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      Reductive evolution in Streptococcus agalactiae and the emergence of a host adapted lineage

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          Abstract

          Background

          During host specialization, inactivation of genes whose function is no more required is favored by changes in selective constraints and evolutionary bottlenecks. The Gram positive bacteria Streptococcus agalactiae (also called GBS), responsible for septicemia and meningitis in neonates also emerged during the seventies as a cause of severe epidemics in fish farms. To decipher the genetic basis for the emergence of these highly virulent GBS strains and of their adaptation to fish, we have analyzed the genomic sequence of seven strains isolated from fish and other poikilotherms.

          Results

          Comparative analysis shows that the two groups of GBS strains responsible for fish epidemic diseases are only distantly related. While strains belonging to the clonal complex 7 cannot be distinguished from their human CC7 counterparts according to their gene content, strains belonging to the ST260-261 types probably diverged a long time ago. In this lineage, specialization to the fish host was correlated with a massive gene inactivation and broad changes in gene expression. We took advantage of the low level of sequence divergence between GBS strains and of the emergence of sublineages to reconstruct the different steps involved in this process. Non-homologous recombination was found to have played a major role in the genome erosion.

          Conclusions

          Our results show that the early phase of genome reduction during host specialization mostly involves accumulation of small and likely reversible indels, followed by a second evolutionary step marked by a higher frequency of large deletions.

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          Most cited references69

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          Genome analysis of multiple pathogenic isolates of Streptococcus agalactiae: implications for the microbial "pan-genome".

          The development of efficient and inexpensive genome sequencing methods has revolutionized the study of human bacterial pathogens and improved vaccine design. Unfortunately, the sequence of a single genome does not reflect how genetic variability drives pathogenesis within a bacterial species and also limits genome-wide screens for vaccine candidates or for antimicrobial targets. We have generated the genomic sequence of six strains representing the five major disease-causing serotypes of Streptococcus agalactiae, the main cause of neonatal infection in humans. Analysis of these genomes and those available in databases showed that the S. agalactiae species can be described by a pan-genome consisting of a core genome shared by all isolates, accounting for approximately 80% of any single genome, plus a dispensable genome consisting of partially shared and strain-specific genes. Mathematical extrapolation of the data suggests that the gene reservoir available for inclusion in the S. agalactiae pan-genome is vast and that unique genes will continue to be identified even after sequencing hundreds of genomes.
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            Artemis: sequence visualization and annotation

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              Comparative analysis of the genome sequences of Bordetella pertussis, Bordetella parapertussis and Bordetella bronchiseptica.

              Bordetella pertussis, Bordetella parapertussis and Bordetella bronchiseptica are closely related Gram-negative beta-proteobacteria that colonize the respiratory tracts of mammals. B. pertussis is a strict human pathogen of recent evolutionary origin and is the primary etiologic agent of whooping cough. B. parapertussis can also cause whooping cough, and B. bronchiseptica causes chronic respiratory infections in a wide range of animals. We sequenced the genomes of B. bronchiseptica RB50 (5,338,400 bp; 5,007 predicted genes), B. parapertussis 12822 (4,773,551 bp; 4,404 genes) and B. pertussis Tohama I (4,086,186 bp; 3,816 genes). Our analysis indicates that B. parapertussis and B. pertussis are independent derivatives of B. bronchiseptica-like ancestors. During the evolution of these two host-restricted species there was large-scale gene loss and inactivation; host adaptation seems to be a consequence of loss, not gain, of function, and differences in virulence may be related to loss of regulatory or control functions.
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                Author and article information

                Contributors
                Journal
                BMC Genomics
                BMC Genomics
                BMC Genomics
                BioMed Central
                1471-2164
                2013
                15 April 2013
                : 14
                : 252
                Affiliations
                [1 ]Unité de Biologie des Bactéries Pathogènes à Gram Positif, 28 rue du Docteur Roux, Paris, Cedex 15, 75724, France
                [2 ]CNRS UMR 3525, Paris, France
                [3 ]CEA/IG/Genoscope, Evry, France
                [4 ]Genomic Platform, Institut Pasteur, Paris, France
                [5 ]Unité de Biologie des Bactéries Intracellulaires, Institut Pasteur, Paris, France
                Article
                1471-2164-14-252
                10.1186/1471-2164-14-252
                3637634
                23586779
                799627dc-595c-4007-9aaf-afa5c0d6b0d1
                Copyright © 2013 Rosinski-Chupin et al.; licensee BioMed Central Ltd.

                This is an Open Access article distributed under the terms of the Creative Commons Attribution License ( http://creativecommons.org/licenses/by/2.0), which permits unrestricted use, distribution, and reproduction in any medium, provided the original work is properly cited.

                History
                : 31 December 2012
                : 1 April 2013
                Categories
                Research Article

                Genetics
                streptococcus agalactiae,host-adaptation,non-homologous recombination,gene inactivation,virulence

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