Subtle genomic differences in Klebsiella pneumoniae sensu stricto isolates indicate host adaptation

Klebsiella pneumoniae sensu stricto (KpI) is an opportunistic pathogen capable of residing as a commensal in both human and bovine intestinal tracts and can cause serious systemic infections in humans and severe clinical mastitis in dairy cattle. It is unclear what role zoonotic and anthroponotic tr...

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Main Authors: Bridget O'Brien, Alla Yushchenko, Jinha Suh, Dongyun Jung, Zhangbin Cai, Ngoc Sang Nguyen, Makeda Semret, Simon Dufour, Séamus Fanning, Jennifer Ronholm
Format: Article
Language:English
Published: Elsevier 2025-06-01
Series:One Health
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Online Access:http://www.sciencedirect.com/science/article/pii/S2352771425000060
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author Bridget O'Brien
Alla Yushchenko
Jinha Suh
Dongyun Jung
Zhangbin Cai
Ngoc Sang Nguyen
Makeda Semret
Simon Dufour
Séamus Fanning
Jennifer Ronholm
author_facet Bridget O'Brien
Alla Yushchenko
Jinha Suh
Dongyun Jung
Zhangbin Cai
Ngoc Sang Nguyen
Makeda Semret
Simon Dufour
Séamus Fanning
Jennifer Ronholm
author_sort Bridget O'Brien
collection DOAJ
description Klebsiella pneumoniae sensu stricto (KpI) is an opportunistic pathogen capable of residing as a commensal in both human and bovine intestinal tracts and can cause serious systemic infections in humans and severe clinical mastitis in dairy cattle. It is unclear what role zoonotic and anthroponotic transmission play in the dissemination of KpI. In this study, we use a comparative genomic approach to identify differences between KpI associated with disease in humans and cattle and aimed to identify any potential genetic barriers limiting transmission of KpI between these two hosts. A total of 128 KpI strains (bovine n = 65; human n = 63) were whole genome sequenced and human and bovine strains were compared based on phylogenomics, the pangenome, mobile genetic elements, and differential gene abundance. No obvious phylogenomic differentiation was observed between isolates from these hosts. However, subtle genetic differences exist between bovine and human KpI which likely reflect environmental adaptation to different host niches, including a higher representation of gene clusters encoding ferric citrate uptake transporters, as well as histidine, arginine, and lactose utilization pathways in bovine isolates. These gene clusters may be positively selected due to the unique metabolic environment of the mammary gland, where lactose, citrate-bound iron, and amino acids like histidine and arginine provide growth advantages for KpI during mastitis. Overall, our study identified no obvious genetic barriers to zoonotic transmission of KpI within the dairy environment and provides insight into the development of host-specific therapeutic options for KpI infections in humans and bovine.
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spelling doaj-art-7d18b890ac7d48d79ff7859a77f346a72025-01-18T05:04:48ZengElsevierOne Health2352-77142025-06-0120100970Subtle genomic differences in Klebsiella pneumoniae sensu stricto isolates indicate host adaptationBridget O'Brien0Alla Yushchenko1Jinha Suh2Dongyun Jung3Zhangbin Cai4Ngoc Sang Nguyen5Makeda Semret6Simon Dufour7Séamus Fanning8Jennifer Ronholm9Faculty of Agricultural and Environmental Sciences, Macdonald Campus, McGill University, Montreal, Quebec, CanadaFaculty of Agricultural and Environmental Sciences, Macdonald Campus, McGill University, Montreal, Quebec, CanadaFaculty of Agricultural and Environmental Sciences, Macdonald Campus, McGill University, Montreal, Quebec, CanadaFaculty of Agricultural and Environmental Sciences, Macdonald Campus, McGill University, Montreal, Quebec, Canada; Mastitis Network, Saint-Hyacinthe, Quebec, Canada; Regroupement FRQNT Op+Lait, Saint-Hyacinthe, Quebec, CanadaFaculty of Agricultural and Environmental Sciences, Macdonald Campus, McGill University, Montreal, Quebec, CanadaFaculty of Agricultural and Environmental Sciences, Macdonald Campus, McGill University, Montreal, Quebec, CanadaMcGill University Health Centre (Infectious Diseases and Medical Microbiology), Montreal, Quebec, CanadaMastitis Network, Saint-Hyacinthe, Quebec, Canada; Faculté de Médecine Vétérinaire, Université de Montréal, Saint-Hyacinthe, Quebec, Canada; Regroupement FRQNT Op+Lait, Saint-Hyacinthe, Quebec, CanadaUCD-Centre for Food Safety, Science Centre South, University College Dublin, Dublin, Ireland; Institute for Global Food Security, School of Biological Sciences, Queen's University Belfast, 19 Chlorine Gardens, Belfast BT9 5DL, IrelandFaculty of Agricultural and Environmental Sciences, Macdonald Campus, McGill University, Montreal, Quebec, Canada; Mastitis Network, Saint-Hyacinthe, Quebec, Canada; Regroupement FRQNT Op+Lait, Saint-Hyacinthe, Quebec, Canada; Corresponding author at: Faculty of Agricultural and Environmental Sciences, Macdonald Campus, McGill University, Montreal, Quebec, Canada.Klebsiella pneumoniae sensu stricto (KpI) is an opportunistic pathogen capable of residing as a commensal in both human and bovine intestinal tracts and can cause serious systemic infections in humans and severe clinical mastitis in dairy cattle. It is unclear what role zoonotic and anthroponotic transmission play in the dissemination of KpI. In this study, we use a comparative genomic approach to identify differences between KpI associated with disease in humans and cattle and aimed to identify any potential genetic barriers limiting transmission of KpI between these two hosts. A total of 128 KpI strains (bovine n = 65; human n = 63) were whole genome sequenced and human and bovine strains were compared based on phylogenomics, the pangenome, mobile genetic elements, and differential gene abundance. No obvious phylogenomic differentiation was observed between isolates from these hosts. However, subtle genetic differences exist between bovine and human KpI which likely reflect environmental adaptation to different host niches, including a higher representation of gene clusters encoding ferric citrate uptake transporters, as well as histidine, arginine, and lactose utilization pathways in bovine isolates. These gene clusters may be positively selected due to the unique metabolic environment of the mammary gland, where lactose, citrate-bound iron, and amino acids like histidine and arginine provide growth advantages for KpI during mastitis. Overall, our study identified no obvious genetic barriers to zoonotic transmission of KpI within the dairy environment and provides insight into the development of host-specific therapeutic options for KpI infections in humans and bovine.http://www.sciencedirect.com/science/article/pii/S2352771425000060Klebsiella pneumoniae sensu strictoComparative genomicsOpportunistic pathogenMastitis
spellingShingle Bridget O'Brien
Alla Yushchenko
Jinha Suh
Dongyun Jung
Zhangbin Cai
Ngoc Sang Nguyen
Makeda Semret
Simon Dufour
Séamus Fanning
Jennifer Ronholm
Subtle genomic differences in Klebsiella pneumoniae sensu stricto isolates indicate host adaptation
One Health
Klebsiella pneumoniae sensu stricto
Comparative genomics
Opportunistic pathogen
Mastitis
title Subtle genomic differences in Klebsiella pneumoniae sensu stricto isolates indicate host adaptation
title_full Subtle genomic differences in Klebsiella pneumoniae sensu stricto isolates indicate host adaptation
title_fullStr Subtle genomic differences in Klebsiella pneumoniae sensu stricto isolates indicate host adaptation
title_full_unstemmed Subtle genomic differences in Klebsiella pneumoniae sensu stricto isolates indicate host adaptation
title_short Subtle genomic differences in Klebsiella pneumoniae sensu stricto isolates indicate host adaptation
title_sort subtle genomic differences in klebsiella pneumoniae sensu stricto isolates indicate host adaptation
topic Klebsiella pneumoniae sensu stricto
Comparative genomics
Opportunistic pathogen
Mastitis
url http://www.sciencedirect.com/science/article/pii/S2352771425000060
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