Improved molecular characterization of the Klebsiella oxytoca complex reveals the prevalence of the kleboxymycin biosynthetic gene cluster

Preetha Shibu; Frazer McCuaig; Anne L. McCartney; Magdalena Kujawska; Lindsay J. Hall; Lesley Hoyles

doi:10.1099/MGEN.0.000592

Improved molecular characterization of the Klebsiella oxytoca complex reveals the prevalence of the kleboxymycin biosynthetic gene cluster

Preetha Shibu, Frazer McCuaig, Anne L. McCartney, Magdalena Kujawska, Lindsay J. Hall, Lesley Hoyles^*

^*Corresponding author for this work

Microbiology and Infection

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Abstract

As part of the ongoing studies with clinically relevant Klebsiella spp., we characterized the genomes of three clinical GES-5-positive ST138 strains originally identified as Klebsiella oxytoca. bla_OXY gene, average nucleotide identity and phylogenetic analyses showed the strains to be Klebsiella michiganensis. Affiliation of the strains to ST138 led us to demonstrate that the current multi-locus sequence typing scheme for K. oxytoca can be used to distinguish members of this genetically diverse complex of bacteria. The strains encoded the kleboxymycin biosynthetic gene cluster (BGC), previously only found in K. oxytoca strains and one strain of Klebsiella grimontii. The finding of this BGC, associated with antibiotic-associated haemorrhagic colitis, in K. michiganensis led us to carry out a wide-ranging study to determine the prevalence of this BGC in Klebsiella spp. Of 7170 publicly available Klebsiella genome sequences screened, 88 encoded the kleboxymycin BGC. All BGC-positive strains belonged to the K. oxytoca complex, with strains of four (K. oxytoca, K. pasteurii, K. grimontii, K. michiganensis) of the six species of complex found to encode the complete BGC. In addition to being found in K. grimontii strains isolated from preterm infants, the BGC was found in K. oxytoca and K. michiganensis metagenome-assembled genomes recovered from neonates. Detection of the kleboxymycin BGC across the K. oxytoca complex may be of clinical relevance and this cluster should be included in databases characterizing virulence factors, in addition to those characterizing BGCs.

Original language	English
Article number	000592
Number of pages	11
Journal	Microbial Genomics
Volume	7
Issue number	6
DOIs	https://doi.org/10.1099/MGEN.0.000592
Publication status	Published - 18 Jun 2021

Bibliographical note

Funding Information:
Consultant microbiologist Dr Frances Davies (Imperial College Healthcare NHS Trust) is thanked for providing access to clinical strains. This work used the computing resources of CLIMB [33], the UK MEDical BIOinformatics partnership (UK Med-Bio, supported by Medical Research Council grant number MR/L01632X/1) and the Nottingham Trent University Hamilton High Performance Computing Cluster. We would like to thank Dave Baker and the QIB core sequencing team for WGS library preparation and sequencing.

Imperial Health Charity is thanked for contributing to registration fees for the Professional Doctorate studies of PS. LH was funded by UK Med-Bio (Medical Research Council grant number MR/L01632X/1). The research placement of FM was funded by Nottingham Trent University. LJH is funded by a Wellcome Trust Investigator Award (no. 100/974/C/13/Z); a BBSRC Norwich Research Park Bioscience Doctoral Training grant no. BB/M011216/1 (supervisor LJH, student MK); an Institute Strategic Programme Gut Microbes and Health grant no. BB/R012490/1 and its constituent projects BBS/E/F/000PR10353 and BBS/E/F/000PR10356; and an Institute Strategic Programme Gut Health and Food Safety grant no. BB/J004529/1 to LJH.

Publisher Copyright:
© 2021 The Authors.

Keywords

Antibiotic-associated haemorrhagic colitis
Klebsiella michiganensis
Necrotizing enterocolitis
Tilimycin
Tillivaline

ASJC Scopus subject areas

Epidemiology
Microbiology
Molecular Biology
Genetics

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ShibuP2021ImprovedFinal published version, 4.39 MBLicence: Creative Commons: Attribution (CC BY)

Cite this

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title = "Improved molecular characterization of the Klebsiella oxytoca complex reveals the prevalence of the kleboxymycin biosynthetic gene cluster",

abstract = "As part of the ongoing studies with clinically relevant Klebsiella spp., we characterized the genomes of three clinical GES-5-positive ST138 strains originally identified as Klebsiella oxytoca. blaOXY gene, average nucleotide identity and phylogenetic analyses showed the strains to be Klebsiella michiganensis. Affiliation of the strains to ST138 led us to demonstrate that the current multi-locus sequence typing scheme for K. oxytoca can be used to distinguish members of this genetically diverse complex of bacteria. The strains encoded the kleboxymycin biosynthetic gene cluster (BGC), previously only found in K. oxytoca strains and one strain of Klebsiella grimontii. The finding of this BGC, associated with antibiotic-associated haemorrhagic colitis, in K. michiganensis led us to carry out a wide-ranging study to determine the prevalence of this BGC in Klebsiella spp. Of 7170 publicly available Klebsiella genome sequences screened, 88 encoded the kleboxymycin BGC. All BGC-positive strains belonged to the K. oxytoca complex, with strains of four (K. oxytoca, K. pasteurii, K. grimontii, K. michiganensis) of the six species of complex found to encode the complete BGC. In addition to being found in K. grimontii strains isolated from preterm infants, the BGC was found in K. oxytoca and K. michiganensis metagenome-assembled genomes recovered from neonates. Detection of the kleboxymycin BGC across the K. oxytoca complex may be of clinical relevance and this cluster should be included in databases characterizing virulence factors, in addition to those characterizing BGCs.",

keywords = "Antibiotic-associated haemorrhagic colitis, Klebsiella michiganensis, Necrotizing enterocolitis, Tilimycin, Tillivaline",

author = "Preetha Shibu and Frazer McCuaig and McCartney, {Anne L.} and Magdalena Kujawska and Hall, {Lindsay J.} and Lesley Hoyles",

note = "Funding Information: Consultant microbiologist Dr Frances Davies (Imperial College Healthcare NHS Trust) is thanked for providing access to clinical strains. This work used the computing resources of CLIMB [33], the UK MEDical BIOinformatics partnership (UK Med-Bio, supported by Medical Research Council grant number MR/L01632X/1) and the Nottingham Trent University Hamilton High Performance Computing Cluster. We would like to thank Dave Baker and the QIB core sequencing team for WGS library preparation and sequencing. Imperial Health Charity is thanked for contributing to registration fees for the Professional Doctorate studies of PS. LH was funded by UK Med-Bio (Medical Research Council grant number MR/L01632X/1). The research placement of FM was funded by Nottingham Trent University. LJH is funded by a Wellcome Trust Investigator Award (no. 100/974/C/13/Z); a BBSRC Norwich Research Park Bioscience Doctoral Training grant no. BB/M011216/1 (supervisor LJH, student MK); an Institute Strategic Programme Gut Microbes and Health grant no. BB/R012490/1 and its constituent projects BBS/E/F/000PR10353 and BBS/E/F/000PR10356; and an Institute Strategic Programme Gut Health and Food Safety grant no. BB/J004529/1 to LJH. Publisher Copyright: {\textcopyright} 2021 The Authors.",

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AU - Hall, Lindsay J.

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N1 - Funding Information: Consultant microbiologist Dr Frances Davies (Imperial College Healthcare NHS Trust) is thanked for providing access to clinical strains. This work used the computing resources of CLIMB [33], the UK MEDical BIOinformatics partnership (UK Med-Bio, supported by Medical Research Council grant number MR/L01632X/1) and the Nottingham Trent University Hamilton High Performance Computing Cluster. We would like to thank Dave Baker and the QIB core sequencing team for WGS library preparation and sequencing. Imperial Health Charity is thanked for contributing to registration fees for the Professional Doctorate studies of PS. LH was funded by UK Med-Bio (Medical Research Council grant number MR/L01632X/1). The research placement of FM was funded by Nottingham Trent University. LJH is funded by a Wellcome Trust Investigator Award (no. 100/974/C/13/Z); a BBSRC Norwich Research Park Bioscience Doctoral Training grant no. BB/M011216/1 (supervisor LJH, student MK); an Institute Strategic Programme Gut Microbes and Health grant no. BB/R012490/1 and its constituent projects BBS/E/F/000PR10353 and BBS/E/F/000PR10356; and an Institute Strategic Programme Gut Health and Food Safety grant no. BB/J004529/1 to LJH. Publisher Copyright: © 2021 The Authors.

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N2 - As part of the ongoing studies with clinically relevant Klebsiella spp., we characterized the genomes of three clinical GES-5-positive ST138 strains originally identified as Klebsiella oxytoca. blaOXY gene, average nucleotide identity and phylogenetic analyses showed the strains to be Klebsiella michiganensis. Affiliation of the strains to ST138 led us to demonstrate that the current multi-locus sequence typing scheme for K. oxytoca can be used to distinguish members of this genetically diverse complex of bacteria. The strains encoded the kleboxymycin biosynthetic gene cluster (BGC), previously only found in K. oxytoca strains and one strain of Klebsiella grimontii. The finding of this BGC, associated with antibiotic-associated haemorrhagic colitis, in K. michiganensis led us to carry out a wide-ranging study to determine the prevalence of this BGC in Klebsiella spp. Of 7170 publicly available Klebsiella genome sequences screened, 88 encoded the kleboxymycin BGC. All BGC-positive strains belonged to the K. oxytoca complex, with strains of four (K. oxytoca, K. pasteurii, K. grimontii, K. michiganensis) of the six species of complex found to encode the complete BGC. In addition to being found in K. grimontii strains isolated from preterm infants, the BGC was found in K. oxytoca and K. michiganensis metagenome-assembled genomes recovered from neonates. Detection of the kleboxymycin BGC across the K. oxytoca complex may be of clinical relevance and this cluster should be included in databases characterizing virulence factors, in addition to those characterizing BGCs.

AB - As part of the ongoing studies with clinically relevant Klebsiella spp., we characterized the genomes of three clinical GES-5-positive ST138 strains originally identified as Klebsiella oxytoca. blaOXY gene, average nucleotide identity and phylogenetic analyses showed the strains to be Klebsiella michiganensis. Affiliation of the strains to ST138 led us to demonstrate that the current multi-locus sequence typing scheme for K. oxytoca can be used to distinguish members of this genetically diverse complex of bacteria. The strains encoded the kleboxymycin biosynthetic gene cluster (BGC), previously only found in K. oxytoca strains and one strain of Klebsiella grimontii. The finding of this BGC, associated with antibiotic-associated haemorrhagic colitis, in K. michiganensis led us to carry out a wide-ranging study to determine the prevalence of this BGC in Klebsiella spp. Of 7170 publicly available Klebsiella genome sequences screened, 88 encoded the kleboxymycin BGC. All BGC-positive strains belonged to the K. oxytoca complex, with strains of four (K. oxytoca, K. pasteurii, K. grimontii, K. michiganensis) of the six species of complex found to encode the complete BGC. In addition to being found in K. grimontii strains isolated from preterm infants, the BGC was found in K. oxytoca and K. michiganensis metagenome-assembled genomes recovered from neonates. Detection of the kleboxymycin BGC across the K. oxytoca complex may be of clinical relevance and this cluster should be included in databases characterizing virulence factors, in addition to those characterizing BGCs.

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KW - Necrotizing enterocolitis

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Improved molecular characterization of the Klebsiella oxytoca complex reveals the prevalence of the kleboxymycin biosynthetic gene cluster

Abstract

Bibliographical note

Keywords

ASJC Scopus subject areas

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