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      A New Phylogenetic Framework for the Animal-Adapted Mycobacterium tuberculosis Complex

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          Abstract

          Tuberculosis (TB) affects humans and other animals and is caused by bacteria from the Mycobacterium tuberculosis complex (MTBC). Previous studies have shown that there are at least nine members of the MTBC infecting animals other than humans; these have also been referred to as ecotypes. However, the ecology and the evolution of these animal-adapted MTBC ecotypes are poorly understood. Here we screened 12,886 publicly available MTBC genomes and newly sequenced 17 animal-adapted MTBC strains, gathering a total of 529 genomes of animal-adapted MTBC strains. Phylogenomic and comparative analyses confirm that the animal-adapted MTBC members are paraphyletic with some members more closely related to the human-adapted Mycobacterium africanum Lineage 6 than to other animal-adapted strains. Furthermore, we identified four main animal-adapted MTBC clades that might correspond to four main host shifts; two of these clades are hypothesized to reflect independent cattle domestication events. Contrary to what would be expected from an obligate pathogen, MTBC nucleotide diversity was not positively correlated with host phylogenetic distances, suggesting that host tropism in the animal-adapted MTBC seems to be driven by contact rates and demographic aspects of the host population rather by than host relatedness. By combining phylogenomics with ecological data, we propose an evolutionary scenario in which the ancestor of Lineage 6 and all animal-adapted MTBC ecotypes was a generalist pathogen that subsequently adapted to different host species. This study provides a new phylogenetic framework to better understand the evolution of the different ecotypes of the MTBC and guide future work aimed at elucidating the molecular mechanisms underlying host range.

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          Most cited references 99

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          Trimmomatic: a flexible trimmer for Illumina sequence data

          Motivation: Although many next-generation sequencing (NGS) read preprocessing tools already existed, we could not find any tool or combination of tools that met our requirements in terms of flexibility, correct handling of paired-end data and high performance. We have developed Trimmomatic as a more flexible and efficient preprocessing tool, which could correctly handle paired-end data. Results: The value of NGS read preprocessing is demonstrated for both reference-based and reference-free tasks. Trimmomatic is shown to produce output that is at least competitive with, and in many cases superior to, that produced by other tools, in all scenarios tested. Availability and implementation: Trimmomatic is licensed under GPL V3. It is cross-platform (Java 1.5+ required) and available at http://www.usadellab.org/cms/index.php?page=trimmomatic Contact: usadel@bio1.rwth-aachen.de Supplementary information: Supplementary data are available at Bioinformatics online.
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            RAxML-VI-HPC: maximum likelihood-based phylogenetic analyses with thousands of taxa and mixed models.

            RAxML-VI-HPC (randomized axelerated maximum likelihood for high performance computing) is a sequential and parallel program for inference of large phylogenies with maximum likelihood (ML). Low-level technical optimizations, a modification of the search algorithm, and the use of the GTR+CAT approximation as replacement for GTR+Gamma yield a program that is between 2.7 and 52 times faster than the previous version of RAxML. A large-scale performance comparison with GARLI, PHYML, IQPNNI and MrBayes on real data containing 1000 up to 6722 taxa shows that RAxML requires at least 5.6 times less main memory and yields better trees in similar times than the best competing program (GARLI) on datasets up to 2500 taxa. On datasets > or =4000 taxa it also runs 2-3 times faster than GARLI. RAxML has been parallelized with MPI to conduct parallel multiple bootstraps and inferences on distinct starting trees. The program has been used to compute ML trees on two of the largest alignments to date containing 25,057 (1463 bp) and 2182 (51,089 bp) taxa, respectively. icwww.epfl.ch/~stamatak
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              APE: Analyses of Phylogenetics and Evolution in R language.

              Analysis of Phylogenetics and Evolution (APE) is a package written in the R language for use in molecular evolution and phylogenetics. APE provides both utility functions for reading and writing data and manipulating phylogenetic trees, as well as several advanced methods for phylogenetic and evolutionary analysis (e.g. comparative and population genetic methods). APE takes advantage of the many R functions for statistics and graphics, and also provides a flexible framework for developing and implementing further statistical methods for the analysis of evolutionary processes. The program is free and available from the official R package archive at http://cran.r-project.org/src/contrib/PACKAGES.html#ape. APE is licensed under the GNU General Public License.
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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
                27 November 2018
                2018
                : 9
                Affiliations
                1Swiss Tropical and Public Health Institute , Basel, Switzerland
                2University of Basel , Basel, Switzerland
                3Istituto Zooprofilattico Sperimentale della Lombardia e dell’Emilia-Romagna: Centro Nazionale di Referenza per la Tubercolosi Bovina , Brescia, Italy
                4SAMRC Centre for TB Research, DST/NRF Centre of Excellence for Biomedical Tuberculosis Research, Division of Molecular Biology and Human Genetics, Faculty of Medicine and Health Sciences, Stellenbosch University , Stellenbosch, South Africa
                5Department of Biosystems Science and Engineering, ETH Zurich , Basel, Switzerland
                6McGill International TB Centre, Infectious Diseases and Immunity in Global Health, McGill University Health Centre and Research Institute , Montréal, QC, Canada
                7Mycobacterium Reference Laboratory, Victoria Infectious Diseases Reference Laboratory, Peter Doherty Institute , Melbourne, VIC, Australia
                8Institute for Integrative Systems Biology (I2SysBio), University of Valencia-CSIC , Valencia, Spain
                Author notes

                Edited by: Haiwei Luo, The Chinese University of Hong Kong, Hong Kong

                Reviewed by: Ana M. S. Guimaraes, Universidade de São Paulo, Brazil; Djaltou Aboubaker Osman, Center of Study and Research of Djibouti (CERD), Ethiopia; Javier Bezos, Complutense University of Madrid, Spain; Robson Francisco De Souza, Universidade de São Paulo, Brazil

                These authors have contributed equally to this work

                This article was submitted to Evolutionary and Genomic Microbiology, a section of the journal Frontiers in Microbiology

                Article
                10.3389/fmicb.2018.02820
                6277475
                Copyright © 2018 Brites, Loiseau, Menardo, Borrell, Boniotti, Warren, Dippenaar, Parsons, Beisel, Behr, Fyfe, Coscolla and Gagneux.

                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.

                Page count
                Figures: 6, Tables: 0, Equations: 0, References: 102, Pages: 14, Words: 0
                Funding
                Funded by: Schweizerischer Nationalfonds zur Förderung der Wissenschaftlichen Forschung 10.13039/501100001711
                Funded by: European Research Council 10.13039/501100000781
                Categories
                Microbiology
                Original Research

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