Enrico Tortoli1, Tarcisio Fedrizzi2, Conor J Meehan3, Alberto Trovato4, Antonella Grottola5, Elisabetta Giacobazzi6, Giulia Fregni Serpini7, Sara Tagliazucchi8, Anna Fabio9, Clotilde Bettua10, Roberto Bertorelli11, Francesca Frascaro12, Veronica De Sanctis13, Monica Pecorari14, Olivier Jousson15, Nicola Segata16, Daniela M Cirillo17. 1. Emerging Bacterial Pathogens Unit, IRCCS San Raffaele Scientific Institute, Milano, Italy. Electronic address: tortoli.enrico@hsr.it. 2. Centre for Integrative Biology, University of Trento, Trento, Italy. Electronic address: t.fedrizzi@unitn.it. 3. Mycobacteriology unit, Department of Biomedical Science, Institute of Tropical Medicine, Antwerp, Belgium. Electronic address: cmeehan@itg.be. 4. Emerging Bacterial Pathogens Unit, IRCCS San Raffaele Scientific Institute, Milano, Italy. Electronic address: trovato.alberto@hsr.it. 5. Microbiology and Virology Unit, University Hospital Polyclinic, Modena, Italy. Electronic address: grottola.antonella@policlinico.mo.it. 6. Centre for Integrative Biology, University of Trento, Trento, Italy. 7. Microbiology and Virology Unit, University Hospital Polyclinic, Modena, Italy. 8. Microbiology and Virology Unit, University Hospital Polyclinic, Modena, Italy. Electronic address: tagliazucchi.sara@policlinico.mo.it. 9. Microbiology and Virology Unit, University Hospital Polyclinic, Modena, Italy. Electronic address: fabio.anna@policlinico.mo.it. 10. Centre for Integrative Biology, University of Trento, Trento, Italy. Electronic address: clotilde.bettua@unitn.it. 11. NGS Facility, Laboratory of Biomolecular Sequence and Structure Analysis for Health, Centre for Integrative Biology, University of Trento, Italy. Electronic address: roberto.bertorelli@unitn.it. 12. Microbiology and Virology Unit, University Hospital Polyclinic, Modena, Italy. Electronic address: francescafrascaro@libero.it. 13. NGS Facility, Laboratory of Biomolecular Sequence and Structure Analysis for Health, Centre for Integrative Biology, University of Trento, Italy. Electronic address: veronica.desanctis@unitn.it. 14. Microbiology and Virology Unit, University Hospital Polyclinic, Modena, Italy. Electronic address: pecorari.monica@policlinico.mo.it. 15. Centre for Integrative Biology, University of Trento, Trento, Italy. Electronic address: olivier.jousson@unitn.it. 16. Centre for Integrative Biology, University of Trento, Trento, Italy. Electronic address: nicola.segata@unitn.it. 17. Emerging Bacterial Pathogens Unit, IRCCS San Raffaele Scientific Institute, Milano, Italy. Electronic address: cirillo.daniela@hsr.it.
Abstract
BACKGROUND: Phylogenetic studies of bacteria have been based so far either on a single gene (usually the 16S rRNA) or on concatenated housekeeping genes. For what concerns the genus Mycobacterium these approaches support the separation of rapidly and slowly growing species and the clustering of most species in well-defined phylogenetic groups. The advent of high-throughput shotgun sequencing leads us to revise conventional taxonomy of mycobacteria on the light of genomic data. For this purpose we investigated 88 newly sequenced species in addition to 60 retrieved from GenBank and used the Average Nucleotide Identity pairwise scores to reconstruct phylogenetic relationships within this genus. RESULTS: Our analysis confirmed the separation of slow and rapid growers and the intermediate position occupied by the M. terrae complex. Among the rapid growers, the species of the M. chelonae-abscessus complex belonged to the most ancestral cluster. Other major clades of rapid growers included the species related to M. fortuitum and M. smegmatis and a large grouping containing mostly environmental species rarely isolated from humans. The members of the M. terrae complex appeared as the most ancestral slow growers. Among slow growers two deep branches led to the clusters of species related to M. celatum and M. xenopi and to a large group harboring most of the species more frequently responsible of disease in humans, including the major pathogenic mycobacteria (M. tuberculosis, M. leprae, M. ulcerans). The species previously grouped in the M. simiae complex were allocated in a number of sub-clades; of them, only the one including the species M. simiae identified the real members of this complex. The other clades included also species previously not considered related to M. simiae. The ANI analysis, in most cases supported by Genome to Genome Distance and by Genomic Signature-Delta Difference, showed that a number of species with standing in literature were indeed synonymous. CONCLUSIONS: Genomic data revealed to be much more informative in comparison with phenotype. We believe that the genomic revolution enabled by high-throughput shotgun sequencing should now be considered in order to revise the conservative approaches still informing taxonomic sciences.
BACKGROUND: Phylogenetic studies of bacteria have been based so far either on a single gene (usually the 16S rRNA) or on concatenated housekeeping genes. For what concerns the genus Mycobacterium these approaches support the separation of rapidly and slowly growing species and the clustering of most species in well-defined phylogenetic groups. The advent of high-throughput shotgun sequencing leads us to revise conventional taxonomy of mycobacteria on the light of genomic data. For this purpose we investigated 88 newly sequenced species in addition to 60 retrieved from GenBank and used the Average Nucleotide Identity pairwise scores to reconstruct phylogenetic relationships within this genus. RESULTS: Our analysis confirmed the separation of slow and rapid growers and the intermediate position occupied by the M. terrae complex. Among the rapid growers, the species of the M. chelonae-abscessus complex belonged to the most ancestral cluster. Other major clades of rapid growers included the species related to M. fortuitum and M. smegmatis and a large grouping containing mostly environmental species rarely isolated from humans. The members of the M. terrae complex appeared as the most ancestral slow growers. Among slow growers two deep branches led to the clusters of species related to M. celatum and M. xenopi and to a large group harboring most of the species more frequently responsible of disease in humans, including the major pathogenic mycobacteria (M. tuberculosis, M. leprae, M. ulcerans). The species previously grouped in the M. simiae complex were allocated in a number of sub-clades; of them, only the one including the species M. simiae identified the real members of this complex. The other clades included also species previously not considered related to M. simiae. The ANI analysis, in most cases supported by Genome to Genome Distance and by Genomic Signature-Delta Difference, showed that a number of species with standing in literature were indeed synonymous. CONCLUSIONS: Genomic data revealed to be much more informative in comparison with phenotype. We believe that the genomic revolution enabled by high-throughput shotgun sequencing should now be considered in order to revise the conservative approaches still informing taxonomic sciences.
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