Whole-Genome Sequencing of Human Clinical <named-content content-type="genus-species">Klebsiella pneumoniae</named-content> Isolates Reveals Misidentification and Misunderstandings of <named-content content-type="genus-species">Klebsiella pneumoniae</named-content>, <named-content content-type="genus-species">Klebsiella variicola</named-content>, and <named-content content-type="genus-species">Klebsiella quasipneumoniae</named-content>
ABSTRACT Klebsiella pneumoniae is a major threat to public health, causing significant morbidity and mortality worldwide. The emergence of highly drug-resistant strains is particularly concerning. There has been a recognition and division of Klebsiella pneumoniae into three distinct phylogenetic gro...
| Main Authors: | , , , , , , |
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| Format: | Article |
| Language: | English |
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American Society for Microbiology
2017-08-01
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| Series: | mSphere |
| Subjects: | |
| Online Access: | https://journals.asm.org/doi/10.1128/mSphereDirect.00290-17 |
| _version_ | 1818824734043799552 |
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| author | S. Wesley Long Sarah E. Linson Matthew Ojeda Saavedra Concepcion Cantu James J. Davis Thomas Brettin Randall J. Olsen |
| author_facet | S. Wesley Long Sarah E. Linson Matthew Ojeda Saavedra Concepcion Cantu James J. Davis Thomas Brettin Randall J. Olsen |
| author_sort | S. Wesley Long |
| collection | DOAJ |
| description | ABSTRACT Klebsiella pneumoniae is a major threat to public health, causing significant morbidity and mortality worldwide. The emergence of highly drug-resistant strains is particularly concerning. There has been a recognition and division of Klebsiella pneumoniae into three distinct phylogenetic groups: Klebsiella pneumoniae, Klebsiella variicola, and Klebsiella quasipneumoniae. K. variicola and K. quasipneumoniae have often been described as opportunistic pathogens that have less virulence in humans than K. pneumoniae does. We recently sequenced the genomes of 1,777 extended-spectrum-beta-lactamase (ESBL)-producing K. pneumoniae isolates recovered from human infections and discovered that 28 strains were phylogenetically related to K. variicola and K. quasipneumoniae. Whole-genome sequencing of 95 additional non-ESBL-producing K. pneumoniae isolates recovered from patients found 12 K. quasipneumoniae strains. Matrix-assisted laser desorption ionization–time of flight mass spectrometry (MALDI-TOF MS) analysis initially identified all patient isolates as K. pneumoniae, suggesting a potential pitfall in conventional clinical microbiology laboratory identification methods. Whole-genome sequence analysis revealed extensive sharing of core gene content and plasmid replicons among the Klebsiella species. For the first time, strains of both K. variicola and K. quasipneumoniae were found to carry the Klebsiella pneumoniae carbapenemase (KPC) gene, while another K. variicola strain was found to carry the New Delhi metallo-beta-lactamase 1 (NDM-1) gene. K. variicola and K. quasipneumoniae infections were not less virulent than K. pneumoniae infections, as assessed by in-hospital mortality and infection type. We also discovered evidence of homologous recombination in one K. variicola strain, as well as one strain from a novel Klebsiella species, which challenge the current understanding of interrelationships between clades of Klebsiella. IMPORTANCE Klebsiella pneumoniae is a serious human pathogen associated with resistance to multiple antibiotics and high mortality. K. variicola and K. quasipneumoniae are closely related organisms that are generally considered to be less-virulent opportunistic pathogens. We used a large, comprehensive, population-based strain collection and whole-genome sequencing to investigate infections caused by these organisms in our hospital system. We discovered that K. variicola and K. quasipneumoniae isolates are often misidentified as K. pneumoniae by routine clinical microbiology diagnostics and frequently cause severe life-threatening infections similar to K. pneumoniae. The presence of KPC in K. variicola and K. quasipneumoniae strains as well as NDM-1 metallo-beta-lactamase in one K. variicola strain is particularly concerning because these genes confer resistance to many different beta-lactam antibiotics. The sharing of plasmids, as well as evidence of homologous recombination, between these three species of Klebsiella is cause for additional concern. |
| first_indexed | 2024-12-19T00:00:34Z |
| format | Article |
| id | doaj.art-1d579fe04fe24e87aff8cf609a60c689 |
| institution | Directory Open Access Journal |
| issn | 2379-5042 |
| language | English |
| last_indexed | 2024-12-19T00:00:34Z |
| publishDate | 2017-08-01 |
| publisher | American Society for Microbiology |
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| series | mSphere |
| spelling | doaj.art-1d579fe04fe24e87aff8cf609a60c6892022-12-21T20:46:29ZengAmerican Society for MicrobiologymSphere2379-50422017-08-012410.1128/mSphereDirect.00290-17Whole-Genome Sequencing of Human Clinical <named-content content-type="genus-species">Klebsiella pneumoniae</named-content> Isolates Reveals Misidentification and Misunderstandings of <named-content content-type="genus-species">Klebsiella pneumoniae</named-content>, <named-content content-type="genus-species">Klebsiella variicola</named-content>, and <named-content content-type="genus-species">Klebsiella quasipneumoniae</named-content>S. Wesley Long0Sarah E. Linson1Matthew Ojeda Saavedra2Concepcion Cantu3James J. Davis4Thomas Brettin5Randall J. Olsen6Center for Molecular and Translational Human Infectious Diseases Research, Department of Pathology and Genomic Medicine, Houston Methodist Research Institute and Houston Methodist Hospital, Houston, Texas, USACenter for Molecular and Translational Human Infectious Diseases Research, Department of Pathology and Genomic Medicine, Houston Methodist Research Institute and Houston Methodist Hospital, Houston, Texas, USACenter for Molecular and Translational Human Infectious Diseases Research, Department of Pathology and Genomic Medicine, Houston Methodist Research Institute and Houston Methodist Hospital, Houston, Texas, USACenter for Molecular and Translational Human Infectious Diseases Research, Department of Pathology and Genomic Medicine, Houston Methodist Research Institute and Houston Methodist Hospital, Houston, Texas, USAComputing, Environment and Life Sciences, Argonne National Laboratory, Argonne, Illinois, USAComputing, Environment and Life Sciences, Argonne National Laboratory, Argonne, Illinois, USACenter for Molecular and Translational Human Infectious Diseases Research, Department of Pathology and Genomic Medicine, Houston Methodist Research Institute and Houston Methodist Hospital, Houston, Texas, USAABSTRACT Klebsiella pneumoniae is a major threat to public health, causing significant morbidity and mortality worldwide. The emergence of highly drug-resistant strains is particularly concerning. There has been a recognition and division of Klebsiella pneumoniae into three distinct phylogenetic groups: Klebsiella pneumoniae, Klebsiella variicola, and Klebsiella quasipneumoniae. K. variicola and K. quasipneumoniae have often been described as opportunistic pathogens that have less virulence in humans than K. pneumoniae does. We recently sequenced the genomes of 1,777 extended-spectrum-beta-lactamase (ESBL)-producing K. pneumoniae isolates recovered from human infections and discovered that 28 strains were phylogenetically related to K. variicola and K. quasipneumoniae. Whole-genome sequencing of 95 additional non-ESBL-producing K. pneumoniae isolates recovered from patients found 12 K. quasipneumoniae strains. Matrix-assisted laser desorption ionization–time of flight mass spectrometry (MALDI-TOF MS) analysis initially identified all patient isolates as K. pneumoniae, suggesting a potential pitfall in conventional clinical microbiology laboratory identification methods. Whole-genome sequence analysis revealed extensive sharing of core gene content and plasmid replicons among the Klebsiella species. For the first time, strains of both K. variicola and K. quasipneumoniae were found to carry the Klebsiella pneumoniae carbapenemase (KPC) gene, while another K. variicola strain was found to carry the New Delhi metallo-beta-lactamase 1 (NDM-1) gene. K. variicola and K. quasipneumoniae infections were not less virulent than K. pneumoniae infections, as assessed by in-hospital mortality and infection type. We also discovered evidence of homologous recombination in one K. variicola strain, as well as one strain from a novel Klebsiella species, which challenge the current understanding of interrelationships between clades of Klebsiella. IMPORTANCE Klebsiella pneumoniae is a serious human pathogen associated with resistance to multiple antibiotics and high mortality. K. variicola and K. quasipneumoniae are closely related organisms that are generally considered to be less-virulent opportunistic pathogens. We used a large, comprehensive, population-based strain collection and whole-genome sequencing to investigate infections caused by these organisms in our hospital system. We discovered that K. variicola and K. quasipneumoniae isolates are often misidentified as K. pneumoniae by routine clinical microbiology diagnostics and frequently cause severe life-threatening infections similar to K. pneumoniae. The presence of KPC in K. variicola and K. quasipneumoniae strains as well as NDM-1 metallo-beta-lactamase in one K. variicola strain is particularly concerning because these genes confer resistance to many different beta-lactam antibiotics. The sharing of plasmids, as well as evidence of homologous recombination, between these three species of Klebsiella is cause for additional concern.https://journals.asm.org/doi/10.1128/mSphereDirect.00290-17clinical microbiologyKPCKlebsiella pneumoniaeKlebsiella quasipneumoniaeKlebsiella variicolaMALDI |
| spellingShingle | S. Wesley Long Sarah E. Linson Matthew Ojeda Saavedra Concepcion Cantu James J. Davis Thomas Brettin Randall J. Olsen Whole-Genome Sequencing of Human Clinical <named-content content-type="genus-species">Klebsiella pneumoniae</named-content> Isolates Reveals Misidentification and Misunderstandings of <named-content content-type="genus-species">Klebsiella pneumoniae</named-content>, <named-content content-type="genus-species">Klebsiella variicola</named-content>, and <named-content content-type="genus-species">Klebsiella quasipneumoniae</named-content> mSphere clinical microbiology KPC Klebsiella pneumoniae Klebsiella quasipneumoniae Klebsiella variicola MALDI |
| title | Whole-Genome Sequencing of Human Clinical <named-content content-type="genus-species">Klebsiella pneumoniae</named-content> Isolates Reveals Misidentification and Misunderstandings of <named-content content-type="genus-species">Klebsiella pneumoniae</named-content>, <named-content content-type="genus-species">Klebsiella variicola</named-content>, and <named-content content-type="genus-species">Klebsiella quasipneumoniae</named-content> |
| title_full | Whole-Genome Sequencing of Human Clinical <named-content content-type="genus-species">Klebsiella pneumoniae</named-content> Isolates Reveals Misidentification and Misunderstandings of <named-content content-type="genus-species">Klebsiella pneumoniae</named-content>, <named-content content-type="genus-species">Klebsiella variicola</named-content>, and <named-content content-type="genus-species">Klebsiella quasipneumoniae</named-content> |
| title_fullStr | Whole-Genome Sequencing of Human Clinical <named-content content-type="genus-species">Klebsiella pneumoniae</named-content> Isolates Reveals Misidentification and Misunderstandings of <named-content content-type="genus-species">Klebsiella pneumoniae</named-content>, <named-content content-type="genus-species">Klebsiella variicola</named-content>, and <named-content content-type="genus-species">Klebsiella quasipneumoniae</named-content> |
| title_full_unstemmed | Whole-Genome Sequencing of Human Clinical <named-content content-type="genus-species">Klebsiella pneumoniae</named-content> Isolates Reveals Misidentification and Misunderstandings of <named-content content-type="genus-species">Klebsiella pneumoniae</named-content>, <named-content content-type="genus-species">Klebsiella variicola</named-content>, and <named-content content-type="genus-species">Klebsiella quasipneumoniae</named-content> |
| title_short | Whole-Genome Sequencing of Human Clinical <named-content content-type="genus-species">Klebsiella pneumoniae</named-content> Isolates Reveals Misidentification and Misunderstandings of <named-content content-type="genus-species">Klebsiella pneumoniae</named-content>, <named-content content-type="genus-species">Klebsiella variicola</named-content>, and <named-content content-type="genus-species">Klebsiella quasipneumoniae</named-content> |
| title_sort | whole genome sequencing of human clinical named content content type genus species klebsiella pneumoniae named content isolates reveals misidentification and misunderstandings of named content content type genus species klebsiella pneumoniae named content named content content type genus species klebsiella variicola named content and named content content type genus species klebsiella quasipneumoniae named content |
| topic | clinical microbiology KPC Klebsiella pneumoniae Klebsiella quasipneumoniae Klebsiella variicola MALDI |
| url | https://journals.asm.org/doi/10.1128/mSphereDirect.00290-17 |
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