Phylogenomics of Globally Spread Clonal Groups 14 and 15 of Klebsiella pneumoniae
ABSTRACT Klebsiella pneumoniae sequence type 14 (ST14) and ST15 caused outbreaks of CTX-M-15 and/or carbapenemase producers worldwide, but their phylogeny and global dynamics remain unclear. We clarified the evolution of K. pneumoniae clonal group 14 (CG14) and CG15 by analyzing the capsular locus (...
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| Format: | Article |
| Language: | English |
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American Society for Microbiology
2023-06-01
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| Series: | Microbiology Spectrum |
| Subjects: | |
| Online Access: | https://journals.asm.org/doi/10.1128/spectrum.03395-22 |
| _version_ | 1827925065990144000 |
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| author | Carla Rodrigues Val F. Lanza Luísa Peixe Teresa M. Coque Ângela Novais |
| author_facet | Carla Rodrigues Val F. Lanza Luísa Peixe Teresa M. Coque Ângela Novais |
| author_sort | Carla Rodrigues |
| collection | DOAJ |
| description | ABSTRACT Klebsiella pneumoniae sequence type 14 (ST14) and ST15 caused outbreaks of CTX-M-15 and/or carbapenemase producers worldwide, but their phylogeny and global dynamics remain unclear. We clarified the evolution of K. pneumoniae clonal group 14 (CG14) and CG15 by analyzing the capsular locus (KL), resistome, virulome, and plasmidome of public genomes (n = 481) and de novo sequences (n = 9) representing main sublineages circulating in Portugal. CG14 and CG15 evolved independently within 6 main subclades defined according to the KL and the accessory genome. The CG14 (n = 65) clade was structured in two large monophyletic subclades, CG14-I (KL2, 86%) and CG14-II (KL16, 14%), whose emergences were dated to 1932 and 1911, respectively. Genes encoding extended-spectrum β-lactamase (ESBL), AmpC, and/or carbapenemases were mostly observed in CG14-I (71% versus 22%). CG15 clade (n = 170) was segregated into subclades CG15-IA (KL19/KL106, 9%), CG15-IB (variable KL types, 6%), CG15-IIA (KL24, 43%) and CG15-IIB (KL112, 37%). Most CG15 genomes carried specific GyrA and ParC mutations and emerged from a common ancestor in 1989. CTX-M-15 was especially prevalent in CG15 (68% CG15 versus 38% CG14) and in CG15-IIB (92%). Plasmidome analysis revealed 27 predominant plasmid groups (PG), including particularly pervasive and recombinant F-type (n = 10), Col (n = 10), and new plasmid types. While blaCTX-M-15 was acquired multiple times by a high diversity of F-type mosaic plasmids, other antibiotic resistance genes (ARGs) were dispersed by IncL (blaOXA-48) or IncC (blaCMY/TEM-24) plasmids. We first demonstrate an independent evolutionary trajectory for CG15 and CG14 and how the acquisition of specific KL, quinolone-resistance determining region (QRDR) mutations (CG15), and ARGs in highly recombinant plasmids could have shaped the expansion and diversification of particular subclades (CG14-I and CG15-IIA/IIB). IMPORTANCE Klebsiella pneumoniae represents a major threat in the burden of antibiotic resistance (ABR). Available studies to explain the origin, the diversity, and the evolution of certain ABR K. pneumoniae populations have mainly been focused on a few clonal groups (CGs) using phylogenetic analysis of the core genome, the accessory genome being overlooked. Here, we provide unique insights into the phylogenetic evolution of CG14 and CG15, two poorly characterized CGs which have contributed to the global dissemination of genes responsible for resistance to first-line antibiotics such as β-lactams. Our results point out an independent evolution of these two CGs and highlight the existence of different subclades structured by the capsular type and the accessory genome. Moreover, the contribution of a turbulent flux of plasmids (especially multireplicon F type and Col) and adaptive traits (antibiotic resistance and metal tolerance genes) to the pangenome reflect the exposure and adaptation of K. pneumoniae under different selective pressures. |
| first_indexed | 2024-03-13T05:20:55Z |
| format | Article |
| id | doaj.art-19d7ca7401bd4b9ab8f7ccfc7a8d73c4 |
| institution | Directory Open Access Journal |
| issn | 2165-0497 |
| language | English |
| last_indexed | 2024-03-13T05:20:55Z |
| publishDate | 2023-06-01 |
| publisher | American Society for Microbiology |
| record_format | Article |
| series | Microbiology Spectrum |
| spelling | doaj.art-19d7ca7401bd4b9ab8f7ccfc7a8d73c42023-06-15T13:18:32ZengAmerican Society for MicrobiologyMicrobiology Spectrum2165-04972023-06-0111310.1128/spectrum.03395-22Phylogenomics of Globally Spread Clonal Groups 14 and 15 of Klebsiella pneumoniaeCarla Rodrigues0Val F. Lanza1Luísa Peixe2Teresa M. Coque3Ângela Novais4UCIBIO, Applied Molecular Biosciences Unit, Department of Biological Sciences, Laboratory of Microbiology, Faculty of Pharmacy, University of Porto, Porto, PortugalUnidad de Genómica Traslacional Hospital Universitario Ramón y Cajal (IRYCIS), Madrid, SpainUCIBIO, Applied Molecular Biosciences Unit, Department of Biological Sciences, Laboratory of Microbiology, Faculty of Pharmacy, University of Porto, Porto, PortugalCIBER en Enfermedades Infecciosas (CIBERINFEC), Madrid, SpainUCIBIO, Applied Molecular Biosciences Unit, Department of Biological Sciences, Laboratory of Microbiology, Faculty of Pharmacy, University of Porto, Porto, PortugalABSTRACT Klebsiella pneumoniae sequence type 14 (ST14) and ST15 caused outbreaks of CTX-M-15 and/or carbapenemase producers worldwide, but their phylogeny and global dynamics remain unclear. We clarified the evolution of K. pneumoniae clonal group 14 (CG14) and CG15 by analyzing the capsular locus (KL), resistome, virulome, and plasmidome of public genomes (n = 481) and de novo sequences (n = 9) representing main sublineages circulating in Portugal. CG14 and CG15 evolved independently within 6 main subclades defined according to the KL and the accessory genome. The CG14 (n = 65) clade was structured in two large monophyletic subclades, CG14-I (KL2, 86%) and CG14-II (KL16, 14%), whose emergences were dated to 1932 and 1911, respectively. Genes encoding extended-spectrum β-lactamase (ESBL), AmpC, and/or carbapenemases were mostly observed in CG14-I (71% versus 22%). CG15 clade (n = 170) was segregated into subclades CG15-IA (KL19/KL106, 9%), CG15-IB (variable KL types, 6%), CG15-IIA (KL24, 43%) and CG15-IIB (KL112, 37%). Most CG15 genomes carried specific GyrA and ParC mutations and emerged from a common ancestor in 1989. CTX-M-15 was especially prevalent in CG15 (68% CG15 versus 38% CG14) and in CG15-IIB (92%). Plasmidome analysis revealed 27 predominant plasmid groups (PG), including particularly pervasive and recombinant F-type (n = 10), Col (n = 10), and new plasmid types. While blaCTX-M-15 was acquired multiple times by a high diversity of F-type mosaic plasmids, other antibiotic resistance genes (ARGs) were dispersed by IncL (blaOXA-48) or IncC (blaCMY/TEM-24) plasmids. We first demonstrate an independent evolutionary trajectory for CG15 and CG14 and how the acquisition of specific KL, quinolone-resistance determining region (QRDR) mutations (CG15), and ARGs in highly recombinant plasmids could have shaped the expansion and diversification of particular subclades (CG14-I and CG15-IIA/IIB). IMPORTANCE Klebsiella pneumoniae represents a major threat in the burden of antibiotic resistance (ABR). Available studies to explain the origin, the diversity, and the evolution of certain ABR K. pneumoniae populations have mainly been focused on a few clonal groups (CGs) using phylogenetic analysis of the core genome, the accessory genome being overlooked. Here, we provide unique insights into the phylogenetic evolution of CG14 and CG15, two poorly characterized CGs which have contributed to the global dissemination of genes responsible for resistance to first-line antibiotics such as β-lactams. Our results point out an independent evolution of these two CGs and highlight the existence of different subclades structured by the capsular type and the accessory genome. Moreover, the contribution of a turbulent flux of plasmids (especially multireplicon F type and Col) and adaptive traits (antibiotic resistance and metal tolerance genes) to the pangenome reflect the exposure and adaptation of K. pneumoniae under different selective pressures.https://journals.asm.org/doi/10.1128/spectrum.03395-22IncF plasmidsaccessory genomeantimicrobial resistanceCol plasmidsgenomic epidemiologyhigh-risk clones |
| spellingShingle | Carla Rodrigues Val F. Lanza Luísa Peixe Teresa M. Coque Ângela Novais Phylogenomics of Globally Spread Clonal Groups 14 and 15 of Klebsiella pneumoniae Microbiology Spectrum IncF plasmids accessory genome antimicrobial resistance Col plasmids genomic epidemiology high-risk clones |
| title | Phylogenomics of Globally Spread Clonal Groups 14 and 15 of Klebsiella pneumoniae |
| title_full | Phylogenomics of Globally Spread Clonal Groups 14 and 15 of Klebsiella pneumoniae |
| title_fullStr | Phylogenomics of Globally Spread Clonal Groups 14 and 15 of Klebsiella pneumoniae |
| title_full_unstemmed | Phylogenomics of Globally Spread Clonal Groups 14 and 15 of Klebsiella pneumoniae |
| title_short | Phylogenomics of Globally Spread Clonal Groups 14 and 15 of Klebsiella pneumoniae |
| title_sort | phylogenomics of globally spread clonal groups 14 and 15 of klebsiella pneumoniae |
| topic | IncF plasmids accessory genome antimicrobial resistance Col plasmids genomic epidemiology high-risk clones |
| url | https://journals.asm.org/doi/10.1128/spectrum.03395-22 |
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