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      Revisiting the taxonomy and evolution of pathogenicity of the genus Leptospira through the prism of genomics

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          There is no author summary for this article yet. Authors can add summaries to their articles on ScienceOpen to make them more accessible to a non-specialist audience.

          Abstract

          The causative agents of leptospirosis are responsible for an emerging zoonotic disease worldwide. One of the major routes of transmission for leptospirosis is the natural environment contaminated with the urine of a wide range of reservoir animals. Soils and surface waters also host a high diversity of non-pathogenic Leptospira and species for which the virulence status is not clearly established. The genus Leptospira is currently divided into 35 species classified into three phylogenetic clusters, which supposedly correlate with the virulence of the bacteria. In this study, a total of 90 Leptospira strains isolated from different environments worldwide including Japan, Malaysia, New Caledonia, Algeria, mainland France, and the island of Mayotte in the Indian Ocean were sequenced. A comparison of average nucleotide identity (ANI) values of genomes of the 90 isolates and representative genomes of known species revealed 30 new Leptospira species. These data also supported the existence of two clades and 4 subclades. To avoid classification that strongly implies assumption on the virulence status of the lineages, we called them P1, P2, S1, S2. One of these subclades has not yet been described and is composed of Leptospira idonii and 4 novel species that are phylogenetically related to the saprophytes. We then investigated genome diversity and evolutionary relationships among members of the genus Leptospira by studying the pangenome and core gene sets. Our data enable the identification of genome features, genes and domains that are important for each subclade, thereby laying the foundation for refining the classification of this complex bacterial genus. We also shed light on atypical genomic features of a group of species that includes the species often associated with human infection, suggesting a specific and ongoing evolution of this group of species that will require more attention. In conclusion, we have uncovered a massive species diversity and revealed a novel subclade in environmental samples collected worldwide and we have redefined the classification of species in the genus. The implication of several new potentially infectious Leptospira species for human and animal health remains to be determined but our data also provide new insights into the emergence of virulence in the pathogenic species.

          Author summary

          Leptospirosis which is an emerging zoonotic disease worldwide, is transmitted to humans through contact with soils or surface waters contaminated with the urine of reservoir animals. Species of Leptospira, which include infectious and non-infectious strains, are ubiquitous in the environment. In this study we have sequenced the genomes of strains of Leptospira isolated from several environmental sources worldwide. Comparison of these genomes with other members of the Leptospira genus revealed the existence of 30 novel Leptospira species. A comparative genomic analysis of species of the genus allowed us to identify genes or genome features that are specific of infectious species, providing insights into virulence evolution in these atypical bacteria but also allow refinement of the Leptospira classification.

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          Most cited references 48

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          MAFFT Multiple Sequence Alignment Software Version 7: Improvements in Performance and Usability

          We report a major update of the MAFFT multiple sequence alignment program. This version has several new features, including options for adding unaligned sequences into an existing alignment, adjustment of direction in nucleotide alignment, constrained alignment and parallel processing, which were implemented after the previous major update. This report shows actual examples to explain how these features work, alone and in combination. Some examples incorrectly aligned by MAFFT are also shown to clarify its limitations. We discuss how to avoid misalignments, and our ongoing efforts to overcome such limitations.
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            Prokka: rapid prokaryotic genome annotation.

             T Seemann (2014)
            The multiplex capability and high yield of current day DNA-sequencing instruments has made bacterial whole genome sequencing a routine affair. The subsequent de novo assembly of reads into contigs has been well addressed. The final step of annotating all relevant genomic features on those contigs can be achieved slowly using existing web- and email-based systems, but these are not applicable for sensitive data or integrating into computational pipelines. Here we introduce Prokka, a command line software tool to fully annotate a draft bacterial genome in about 10 min on a typical desktop computer. It produces standards-compliant output files for further analysis or viewing in genome browsers. Prokka is implemented in Perl and is freely available under an open source GPLv2 license from http://vicbioinformatics.com/. © The Author 2014. Published by Oxford University Press. All rights reserved. For Permissions, please e-mail: journals.permissions@oup.com.
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              IQ-TREE: A Fast and Effective Stochastic Algorithm for Estimating Maximum-Likelihood Phylogenies

              Large phylogenomics data sets require fast tree inference methods, especially for maximum-likelihood (ML) phylogenies. Fast programs exist, but due to inherent heuristics to find optimal trees, it is not clear whether the best tree is found. Thus, there is need for additional approaches that employ different search strategies to find ML trees and that are at the same time as fast as currently available ML programs. We show that a combination of hill-climbing approaches and a stochastic perturbation method can be time-efficiently implemented. If we allow the same CPU time as RAxML and PhyML, then our software IQ-TREE found higher likelihoods between 62.2% and 87.1% of the studied alignments, thus efficiently exploring the tree-space. If we use the IQ-TREE stopping rule, RAxML and PhyML are faster in 75.7% and 47.1% of the DNA alignments and 42.2% and 100% of the protein alignments, respectively. However, the range of obtaining higher likelihoods with IQ-TREE improves to 73.3-97.1%.
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                Author and article information

                Contributors
                Role: Data curationRole: Formal analysisRole: InvestigationRole: MethodologyRole: SoftwareRole: Writing – original draftRole: Writing – review & editing
                Role: Data curationRole: Formal analysisRole: ValidationRole: Writing – review & editing
                Role: InvestigationRole: MethodologyRole: ResourcesRole: Writing – review & editing
                Role: Investigation
                Role: Formal analysisRole: InvestigationRole: Methodology
                Role: Investigation
                Role: Investigation
                Role: Investigation
                Role: Investigation
                Role: Formal analysisRole: InvestigationRole: Validation
                Role: Investigation
                Role: Investigation
                Role: ConceptualizationRole: Formal analysisRole: InvestigationRole: SupervisionRole: ValidationRole: Writing – original draftRole: Writing – review & editing
                Role: ConceptualizationRole: Formal analysisRole: Funding acquisitionRole: MethodologyRole: SupervisionRole: ValidationRole: Writing – original draft
                Role: ConceptualizationRole: Data curationRole: Formal analysisRole: Funding acquisitionRole: InvestigationRole: MethodologyRole: SupervisionRole: ValidationRole: Writing – original draft
                Role: Editor
                Journal
                PLoS Negl Trop Dis
                PLoS Negl Trop Dis
                plos
                plosntds
                PLoS Neglected Tropical Diseases
                Public Library of Science (San Francisco, CA USA )
                1935-2727
                1935-2735
                23 May 2019
                May 2019
                : 13
                : 5
                Affiliations
                [1 ] INRS-Institut Armand-Frappier, Bacterial Symbionts Evolution, Laval, Quebec, Canada
                [2 ] Institut Pasteur, Biology of Spirochetes unit, Paris, France
                [3 ] Université Paris Diderot, Ecole doctorale BioSPC, Paris, France
                [4 ] Institut Pasteur de Nouméa, Leptospirosis Research and Expertise Unit, Nouméa, New Caledonia
                [5 ] Universiti Putra Malaysia, Faculty of Medicine and Health Sciences, Department of Medical Microbiology and Parasitology, Serdang, Malaysia
                [6 ] Universiti Sains Malaysia, Department of Medical Microbiology and Parasitology, Kubang Kerian, Malaysia
                [7 ] Institute for Medical Research, Kuala Lumpur, Malaysia
                [8 ] Chiba Institute of Science, Faculty of Pharmaceutical Sciences, Laboratory of Microbiology and Immunology, Choshi, Japan
                [9 ] Hokkaido University, Department of Disease Control, Graduate School of Veterinary Medicine, Laboratory of Parasitology, Sapporo, Japan
                [10 ] Institut Pasteur d’Alger, Algeria
                Instituto Butantan, BRAZIL
                Author notes

                The authors have declared that no competing interests exist.

                ‡ PB, FJV and MP also contributed equally to this work.

                Article
                PNTD-D-18-01947
                10.1371/journal.pntd.0007270
                6532842
                31120895
                © 2019 Vincent et al

                This is an open access article distributed under the terms of the Creative Commons Attribution License, which permits unrestricted use, distribution, and reproduction in any medium, provided the original author and source are credited.

                Page count
                Figures: 8, Tables: 0, Pages: 25
                Product
                Funding
                Funded by: PTR
                Award ID: 30-17
                Award Recipient :
                This work was supported in part by a donation from Foundation MSD to the ‘PIBnet’ programme of Institut Pasteur, by Public Health France (SPF), by Institut Pasteur through grant PTR 30-2017 and by the Malaysia Ministry of Education through Long-Term Research Grant Scheme (LRGS Phase 2/2014, UPM/700-2/7/LRGS/5526400). This work was part of the PhD thesis of O. S. who received financial support from “Université Paris Diderot” and “Sorbonne Paris Cité”. ATV received a Postdoctoral Fellowship from the Natural Sciences and Engineering Research Council of Canada. FJV is a research scholar of the Fonds de Recherche du Québec-Santé. The funders had no role in the design, conduct or conclusions of the study.
                Categories
                Research Article
                Biology and Life Sciences
                Organisms
                Bacteria
                Leptospira
                Biology and Life Sciences
                Microbiology
                Medical Microbiology
                Microbial Pathogens
                Bacterial Pathogens
                Leptospira
                Medicine and Health Sciences
                Pathology and Laboratory Medicine
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                Leptospira Interrogans
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                Custom metadata
                All relevant data are within the paper and its Supporting Information files. Full-genome sequences can be found in NCBI using the accession numbers shown in S1 Table. Our curated species database is also publicly available at http://fveyrier.profs.inrs.ca/Download/Dataset.zip.

                Infectious disease & Microbiology

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