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      Characterization of the First Virulent Phage Infecting Oenococcus oeni, the Queen of the Cellars

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          Abstract

          There has been little exploration of how phages contribute to the diversity of the bacterial community associated with winemaking and may impact fermentations and product quality. Prophages of Oenococcus oeni, the most common species of lactic acid bacteria (LAB) associated with malolactic fermentation of wine, have been described, but no data is available regarding phages of O. oeni with true virulent lifestyles. The current study reports on the incidence and characterization of the first group of virulent oenophages named Vinitor, isolated from the enological environment. Vinitor phages are morphologically very similar to siphoviruses infecting other LAB. Although widespread during winemaking, they are more abundant in musts than temperate oenophages. We obtained the complete genomic sequences of phages Vinitor162 and Vinitor27, isolated from white and red wines, respectively. The assembled genomes shared 97.6% nucleotide identity and belong to the same species. Coupled with phylogenetic analysis, our study revealed that the genomes of Vinitor phages are architecturally mosaics and represent unique combinations of modules amongst LAB infecting-phages. Our data also provide some clues to possible evolutionary connections between Vinitor and (pro)phages associated to epiphytic and insect-related bacteria.

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          Most cited references71

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          SPAdes: a new genome assembly algorithm and its applications to single-cell sequencing.

          The lion's share of bacteria in various environments cannot be cloned in the laboratory and thus cannot be sequenced using existing technologies. A major goal of single-cell genomics is to complement gene-centric metagenomic data with whole-genome assemblies of uncultivated organisms. Assembly of single-cell data is challenging because of highly non-uniform read coverage as well as elevated levels of sequencing errors and chimeric reads. We describe SPAdes, a new assembler for both single-cell and standard (multicell) assembly, and demonstrate that it improves on the recently released E+V-SC assembler (specialized for single-cell data) and on popular assemblers Velvet and SoapDeNovo (for multicell data). SPAdes generates single-cell assemblies, providing information about genomes of uncultivatable bacteria that vastly exceeds what may be obtained via traditional metagenomics studies. SPAdes is available online ( http://bioinf.spbau.ru/spades ). It is distributed as open source software.
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            Gapped BLAST and PSI-BLAST: a new generation of protein database search programs.

            S Altschul (1997)
            The BLAST programs are widely used tools for searching protein and DNA databases for sequence similarities. For protein comparisons, a variety of definitional, algorithmic and statistical refinements described here permits the execution time of the BLAST programs to be decreased substantially while enhancing their sensitivity to weak similarities. A new criterion for triggering the extension of word hits, combined with a new heuristic for generating gapped alignments, yields a gapped BLAST program that runs at approximately three times the speed of the original. In addition, a method is introduced for automatically combining statistically significant alignments produced by BLAST into a position-specific score matrix, and searching the database using this matrix. The resulting Position-Specific Iterated BLAST (PSI-BLAST) program runs at approximately the same speed per iteration as gapped BLAST, but in many cases is much more sensitive to weak but biologically relevant sequence similarities. PSI-BLAST is used to uncover several new and interesting members of the BRCT superfamily.
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              New algorithms and methods to estimate maximum-likelihood phylogenies: assessing the performance of PhyML 3.0.

              PhyML is a phylogeny software based on the maximum-likelihood principle. Early PhyML versions used a fast algorithm performing nearest neighbor interchanges to improve a reasonable starting tree topology. Since the original publication (Guindon S., Gascuel O. 2003. A simple, fast and accurate algorithm to estimate large phylogenies by maximum likelihood. Syst. Biol. 52:696-704), PhyML has been widely used (>2500 citations in ISI Web of Science) because of its simplicity and a fair compromise between accuracy and speed. In the meantime, research around PhyML has continued, and this article describes the new algorithms and methods implemented in the program. First, we introduce a new algorithm to search the tree space with user-defined intensity using subtree pruning and regrafting topological moves. The parsimony criterion is used here to filter out the least promising topology modifications with respect to the likelihood function. The analysis of a large collection of real nucleotide and amino acid data sets of various sizes demonstrates the good performance of this method. Second, we describe a new test to assess the support of the data for internal branches of a phylogeny. This approach extends the recently proposed approximate likelihood-ratio test and relies on a nonparametric, Shimodaira-Hasegawa-like procedure. A detailed analysis of real alignments sheds light on the links between this new approach and the more classical nonparametric bootstrap method. Overall, our tests show that the last version (3.0) of PhyML is fast, accurate, stable, and ready to use. A Web server and binary files are available from http://www.atgc-montpellier.fr/phyml/.
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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
                13 January 2021
                2020
                : 11
                : 596541
                Affiliations
                [1] 1University of Bordeaux, ISVV, EA4577 Œnologie , Villenave d’Ornon, France
                [2] 2INRA, ISVV, USC 1366 Oenologie , Villenave d’Ornon, France
                [3] 3Architecture et Fonction des Macromolécules Biologiques, Aix-Marseille Université, Campus de Luminy , Marseille, France
                [4] 4Architecture et Fonction des Macromolécules Biologiques, Centre National de la Recherche Scientifique (CNRS) , Marseille, France
                [5] 5Bordeaux INP, ISVV, EA4577 Œnologie , Villenave d’Ornon, France
                Author notes

                Edited by: Andrew S. Lang, Memorial University of Newfoundland, Canada

                Reviewed by: Raul Raya, CONICET Centro de Referencia para Lactobacilos (CERELA), Argentina; Vittorio Capozzi, Italian National Research Council, Italy

                *Correspondence: Claire Le Marrec, clehenaff@ 123456enscbp.fr

                These authors have contributed equally to this work

                This article was submitted to Virology, a section of the journal Frontiers in Microbiology

                Article
                10.3389/fmicb.2020.596541
                7838156
                33519734
                f1362085-4907-44e8-a6a2-53a7db529b85
                Copyright © 2021 Philippe, Chaïb, Jaomanjaka, Claisse, Lucas, Samot, Cambillau and Le Marrec.

                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(s) 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
                : 19 August 2020
                : 14 December 2020
                Page count
                Figures: 5, Tables: 3, Equations: 0, References: 72, Pages: 13, Words: 0
                Funding
                Funded by: Agence Nationale de la Recherche 10.13039/501100001665
                Categories
                Microbiology
                Original Research

                Microbiology & Virology
                lactic acid bacteria,phage (bacteriophage),phage phylogenetics,lytic phage,oenococcus,fermentation,wine,grapes

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