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      Shigella sonnei genome sequencing and phylogenetic analysis indicate recent global dissemination from Europe

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          Abstract

          Shigella are human-adapted Escherichia coli that have gained the ability to invade the human gut mucosa and cause dysentery 1, 2 , spreading efficiently via low-dose fecal-oral transmission 3, 4 . Historically, S. sonnei has been predominantly responsible for dysentery in developed countries, but is now emerging as a problem in the developing world, apparently replacing the more diverse S. flexneri in areas undergoing economic development and improvements in water quality 4- 6 . Classical approaches have shown S. sonnei is genetically conserved and clonal 7 . We report here whole-genome sequencing of 132 globally-distributed isolates. Our phylogenetic analysis shows that the current S. sonnei population descends from a common ancestor that existed less than 500 years ago and has diversified into several distinct lineages with unique characteristics. Our analysis suggests the majority of this diversification occurred in Europe, followed by more recent establishment of local pathogen populations in other continents predominantly due to the pandemic spread of a single, rapidly-evolving, multidrug resistant lineage.

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          Most cited references31

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          Microorganisms resistant to free-living amoebae.

          Free-living amoebae feed on bacteria, fungi, and algae. However, some microorganisms have evolved to become resistant to these protists. These amoeba-resistant microorganisms include established pathogens, such as Cryptococcus neoformans, Legionella spp., Chlamydophila pneumoniae, Mycobacterium avium, Listeria monocytogenes, Pseudomonas aeruginosa, and Francisella tularensis, and emerging pathogens, such as Bosea spp., Simkania negevensis, Parachlamydia acanthamoebae, and Legionella-like amoebal pathogens. Some of these amoeba-resistant bacteria (ARB) are lytic for their amoebal host, while others are considered endosymbionts, since a stable host-parasite ratio is maintained. Free-living amoebae represent an important reservoir of ARB and may, while encysted, protect the internalized bacteria from chlorine and other biocides. Free-living amoebae may act as a Trojan horse, bringing hidden ARB within the human "Troy," and may produce vesicles filled with ARB, increasing their transmission potential. Free-living amoebae may also play a role in the selection of virulence traits and in adaptation to survival in macrophages. Thus, intra-amoebal growth was found to enhance virulence, and similar mechanisms seem to be implicated in the survival of ARB in response to both amoebae and macrophages. Moreover, free-living amoebae represent a useful tool for the culture of some intracellular bacteria and new bacterial species that might be potential emerging pathogens.
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            Global burden of Shigella infections: implications for vaccine development and implementation of control strategies.

            Few studies provide data on the global morbidity and mortality caused by infection with Shigella spp.; such estimates are needed, however, to plan strategies of prevention and treatment. Here we report the results of a review of the literature published between 1966 and 1997 on Shigella infection. The data obtained permit calculation of the number of cases of Shigella infection and the associated mortality occurring worldwide each year, by age, and (as a proxy for disease severity) by clinical category, i.e. mild cases remaining at home, moderate cases requiring outpatient care, and severe cases demanding hospitalization. A sensitivity analysis was performed to estimate the high and low range of morbid and fatal cases in each category. Finally, the frequency distribution of Shigella infection, by serogroup and serotype and by region of the world, was determined. The annual number of Shigella episodes throughout the world was estimated to be 164.7 million, of which 163.2 million were in developing countries (with 1.1 million deaths) and 1.5 million in industrialized countries. A total of 69% of all episodes and 61% of all deaths attributable to shigellosis involved children under 5 years of age. The median percentages of isolates of S. flexneri, S. sonnei, S. boydii, and S. dysenteriae were, respectively, 60%, 15%, 6%, and 6% (30% of S. dysenteriae cases were type 1) in developing countries; and 16%, 77%, 2%, and 1% in industrialized countries. In developing countries, the predominant serotype of S. flexneri is 2a, followed by 1b, 3a, 4a, and 6. In industrialized countries, most isolates are S. flexneri 2a or other unspecified type 2 strains. Shigellosis, which continues to have an important global impact, cannot be adequately controlled with the existing prevention and treatment measures. Innovative strategies, including development of vaccines against the most common serotypes, could provide substantial benefits.
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              Phylogenetic diversity and historical patterns of pandemic spread of Yersinia pestis

              Pandemic infectious diseases have accompanied humans since their origins1, and have shaped the form of civilizations2. 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.

                Author and article information

                Journal
                9216904
                2419
                Nat Genet
                Nat. Genet.
                Nature genetics
                1061-4036
                1546-1718
                6 July 2012
                05 August 2012
                September 2012
                01 March 2013
                : 44
                : 9
                : 1056-1059
                Affiliations
                [1 ]University of Melbourne, Department of Microbiology and Immunology, Royal Parade, Melbourne, Victoria, 3010, Australia
                [2 ]The Hospital for Tropical Diseases, Wellcome Trust Major Overseas Programme, Oxford University Clinical Research Unit, Ho Chi Minh City, Vietnam
                [3 ]Institut Pasteur, Unité des Bactéries Pathogènes Entériques, Paris, France
                [4 ]Center for Infectious Disease Dynamics, Department of Biology, The Pennsylvania State University, University Park, PA 16802, USA
                [5 ]Fogarty International Center, National Institutes of Health, Bethesda, MD 20892, USA
                [6 ]Strathclyde Institute of Pharmacy and Biomedical Sciences, University of Strathclyde, Glasgow, G4 0RE, UK
                [7 ]Scottish Salmonella, Shigella and Clostridium difficile Reference Laboratory, Stobhill Hospital, 133 Balornock Road, Glasgow, UK
                [8 ]Molecular Biology Laboratory, International Vaccine Institute (IVI), Seoul, Republic of Korea
                [9 ]Department of Pharmacy, College of Pharmacy, Hanyang University, Ansan, Kyeonggi-do, 426-791, Korea
                [10 ]Department of Genetics, Evolution and Bioagents, Biology Institute, Campinas State University – UNICAMP, Brazil
                [11 ]Wellcome Trust Sanger Institute, Wellcome Trust Genome Campus, Hinxton, Cambridge, UK, CB10 1SA
                Article
                UKMS49152
                10.1038/ng.2369
                3442231
                22863732
                0c00aa71-a73b-4b98-a29b-557a3d73ec6d

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                Genetics
                Genetics

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