Evolution and host-specific adaptation of Pseudomonas aeruginosa

Aaron Weimann^{1

2

3

4}, Adam M Dinan^{1

2

3}, Christopher Ruis^{1

2

3

4}, Audrey Bernut⁵, Stéphane Pont⁵, Karen Brown^{1

2

6}, Judy Ryan^{1

2}, Lúcia Santos⁷, Louise Ellison², Emem Ukor^{2

6}, Arun P Pandurangan^{1

8

9}, Sina Krokowski^{1

2}, Tom L Blundell^{1

8

9}, Martin Welch⁸, Beth Blane⁹, Kim Judge¹⁰, Rachel Bousfield^{9

11}, Nicholas Brown¹¹, Josephine M Bryant¹⁰, Irena Kukavica-Ibrulj¹², Giordano Rampioni^{13

14}, Livia Leoni¹³, Patrick T Harrison⁷, Sharon J Peacock^{9

11}, Nicholas R Thomson^{10

15}, Jeff Gauthier¹², Jo L Fothergill¹⁶, Roger C Levesque¹², Julian Parkhill⁴, R Andres Floto^{1

2

3

6

9

11}

Affiliations

¹ Victor Phillip Dahdaleh Heart & Lung Research Institute, University of Cambridge, Cambridge, UK.
² University of Cambridge Molecular Immunity Unit, MRC Laboratory of Molecular Biology, Cambridge, UK.
³ Cambridge Centre for AI in Medicine, University of Cambridge, Cambridge, UK.
⁴ Department of Veterinary Medicine, University of Cambridge, Cambridge, UK.
⁵ Laboratory of Pathogens and Host Immunity (LPHI), UMR5235, CNRS/Université de Montpellier, Montpellier, France.
⁶ Cambridge Centre for Lung Infection, Royal Papworth Hospital, Cambridge, UK.
⁷ Department of Physiology, Bioscience Institute, University College Cork, Cork, Ireland.
⁸ Department of Biochemistry, University of Cambridge, Cambridge, UK.
⁹ Department of Medicine, University of Cambridge, Cambridge, UK.
¹⁰ Wellcome Sanger Institute, Hinxton, UK.
¹¹ Cambridge University Hospitals Trust, Cambridge, UK.
¹² Institut de Biologie Intégrative et des Systèmes (IBIS), Université Laval, Québec City, Québec, Canada.
¹³ Department of Science, University Roma Tre, Rome, Italy.
¹⁴ IRCCS Fondazione Santa Lucia, Rome, Italy.
¹⁵ London School of Hygiene and Tropical Medicine, London, UK.
¹⁶ Department of Clinical Infection, Microbiology and Immunology, University of Liverpool, Liverpool, UK.

PMID: 38963857
DOI: 10.1126/science.adi0908

Evolution and host-specific adaptation of Pseudomonas aeruginosa

Aaron Weimann et al. Science. 2024.

. 2024 Jul 5;385(6704):eadi0908.

doi: 10.1126/science.adi0908. Epub 2024 Jul 5.

Authors

Affiliations

¹ Victor Phillip Dahdaleh Heart & Lung Research Institute, University of Cambridge, Cambridge, UK.
² University of Cambridge Molecular Immunity Unit, MRC Laboratory of Molecular Biology, Cambridge, UK.
³ Cambridge Centre for AI in Medicine, University of Cambridge, Cambridge, UK.
⁴ Department of Veterinary Medicine, University of Cambridge, Cambridge, UK.
⁵ Laboratory of Pathogens and Host Immunity (LPHI), UMR5235, CNRS/Université de Montpellier, Montpellier, France.
⁶ Cambridge Centre for Lung Infection, Royal Papworth Hospital, Cambridge, UK.
⁷ Department of Physiology, Bioscience Institute, University College Cork, Cork, Ireland.
⁸ Department of Biochemistry, University of Cambridge, Cambridge, UK.
⁹ Department of Medicine, University of Cambridge, Cambridge, UK.
¹⁰ Wellcome Sanger Institute, Hinxton, UK.
¹¹ Cambridge University Hospitals Trust, Cambridge, UK.
¹² Institut de Biologie Intégrative et des Systèmes (IBIS), Université Laval, Québec City, Québec, Canada.
¹³ Department of Science, University Roma Tre, Rome, Italy.
¹⁴ IRCCS Fondazione Santa Lucia, Rome, Italy.
¹⁵ London School of Hygiene and Tropical Medicine, London, UK.
¹⁶ Department of Clinical Infection, Microbiology and Immunology, University of Liverpool, Liverpool, UK.

PMID: 38963857
DOI: 10.1126/science.adi0908

Abstract

The major human bacterial pathogen Pseudomonas aeruginosa causes multidrug-resistant infections in people with underlying immunodeficiencies or structural lung diseases such as cystic fibrosis (CF). We show that a few environmental isolates, driven by horizontal gene acquisition, have become dominant epidemic clones that have sequentially emerged and spread through global transmission networks over the past 200 years. These clones demonstrate varying intrinsic propensities for infecting CF or non-CF individuals (linked to specific transcriptional changes enabling survival within macrophages); have undergone multiple rounds of convergent, host-specific adaptation; and have eventually lost their ability to transmit between different patient groups. Our findings thus explain the pathogenic evolution of P. aeruginosa and highlight the importance of global surveillance and cross-infection prevention in averting the emergence of future epidemic clones.

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Evolution and host-specific adaptation of Pseudomonas aeruginosa

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Evolution and host-specific adaptation of Pseudomonas aeruginosa

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