Revisiting the taxonomy and evolution of pathogenicity of the genus Leptospira through the prism of genomics
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...
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| Published in | PLoS neglected tropical diseases Vol. 13; no. 5; p. e0007270 |
|---|---|
| Main Authors | , , , , , , , , , , , , , , |
| Format | Journal Article |
| Language | English |
| Published |
United States
Public Library of Science
23.05.2019
Public Library of Science (PLoS) |
| Subjects | |
| Online Access | Get full text |
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| 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. |
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| AbstractList | 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. 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.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. 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. 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. |
| Audience | Academic |
| Author | Nakao, Ryo Amran, Fairuz Thibeaux, Roman Goarant, Cyrille Ismail, Nabilah Neela, Vasantha Kumari Veyrier, Frederic J. Mohd Khalid, Mohd Khairul Nizam Amara Korba, Anissa Masuzawa, Toshiyuki Vincent, Antony T. Bourhy, Pascale Picardeau, Mathieu Schiettekatte, Olivier Bernet, Eve |
| AuthorAffiliation | 9 Hokkaido University, Department of Disease Control, Graduate School of Veterinary Medicine, Laboratory of Parasitology, Sapporo, Japan 7 Institute for Medical Research, Kuala Lumpur, Malaysia 10 Institut Pasteur d’Alger, Algeria 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 Instituto Butantan, BRAZIL 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 1 INRS-Institut Armand-Frappier, Bacterial Symbionts Evolution, Laval, Quebec, Canada 8 Chiba Institute of Science, Faculty of Pharmaceutical Sciences, Laboratory of Microbiology and Immunology, Choshi, Japan |
| AuthorAffiliation_xml | – name: Instituto Butantan, BRAZIL – name: 10 Institut Pasteur d’Alger, Algeria – name: 4 Institut Pasteur de Nouméa, Leptospirosis Research and Expertise Unit, Nouméa, New Caledonia – name: 1 INRS-Institut Armand-Frappier, Bacterial Symbionts Evolution, Laval, Quebec, Canada – name: 6 Universiti Sains Malaysia, Department of Medical Microbiology and Parasitology, Kubang Kerian, Malaysia – name: 5 Universiti Putra Malaysia, Faculty of Medicine and Health Sciences, Department of Medical Microbiology and Parasitology, Serdang, Malaysia – name: 8 Chiba Institute of Science, Faculty of Pharmaceutical Sciences, Laboratory of Microbiology and Immunology, Choshi, Japan – name: 7 Institute for Medical Research, Kuala Lumpur, Malaysia – name: 9 Hokkaido University, Department of Disease Control, Graduate School of Veterinary Medicine, Laboratory of Parasitology, Sapporo, Japan – name: 2 Institut Pasteur, Biology of Spirochetes unit, Paris, France – name: 3 Université Paris Diderot, Ecole doctorale BioSPC, Paris, France |
| Author_xml | – sequence: 1 givenname: Antony T. surname: Vincent fullname: Vincent, Antony T. – sequence: 2 givenname: Olivier surname: Schiettekatte fullname: Schiettekatte, Olivier – sequence: 3 givenname: Cyrille orcidid: 0000-0002-0690-9464 surname: Goarant fullname: Goarant, Cyrille – sequence: 4 givenname: Vasantha Kumari surname: Neela fullname: Neela, Vasantha Kumari – sequence: 5 givenname: Eve surname: Bernet fullname: Bernet, Eve – sequence: 6 givenname: Roman surname: Thibeaux fullname: Thibeaux, Roman – sequence: 7 givenname: Nabilah surname: Ismail fullname: Ismail, Nabilah – sequence: 8 givenname: Mohd Khairul Nizam orcidid: 0000-0001-7200-3102 surname: Mohd Khalid fullname: Mohd Khalid, Mohd Khairul Nizam – sequence: 9 givenname: Fairuz surname: Amran fullname: Amran, Fairuz – sequence: 10 givenname: Toshiyuki surname: Masuzawa fullname: Masuzawa, Toshiyuki – sequence: 11 givenname: Ryo orcidid: 0000-0002-3105-7603 surname: Nakao fullname: Nakao, Ryo – sequence: 12 givenname: Anissa surname: Amara Korba fullname: Amara Korba, Anissa – sequence: 13 givenname: Pascale surname: Bourhy fullname: Bourhy, Pascale – sequence: 14 givenname: Frederic J. surname: Veyrier fullname: Veyrier, Frederic J. – sequence: 15 givenname: Mathieu orcidid: 0000-0002-5338-5579 surname: Picardeau fullname: Picardeau, Mathieu |
| BackLink | https://www.ncbi.nlm.nih.gov/pubmed/31120895$$D View this record in MEDLINE/PubMed https://riip.hal.science/pasteur-02275485$$DView record in HAL |
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