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

Alexandre Maciel-Guerra, Kubra Babaarslan, Michelle Baker, Aura Rahman, Maqsud Hossain, Abdus Sadique, Jahidul Alam, Salim Uzzaman, Mohammad Ferdous Rahman Sarker, Nasrin Sultana, Ashraful Islam Khan, Yasmin Ara Begum, Mokibul Hassan Afrad, Nicola Senin, Zakir Hossain Habib, Tahmina Shirin, Firdausi Qadri and Tania Dottorini ()
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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
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

Nature Communications, 2024, vol. 15, issue 1, 1-21

Abstract: 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.

Date: 2024
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DOI: 10.1038/s41467-024-52238-0

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