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      Genomic Diversity and Evolution of the Fish Pathogen Flavobacterium psychrophilum

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          Abstract

          Flavobacterium psychrophilum, the etiological agent of rainbow trout fry syndrome and bacterial cold-water disease in salmonid fish, is currently one of the main bacterial pathogens hampering the productivity of salmonid farming worldwide. In this study, the genomic diversity of the F. psychrophilum species is analyzed using a set of 41 genomes, including 30 newly sequenced isolates. These were selected on the basis of available MLST data with the two-fold objective of maximizing the coverage of the species diversity and of allowing a focus on the main clonal complex (CC-ST10) infecting farmed rainbow trout ( Oncorhynchus mykiss) worldwide. The results reveal a bacterial species harboring a limited genomic diversity both in terms of nucleotide diversity, with ~0.3% nucleotide divergence inside CDSs in pairwise genome comparisons, and in terms of gene repertoire, with the core genome accounting for ~80% of the genes in each genome. The pan-genome seems nevertheless “open” according to the scaling exponent of a power-law fitted on the rate of new gene discovery when genomes are added one-by-one. Recombination is a key component of the evolutionary process of the species as seen in the high level of apparent homoplasy in the core genome. Using a Hidden Markov Model to delineate recombination tracts in pairs of closely related genomes, the average recombination tract length was estimated to ~4.0 Kbp and the typical ratio of the contributions of recombination and mutations to nucleotide-level differentiation (r/m) was estimated to ~13. Within CC-ST10, evolutionary distances computed on non-recombined regions and comparisons between 22 isolates sampled up to 27 years apart suggest a most recent common ancestor in the second half of the nineteenth century in North America with subsequent diversification and transmission of this clonal complex coinciding with the worldwide expansion of rainbow trout farming. With the goal to promote the development of tools for the genetic manipulation of F. psychrophilum, a particular attention was also paid to plasmids. Their extraction and sequencing to completion revealed plasmid diversity that remained hidden to classical plasmid profiling due to size similarities.

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          Most cited references78

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          ClonalFrameML: Efficient Inference of Recombination in Whole Bacterial Genomes

          Recombination is an important evolutionary force in bacteria, but it remains challenging to reconstruct the imports that occurred in the ancestry of a genomic sample. Here we present ClonalFrameML, which uses maximum likelihood inference to simultaneously detect recombination in bacterial genomes and account for it in phylogenetic reconstruction. ClonalFrameML can analyse hundreds of genomes in a matter of hours, and we demonstrate its usefulness on simulated and real datasets. We find evidence for recombination hotspots associated with mobile elements in Clostridium difficile ST6 and a previously undescribed 310kb chromosomal replacement in Staphylococcus aureus ST582. ClonalFrameML is freely available at http://clonalframeml.googlecode.com/.
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            Estimating synonymous and nonsynonymous substitution rates under realistic evolutionary models.

            Q. Z. Yang (2000)
            Approximate methods for estimating the numbers of synonymous and nonsynonymous substitutions between two DNA sequences involve three steps: counting of synonymous and nonsynonymous sites in the two sequences, counting of synonymous and nonsynonymous differences between the two sequences, and correcting for multiple substitutions at the same site. We examine complexities involved in those steps and propose a new approximate method that takes into account two major features of DNA sequence evolution: transition/transversion rate bias and base/codon frequency bias. We compare the new method with maximum likelihood, as well as several other approximate methods, by examining infinitely long sequences, performing computer simulations, and analyzing a real data set. The results suggest that when there are transition/transversion rate biases and base/codon frequency biases, previously described approximate methods for estimating the nonsynonymous/synonymous rate ratio may involve serious biases, and the bias can be both positive and negative. The new method is, in general, superior to earlier approximate methods and may be useful for analyzing large data sets, although maximum likelihood appears to always be the method of choice.
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              Rate and molecular spectrum of spontaneous mutations in the bacterium Escherichia coli as determined by whole-genome sequencing.

              Knowledge of the rate and nature of spontaneous mutation is fundamental to understanding evolutionary and molecular processes. In this report, we analyze spontaneous mutations accumulated over thousands of generations by wild-type Escherichia coli and a derivative defective in mismatch repair (MMR), the primary pathway for correcting replication errors. The major conclusions are (i) the mutation rate of a wild-type E. coli strain is ~1 × 10(-3) per genome per generation; (ii) mutations in the wild-type strain have the expected mutational bias for G:C > A:T mutations, but the bias changes to A:T > G:C mutations in the absence of MMR; (iii) during replication, A:T > G:C transitions preferentially occur with A templating the lagging strand and T templating the leading strand, whereas G:C > A:T transitions preferentially occur with C templating the lagging strand and G templating the leading strand; (iv) there is a strong bias for transition mutations to occur at 5'ApC3'/3'TpG5' sites (where bases 5'A and 3'T are mutated) and, to a lesser extent, at 5'GpC3'/3'CpG5' sites (where bases 5'G and 3'C are mutated); (v) although the rate of small (≤4 nt) insertions and deletions is high at repeat sequences, these events occur at only 1/10th the genomic rate of base-pair substitutions. MMR activity is genetically regulated, and bacteria isolated from nature often lack MMR capacity, suggesting that modulation of MMR can be adaptive. Thus, comparing results from the wild-type and MMR-defective strains may lead to a deeper understanding of factors that determine mutation rates and spectra, how these factors may differ among organisms, and how they may be shaped by environmental conditions.
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                Author and article information

                Contributors
                Journal
                Front Microbiol
                Front Microbiol
                Front. Microbiol.
                Frontiers in Microbiology
                Frontiers Media S.A.
                1664-302X
                07 February 2018
                2018
                : 9
                : 138
                Affiliations
                [1] 1Unité de Virologie et Immunologie Moléculaires (VIM), Institut National de la Recherche Agronomique, Université Paris-Saclay , Jouy-en-Josas, France
                [2] 2Unité Mathématiques et Informatique Appliquées du Génome à l'Environnement (MaIAGE), Institut National de la Recherche Agronomique, Université Paris-Saclay , Jouy-en-Josas, France
                [3] 3Section for Bacteriology and Pathology, National Veterinary Institute, Technical University of Denmark , Kgs. Lyngby, Denmark
                [4] 4Department of Aquatic Animal health, Norwegian Veterinary Institute , Bergen, Norway
                [5] 5Laboratory of Aquatic Pathobiology, Environmental and Marine Biology, Faculty of Science and Engineering, Åbo Akademi University , Turku, Finland
                [6] 6Laboratory of Applied Microbiology, Department for Environment Constructions and Design, University of Applied Sciences and Arts of Southern Switzerland (SUPSI) , Bellinzona, Switzerland
                [7] 7Centre for Fish and Wildlife Health (FIWI), University of Bern , Bern, Switzerland
                [8] 8Department of Fish Pathology, Istituto Zooprofilattico Sperimentale delle Venezie , Legnaro, Italy
                [9] 9National Center for Cool and Cold Water Aquaculture, Agricultural Research Service, United States Department of Agriculture , Kearneysville, WV, United States
                [10] 10Department of Fisheries, Kindai University , Nara, Japan
                [11] 11Departamento Facultad de Ciencias Biológicas, Universidad Andres Bello, Universidad Andres BelloViña del Mar, Interdisciplinary Center for Aquaculture Research , Concepción, Chile
                Author notes

                Edited by: Shicheng Chen, Michigan State University, United States

                Reviewed by: Ernesto Ormeño-Orrillo, National Agrarian University, Peru; Karol Gliniewicz, University of Idaho, United States

                *Correspondence: Eric Duchaud eric.duchaud@ 123456inra.fr

                This article was submitted to Microbial Physiology and Metabolism, a section of the journal Frontiers in Microbiology

                Article
                10.3389/fmicb.2018.00138
                5808330
                29467746
                29eab928-49c4-4412-a18a-7b941ccdcbf3
                Copyright © 2018 Duchaud, Rochat, Habib, Barbier, Loux, Guérin, Dalsgaard, Madsen, Nilsen, Sundell, Wiklund, Strepparava, Wahli, Caburlotto, Manfrin, Wiens, Fujiwara-Nagata, Avendaño-Herrera, Bernardet and Nicolas.

                This is an open-access article distributed under the terms of the Creative Commons Attribution License (CC BY). The use, distribution or reproduction in other forums is permitted, provided the original author(s) and the copyright owner are credited and that the original publication in this journal is cited, in accordance with accepted academic practice. No use, distribution or reproduction is permitted which does not comply with these terms.

                History
                : 27 July 2017
                : 22 January 2018
                Page count
                Figures: 9, Tables: 1, Equations: 0, References: 97, Pages: 20, Words: 15789
                Categories
                Microbiology
                Original Research

                Microbiology & Virology
                flavobacterium psychrophilum,aquaculture,fish-pathogenic bacteria,comparative genomics,clonal-complex,homologous recombination

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