A large-scale genomic snapshot of Klebsiella spp. isolates in Northern Italy reveals limited transmission between clinical and non-clinical settings

Edward Feil; Ross Booton; Teemu Kallonen; Marjorie Gibbon; Natacha Monge Gomes Do Couto; Virginie Passet; Sebastian Fernandez; Carla Rodrigues; Louise Matthews; Sonia Mitchell; Richard Reeve; Sophia David; Cristina Merla; Marta Corbella; Carolina Ferrari; Francesco Comandatore; Piero Manone; Sylvain Brisse; Davide Sassera; Jukka Corander

doi:10.1038/s41564-022-01263-0

A large-scale genomic snapshot of Klebsiella spp. isolates in Northern Italy reveals limited transmission between clinical and non-clinical settings

Edward Feil, Ross Booton, Teemu Kallonen, Marjorie Gibbon, Natacha Monge Gomes Do Couto, Virginie Passet, Sebastian Fernandez, Carla Rodrigues, Louise Matthews, Sonia Mitchell, Richard Reeve, Sophia David, Cristina Merla, Marta Corbella, Carolina Ferrari, Francesco Comandatore, Piero Manone, Sylvain Brisse, Davide Sassera, Jukka Corander

Research output: Contribution to journal › Article › peer-review

59 Citations (SciVal)

Abstract

The Klebsiella group is genetically and ecologically diverse, being found in humans, livestock, plants, soil, water, and wild animals. Many species are opportunistic pathogens, and can harbour diverse classes of antimicrobial resistance (AMR) genes. Health-care associated Klebsiella pneumoniae clones that are non-susceptible to carbapenems can spread rapidly, representing a high public-health burden. Here we report an analysis of 3,482 genome sequences representing 15 Klebsiella species sampled over a 15-month period from a wide range of clinical, community, animal, and environmental settings in and around the Italian city of Pavia. Northern Italy is a hotspot for hospital-acquired Carbapenem non-susceptible Klebsiella, and thus a pertinent setting to examine the overlap between isolates in clinical and non-clinical settings. We find no genotypic or phenotypic evidence for non-susceptibility to carbapenems outside of the clinical environment. Although we note occasional transmission between clinical and non-clinical settings, our data point to a limited role of animal and environmental reservoirs in human acquisition of Klebsiella spp. We also provide a detailed genus-wide view of genomic diversity and population structure, including the identification of novel groups.

Original language	English
Pages (from-to)	2054-2067
Journal	Nature Microbiology
Volume	7
Early online date	21 Nov 2022
DOIs	https://doi.org/10.1038/s41564-022-01263-0
Publication status	Published - 31 Dec 2022

Bibliographical note

This work was funded by the SpARK project, awarded to EJF, 'The rates and routes of transmission of 584 multidrug resistant Klebsiella clones and genes into the clinic from environmental sources', which has 585 received funding under the 2016 JPI-AMR call 'Transmission Dynamics' (MRC reference 586 MR/R00241X/1); and by the French Government’s Investissement d’Avenir program Laboratoire 587 d’Excellence 'Integrative Biology of Emerging Infectious Diseases' (ANR-10-LABX-62-IBEID). JC and 588 HAT were funded by the ERC grant no. 742158. JC and TK were funded by the Norwegian Research 589 Council grant no. 271162. The use of MRC-CLIMB57 was critical for the computational aspects of this 590 work. We are grateful to Ruth Zadoks and Alan McNally for advice during the course of the project.

Funding

This work was funded by the SpARK project, awarded to E.J.F., ‘The rates and routes of transmission of multidrug-resistant Klebsiella clones and genes into the clinic from environmental sources’, which has received funding under the 2016 Joint Programming Initiative on Antimicrobial Resistance call ‘Transmission dynamics’ (medical research council (MRC) reference no. MR/R00241X/1) and by the French Government’s Investissement d’Avenir program Laboratoire d’Excellence ‘Integrative Biology of Emerging Infectious Diseases’ (no. ANR-10-LABX-62-IBEID). J.C. and H.A.T. were funded by the European Research Council grant no. 742158. J.C. and T.K. were funded by the Norwegian Research Council grant no. 271162. The use of the MRC Cloud Infrastructure for Microbial Bioinformatics was critical for the computational aspects of this work. We thank R. Zadoks and A. McNally for advice during the course of the project.

UN SDGs

This output contributes to the following UN Sustainable Development Goals (SDGs)

Access to Document

10.1038/s41564-022-01263-0Licence: CC BY

Embargoed Document

spark accepted.pdf
Accepted author manuscript, 9.74 MB
Licence: Unspecified
Embargo ends: 31/12/99
Request copy

SpARK - The Rates and Routes of Transmission of Multidrug Resistant Klebsiella Clones into the Clinic from Environmental Sources
Feil, E. (PI)
MRC
1/04/17 → 31/12/20
Project: Research council

Cite this

Feil, E., Booton, R., Kallonen, T., Gibbon, M., Monge Gomes Do Couto, N., Passet, V., Fernandez, S., Rodrigues, C., Matthews, L., Mitchell, S., Reeve, R., David, S., Merla, C., Corbella, M., Ferrari, C., Comandatore, F., Manone, P., Brisse, S., Sassera, D., & Corander, J. (2022). A large-scale genomic snapshot of Klebsiella spp. isolates in Northern Italy reveals limited transmission between clinical and non-clinical settings. Nature Microbiology, 7, 2054-2067. https://doi.org/10.1038/s41564-022-01263-0

Feil, E, Booton, R, Kallonen, T, Gibbon, M, Monge Gomes Do Couto, N, Passet, V, Fernandez, S, Rodrigues, C, Matthews, L, Mitchell, S, Reeve, R, David, S, Merla, C, Corbella, M, Ferrari, C, Comandatore, F, Manone, P, Brisse, S, Sassera, D & Corander, J 2022, 'A large-scale genomic snapshot of Klebsiella spp. isolates in Northern Italy reveals limited transmission between clinical and non-clinical settings', Nature Microbiology, vol. 7, pp. 2054-2067. https://doi.org/10.1038/s41564-022-01263-0

@article{657ffc001dda4df1a4a87bdc8096d7b3,

title = "A large-scale genomic snapshot of Klebsiella spp. isolates in Northern Italy reveals limited transmission between clinical and non-clinical settings",

abstract = "The Klebsiella group is genetically and ecologically diverse, being found in humans, livestock, plants, soil, water, and wild animals. Many species are opportunistic pathogens, and can harbour diverse classes of antimicrobial resistance (AMR) genes. Health-care associated Klebsiella pneumoniae clones that are non-susceptible to carbapenems can spread rapidly, representing a high public-health burden. Here we report an analysis of 3,482 genome sequences representing 15 Klebsiella species sampled over a 15-month period from a wide range of clinical, community, animal, and environmental settings in and around the Italian city of Pavia. Northern Italy is a hotspot for hospital-acquired Carbapenem non-susceptible Klebsiella, and thus a pertinent setting to examine the overlap between isolates in clinical and non-clinical settings. We find no genotypic or phenotypic evidence for non-susceptibility to carbapenems outside of the clinical environment. Although we note occasional transmission between clinical and non-clinical settings, our data point to a limited role of animal and environmental reservoirs in human acquisition of Klebsiella spp. We also provide a detailed genus-wide view of genomic diversity and population structure, including the identification of novel groups.",

author = "Edward Feil and Ross Booton and Teemu Kallonen and Marjorie Gibbon and {Monge Gomes Do Couto}, Natacha and Virginie Passet and Sebastian Fernandez and Carla Rodrigues and Louise Matthews and Sonia Mitchell and Richard Reeve and Sophia David and Cristina Merla and Marta Corbella and Carolina Ferrari and Francesco Comandatore and Piero Manone and Sylvain Brisse and Davide Sassera and Jukka Corander",

note = "This work was funded by the SpARK project, awarded to EJF, 'The rates and routes of transmission of 584 multidrug resistant Klebsiella clones and genes into the clinic from environmental sources', which has 585 received funding under the 2016 JPI-AMR call 'Transmission Dynamics' (MRC reference 586 MR/R00241X/1); and by the French Government{\textquoteright}s Investissement d{\textquoteright}Avenir program Laboratoire 587 d{\textquoteright}Excellence 'Integrative Biology of Emerging Infectious Diseases' (ANR-10-LABX-62-IBEID). JC and 588 HAT were funded by the ERC grant no. 742158. JC and TK were funded by the Norwegian Research 589 Council grant no. 271162. The use of MRC-CLIMB57 was critical for the computational aspects of this 590 work. We are grateful to Ruth Zadoks and Alan McNally for advice during the course of the project. ",

year = "2022",

month = dec,

day = "31",

doi = "10.1038/s41564-022-01263-0",

language = "English",

volume = "7",

pages = "2054--2067",

journal = "Nature Microbiology",

issn = "2058-5276",

publisher = "Nature Research",

}

TY - JOUR

T1 - A large-scale genomic snapshot of Klebsiella spp. isolates in Northern Italy reveals limited transmission between clinical and non-clinical settings

AU - Feil, Edward

AU - Booton, Ross

AU - Kallonen, Teemu

AU - Gibbon, Marjorie

AU - Monge Gomes Do Couto, Natacha

AU - Passet, Virginie

AU - Fernandez, Sebastian

AU - Rodrigues, Carla

AU - Matthews, Louise

AU - Mitchell, Sonia

AU - Reeve, Richard

AU - David, Sophia

AU - Merla, Cristina

AU - Corbella, Marta

AU - Ferrari, Carolina

AU - Comandatore, Francesco

AU - Manone, Piero

AU - Brisse, Sylvain

AU - Sassera, Davide

AU - Corander, Jukka

N1 - This work was funded by the SpARK project, awarded to EJF, 'The rates and routes of transmission of 584 multidrug resistant Klebsiella clones and genes into the clinic from environmental sources', which has 585 received funding under the 2016 JPI-AMR call 'Transmission Dynamics' (MRC reference 586 MR/R00241X/1); and by the French Government’s Investissement d’Avenir program Laboratoire 587 d’Excellence 'Integrative Biology of Emerging Infectious Diseases' (ANR-10-LABX-62-IBEID). JC and 588 HAT were funded by the ERC grant no. 742158. JC and TK were funded by the Norwegian Research 589 Council grant no. 271162. The use of MRC-CLIMB57 was critical for the computational aspects of this 590 work. We are grateful to Ruth Zadoks and Alan McNally for advice during the course of the project.

PY - 2022/12/31

Y1 - 2022/12/31

N2 - The Klebsiella group is genetically and ecologically diverse, being found in humans, livestock, plants, soil, water, and wild animals. Many species are opportunistic pathogens, and can harbour diverse classes of antimicrobial resistance (AMR) genes. Health-care associated Klebsiella pneumoniae clones that are non-susceptible to carbapenems can spread rapidly, representing a high public-health burden. Here we report an analysis of 3,482 genome sequences representing 15 Klebsiella species sampled over a 15-month period from a wide range of clinical, community, animal, and environmental settings in and around the Italian city of Pavia. Northern Italy is a hotspot for hospital-acquired Carbapenem non-susceptible Klebsiella, and thus a pertinent setting to examine the overlap between isolates in clinical and non-clinical settings. We find no genotypic or phenotypic evidence for non-susceptibility to carbapenems outside of the clinical environment. Although we note occasional transmission between clinical and non-clinical settings, our data point to a limited role of animal and environmental reservoirs in human acquisition of Klebsiella spp. We also provide a detailed genus-wide view of genomic diversity and population structure, including the identification of novel groups.

AB - The Klebsiella group is genetically and ecologically diverse, being found in humans, livestock, plants, soil, water, and wild animals. Many species are opportunistic pathogens, and can harbour diverse classes of antimicrobial resistance (AMR) genes. Health-care associated Klebsiella pneumoniae clones that are non-susceptible to carbapenems can spread rapidly, representing a high public-health burden. Here we report an analysis of 3,482 genome sequences representing 15 Klebsiella species sampled over a 15-month period from a wide range of clinical, community, animal, and environmental settings in and around the Italian city of Pavia. Northern Italy is a hotspot for hospital-acquired Carbapenem non-susceptible Klebsiella, and thus a pertinent setting to examine the overlap between isolates in clinical and non-clinical settings. We find no genotypic or phenotypic evidence for non-susceptibility to carbapenems outside of the clinical environment. Although we note occasional transmission between clinical and non-clinical settings, our data point to a limited role of animal and environmental reservoirs in human acquisition of Klebsiella spp. We also provide a detailed genus-wide view of genomic diversity and population structure, including the identification of novel groups.

U2 - 10.1038/s41564-022-01263-0

DO - 10.1038/s41564-022-01263-0

M3 - Article

SN - 2058-5276

VL - 7

SP - 2054

EP - 2067

JO - Nature Microbiology

JF - Nature Microbiology

ER -

A large-scale genomic snapshot of Klebsiella spp. isolates in Northern Italy reveals limited transmission between clinical and non-clinical settings

Abstract

Bibliographical note

Funding

UN SDGs

Access to Document

Embargoed Document

Fingerprint

Projects

SpARK - The Rates and Routes of Transmission of Multidrug Resistant Klebsiella Clones into the Clinic from Environmental Sources

Cite this