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A Dual Barcoding Approach to Bacterial Strain Nomenclature: Genomic Taxonomy of Klebsiella pneumoniae Strains.

ABSTRACT: Sublineages (SLs) within microbial species can differ widely in their ecology and pathogenicity, and their precise definition is important in basic research and for industrial or public health applications. Widely accepted strategies to define SLs are currently missing, which confuses communication in population biology and epidemiological surveillance. Here, we propose a broadly applicable genomic classification and nomenclature approach for bacterial strains, using the prominent public health threat Klebsiella pneumoniae as a model. Based on a 629-gene core genome multilocus sequence typing (cgMLST) scheme, we devised a dual barcoding system that combines multilevel single linkage (MLSL) clustering and life identification numbers (LINs). Phylogenetic and clustering analyses of >7,000 genome sequences captured population structure discontinuities, which were used to guide the definition of 10 infraspecific genetic dissimilarity thresholds. The widely used 7-gene multilocus sequence typing (MLST) nomenclature was mapped onto MLSL SLs (threshold: 190 allelic mismatches) and clonal group (threshold: 43) identifiers for backwards nomenclature compatibility. The taxonomy is publicly accessible through a community-curated platform (https://bigsdb.pasteur.fr/klebsiella), which also enables external users' genomic sequences identification. The proposed strain taxonomy combines two phylogenetically informative barcode systems that provide full stability (LIN codes) and nomenclatural continuity with previous nomenclature (MLSL). This species-specific dual barcoding strategy for the genomic taxonomy of microbial strains is broadly applicable and should contribute to unify global and cross-sector collaborative knowledge on the emergence and microevolution of bacterial pathogens.

SUBMITTER: Hennart M

PROVIDER: S-EPMC9254007 | biostudies-literature | 2022 Jul

REPOSITORIES: biostudies-literature

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A Dual Barcoding Approach to Bacterial Strain Nomenclature: Genomic Taxonomy of Klebsiella pneumoniae Strains.

Hennart Melanie M Guglielmini Julien J Bridel Sébastien S Maiden Martin C J MCJ Jolley Keith A KA Criscuolo Alexis A Brisse Sylvain S

Molecular biology and evolution 20220701 7

Sublineages (SLs) within microbial species can differ widely in their ecology and pathogenicity, and their precise definition is important in basic research and for industrial or public health applications. Widely accepted strategies to define SLs are currently missing, which confuses communication in population biology and epidemiological surveillance. Here, we propose a broadly applicable genomic classification and nomenclature approach for bacterial strains, using the prominent public health ...[more]

PMID: 35700230

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Project description:ObjectivesGenomic surveillance of Klebsiella pneumoniae carbapenemase-producing Klebsiella pneumoniae (KPC-Kp) is crucial for virulence, drug-resistance monitoring, and outbreak containment.MethodsGenomic analysis on 87 KPC-Kp strains isolated from 3 Northern Italy hospitals in 2019-2021 was performed by whole genome sequencing (WGS), to characterize resistome, virulome, and mobilome, and to assess potential associations with phenotype resistance and clinical presentation. Maximum Likelihood and Minimum Spanning Trees were used to determine strain correlations and identify potential transmission clusters.ResultsOverall, 15 different STs were found; the predominant ones included ST307 (35, 40.2%), ST512/1519 (15, 17.2%), ST20 (12, 13.8%), and ST101 (7, 8.1%). 33 (37.9%) KPC-Kp strains were noticed to be in five transmission clusters (median number of isolates in each cluster: 5 [3-10]), four of them characterized by intra-hospital transmission. All 87 strains harbored Tn4401a transposon, carrying blaKPC-3 (48, 55.2%), blaKPC-2 (38, 43.7%), and in one case (1.2%) blaKPC-33, the latter gene conferred resistance to ceftazidime/avibactam (CZA). Thirty strains (34.5%) harbored porin mutations; of them, 7 (8.1%) carried multiple Tn4401a copies. These strains were characterized by significantly higher CZA minimum inhibitory concentration compared with strains with no porin mutations or single Tn4401a copy, respectively, even if they did not overcome the resistance breakpoint of 8 ug/mL. Median 2 (IQR:1-2) virulence factors per strain were detected. The lowest number was observed in ST20 compared to the other STs (p<0.001). While ST307 was associated with infection events, a trend associated with colonization events could be observed for ST20.ConclusionsIntegration of genomic, resistance score, and clinical data allowed us to define a relative diversification of KPC-Kp in Northern Italy between 2019 and 2021, characterized by few large transmission chains and rare inter-hospital transmission. Our results also provided initial evidence of correlation between KPC-Kp genomic signatures and higher MIC levels to some antimicrobial agents or colonization/infection status, once again underlining WGS's importance in bacterial surveillance.

Project description:This study aimed to explore the relationship between wild birds and the transmission of multidrug-resistant strains. Klebsiella pneumoniae was isolated from fresh feces of captured wild birds and assessed by the broth microdilution method and comparative genomics. Four Klebsiella pneumoniae isolates showed different resistance phenotypes; S90-2 and S141 were both resistant to ampicillin, cefuroxime, and cefazolin, while M911-1 and S130-1 were sensitive to most of the 14 antibiotics tested. S90-2 belongs to sequence type 629 (ST629), and its genome includes 30 resistance genes, including blaCTX-M-14 and blaSHV-11, while its plasmid pS90-2.3 (IncR) carries qacEdelta1, sul1, and aph(3')-Ib. S141 belongs to ST1662, and its genome includes a total of 27 resistance genes, including blaSHV-217. M911-1 is a new ST, carrying blaSHV-1 and fosA6, and its plasmid pM911-1.1 (novel) carries qnrS1, blaLAP-2, and tet(A). S130-1 belongs to ST3753, carrying blaSHV-11 and fosA6, and its plasmid pS130-1 [IncFIB(K)] carries only one resistance gene, tet(A). pM911-1.1 and pS90-2.3 do not have conjugative transfer ability, but their resistance gene fragments are derived from multiple homologous Enterobacteriaceae strain chromosomes or plasmids, and the formation of resistance gene fragments (multidrug resistance region) involves interactions between multiple mobile element genes, resulting in a complex and diverse resistance plasmid structure. The homologous plasmids related to pM911-1.1 and pS90-2.3 were mainly from isolated human-infecting bacteria in China, namely, K. pneumoniae and Escherichia coli. The multidrug-resistant K. pneumoniae isolates carried by wild birds in this study had drug resistance phenotypes conferred primarily by multidrug resistance plasmids that were closely related to human-infecting bacteria. IMPORTANCE Little is known about the pathogenic microorganisms carried by wild animals. This study found that the multidrug resistance phenotype of Klebsiella pneumoniae isolates carried by wild birds was mainly attributed to multidrug resistance plasmids, and these multidrug resistance plasmids from wild birds were closely related to human-infecting bacteria. Wild bird habitats overlap to a great extent with human and livestock habitats, which further increases the potential for horizontal transfer of multidrug-resistant bacteria among humans, animals, and the environment. Therefore, wild birds, as potential transmission hosts of multidrug-resistant bacteria, should be given attention and monitored.

Project description:UNLABELLED:Carbapenem-resistant Enterobacteriaceae (CRE), especially Klebsiella pneumoniae carbapenemase (KPC)-producing K. pneumoniae, pose an urgent threat in health facilities in the United States and worldwide. K. pneumoniae isolates classified as sequence type 258 (ST258) by multilocus sequence typing are largely responsible for the global spread of KPC. A recent comparative genome study revealed that ST258 K. pneumoniae strains are two distinct genetic clades; however, the molecular origin of ST258 largely remains unknown, and our understanding of the evolution of the two genetic clades is incomplete. Here we compared the genetic structures and single-nucleotide polymorphism (SNP) distributions in the core genomes of strains from two ST258 clades and other STs (ST11, ST442, and ST42). We identified an ~1.1-Mbp region on ST258 genomes that is homogeneous to that of ST442, while the rest of the ST258 genome resembles that of ST11. Our results suggest ST258 is a hybrid clone--80% of the genome originated from ST11-like strains and 20% from ST442-like strains. Meanwhile, we sequenced an ST42 strain that carries the same K-antigen-encoding capsule polysaccharide biosynthesis gene (cps) region as ST258 clade I strains. Comparison of the cps-harboring regions between the ST42 and ST258 strains (clades I and II) suggests the ST258 clade I strains evolved from a clade II strain as a result of cps region replacement. Our findings unravel the molecular evolution history of ST258 strains, an important first step toward the development of diagnostic, therapeutic, and vaccine strategies to combat infections caused by multidrug-resistant K. pneumoniae. IMPORTANCE:Recombination events and replacement of chromosomal regions have been documented in various bacteria, and these events have given rise to successful pathogenic clones. Here we used comparative genomic analyses to discover that the ST258 K. pneumoniae genome is a hybrid--80% of the chromosome is homologous to ST11 strains, while the remaining 20% is homologous to that of ST442. Meanwhile, a recent study indicated that ST258 strains can be segregated into two ST258 clades, with distinct capsule polysaccharide gene (cps) regions. Our analysis suggests ST258 clade I strains evolved from clade II through homologous recombination of cps region. Horizontal transfer of the cps region appears to be a key element driving the molecular diversification in K. pneumoniae strains. These findings not only extend our understanding of the molecular evolution of ST258 but are an important step toward the development of effective control and treatment strategies for multidrug-resistant K. pneumoniae.

Dataset Information

A Dual Barcoding Approach to Bacterial Strain Nomenclature: Genomic Taxonomy of Klebsiella pneumoniae Strains.

Publications

A Dual Barcoding Approach to Bacterial Strain Nomenclature: Genomic Taxonomy of Klebsiella pneumoniae Strains.

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