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Core and accessory genomic traits of Vibrio cholerae O1 drive lineage transmission and disease severity

Author

Listed:
  • Alexandre Maciel-Guerra

    (University of Nottingham, College Road, Sutton Bonington)

  • Kubra Babaarslan

    (University of Nottingham, College Road, Sutton Bonington)

  • Michelle Baker

    (University of Nottingham, College Road, Sutton Bonington)

  • Aura Rahman

    (NSU Genome Research Institute (NGRI), North South University)

  • Maqsud Hossain

    (University of Nottingham, College Road, Sutton Bonington
    NSU Genome Research Institute (NGRI), North South University)

  • Abdus Sadique

    (NSU Genome Research Institute (NGRI), North South University)

  • Jahidul Alam

    (NSU Genome Research Institute (NGRI), North South University)

  • Salim Uzzaman

    (Disease Control and Research (IEDCR))

  • Mohammad Ferdous Rahman Sarker

    (Disease Control and Research (IEDCR))

  • Nasrin Sultana

    (Disease Control and Research (IEDCR))

  • Ashraful Islam Khan

    (International Centre for Diarrhoeal Disease Research, Bangladesh (icddr, b))

  • Yasmin Ara Begum

    (International Centre for Diarrhoeal Disease Research, Bangladesh (icddr, b))

  • Mokibul Hassan Afrad

    (International Centre for Diarrhoeal Disease Research, Bangladesh (icddr, b))

  • Nicola Senin

    (University of Perugia)

  • Zakir Hossain Habib

    (Disease Control and Research (IEDCR))

  • Tahmina Shirin

    (Disease Control and Research (IEDCR))

  • Firdausi Qadri

    (International Centre for Diarrhoeal Disease Research, Bangladesh (icddr, b))

  • Tania Dottorini

    (University of Nottingham, College Road, Sutton Bonington
    University of Nottingham Ningbo China)

Abstract

In Bangladesh, Vibrio cholerae lineages are undergoing genomic evolution, with increased virulence and spreading ability. However, our understanding of the genomic determinants influencing lineage transmission and disease severity remains incomplete. Here, we developed a computational framework using machine-learning, genome scale metabolic modelling (GSSM) and 3D structural analysis, to identify V. cholerae genomic traits linked to lineage transmission and disease severity. We analysed in-patients isolates from six Bangladeshi regions (2015-2021), and uncovered accessory genes and core SNPs unique to the most recent dominant lineage, with virulence, motility and bacteriophage resistance functions. We also found a strong correlation between V. cholerae genomic traits and disease severity, with some traits overlapping those driving lineage transmission. GSMM and 3D structure analysis unveiled a complex interplay between transcription regulation, protein interaction and stability, and metabolic networks, associated to lifestyle adaptation, intestinal colonization, acid tolerance and symptom severity. Our findings support advancing therapeutics and targeted interventions to mitigate cholera spread.

Suggested Citation

  • Alexandre Maciel-Guerra & Kubra Babaarslan & Michelle Baker & Aura Rahman & Maqsud Hossain & Abdus Sadique & Jahidul Alam & Salim Uzzaman & Mohammad Ferdous Rahman Sarker & Nasrin Sultana & Ashraful I, 2024. "Core and accessory genomic traits of Vibrio cholerae O1 drive lineage transmission and disease severity," Nature Communications, Nature, vol. 15(1), pages 1-21, December.
    • Handle: RePEc:nat:natcom:v:15:y:2024:i:1:d:10.1038_s41467-024-52238-0
    DOI: 10.1038/s41467-024-52238-0
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    References listed on IDEAS

    as
    1. Kathryn Tunyasuvunakool & Jonas Adler & Zachary Wu & Tim Green & Michal Zielinski & Augustin Žídek & Alex Bridgland & Andrew Cowie & Clemens Meyer & Agata Laydon & Sameer Velankar & Gerard J. Kleywegt, 2021. "Highly accurate protein structure prediction for the human proteome," Nature, Nature, vol. 596(7873), pages 590-596, August.
    2. Michelle Baker & Xibin Zhang & Alexandre Maciel-Guerra & Kubra Babaarslan & Yinping Dong & Wei Wang & Yujie Hu & David Renney & Longhai Liu & Hui Li & Maqsud Hossain & Stephan Heeb & Zhiqin Tong & Nic, 2024. "Convergence of resistance and evolutionary responses in Escherichia coli and Salmonella enterica co-inhabiting chicken farms in China," Nature Communications, Nature, vol. 15(1), pages 1-21, December.
    3. D. Scott Merrell & Susan M. Butler & Firdausi Qadri & Nadia A. Dolganov & Ahsfaqul Alam & Mitchell B. Cohen & Stephen B. Calderwood & Gary K. Schoolnik & Andrew Camilli, 2002. "Host-induced epidemic spread of the cholera bacterium," Nature, Nature, vol. 417(6889), pages 642-645, June.
    4. Md Mamun Monir & Mohammad Tarequl Islam & Razib Mazumder & Dinesh Mondal & Kazi Sumaita Nahar & Marzia Sultana & Masatomo Morita & Makoto Ohnishi & Anwar Huq & Haruo Watanabe & Firdausi Qadri & Mustaf, 2023. "Genomic attributes of Vibrio cholerae O1 responsible for 2022 massive cholera outbreak in Bangladesh," Nature Communications, Nature, vol. 14(1), pages 1-8, December.
    5. John Jumper & Richard Evans & Alexander Pritzel & Tim Green & Michael Figurnov & Olaf Ronneberger & Kathryn Tunyasuvunakool & Russ Bates & Augustin Žídek & Anna Potapenko & Alex Bridgland & Clemens Me, 2021. "Highly accurate protein structure prediction with AlphaFold," Nature, Nature, vol. 596(7873), pages 583-589, August.
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