and text and data- mine the content in such documents, for the purposes of academic research, subject always to the full Conditions of use: http://www.nature.com/authors/editorial_policies/license.html#terms

                Funding
                Funded by: Science Foundation Ireland :
                Award ID: 05/FE1/B882 || SFI_
                Categories
                Article

                Genetics
                phylogeography,epidemic spread,snp typing,neutral evolution,genomic comparisons
                Genetics
                phylogeography, epidemic spread, snp typing, neutral evolution, genomic comparisons

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