Genomic and functional determinants of host spectrum in Group B Streptococcus.


Journal

PLoS pathogens
ISSN: 1553-7374
Titre abrégé: PLoS Pathog
Pays: United States
ID NLM: 101238921

Informations de publication

Date de publication:
12 Aug 2024
Historique:
received: 25 04 2024
accepted: 08 07 2024
medline: 12 8 2024
pubmed: 12 8 2024
entrez: 12 8 2024
Statut: aheadofprint

Résumé

Group B Streptococcus (GBS) is a major human and animal pathogen that threatens public health and food security. Spill-over and spill-back between host species is possible due to adaptation and amplification of GBS in new niches but the evolutionary and functional mechanisms underpinning those phenomena are poorly known. Based on analysis of 1,254 curated genomes from all major GBS host species and six continents, we found that the global GBS population comprises host-generalist, host-adapted and host-restricted sublineages, which are found across host groups, preferentially within one host group, or exclusively within one host group, respectively, and show distinct levels of recombination. Strikingly, the association of GBS genomes with the three major host groups (humans, cattle, fish) is driven by a single accessory gene cluster per host, regardless of sublineage or the breadth of host spectrum. Moreover, those gene clusters are shared with other streptococcal species occupying the same niche and are functionally relevant for host tropism. Our findings demonstrate (1) the heterogeneity of genome plasticity within a bacterial species of public health importance, enabling the identification of high-risk clones; (2) the contribution of inter-species gene transmission to the evolution of GBS; and (3) the importance of considering the role of animal hosts, and the accessory gene pool associated with their microbiota, in the evolution of multi-host bacterial pathogens. Collectively, these phenomena may explain the adaptation and clonal expansion of GBS in animal reservoirs and the risk of spill-over and spill-back between animals and humans.

Identifiants

pubmed: 39133742
doi: 10.1371/journal.ppat.1012400
pii: PPATHOGENS-D-24-00882
doi:

Types de publication

Journal Article

Langues

eng

Sous-ensembles de citation

IM

Pagination

e1012400

Informations de copyright

Copyright: © 2024 Crestani et al. This is an open access article distributed under the terms of the Creative Commons Attribution License, which permits unrestricted use, distribution, and reproduction in any medium, provided the original author and source are credited.

Déclaration de conflit d'intérêts

I have read the journal’s policy and the authors of this manuscript have the following competing interests: A patent for Group B Streptococcus (GBS) antigens associated with strains virulent in fish has been filed by the Moredun Research Institute. MF and RZ are named inventors on this application. The International Patent Application number is WO 2016/034879 Al. This application covers GBS genes required for virulence in fish, i.e. Locus 3 as described in this manuscript.

Auteurs

Chiara Crestani (C)

Institute of Biodiversity, Animal Health & Comparative Medicine, University of Glasgow, Glasgow, Scotland, United Kingdom.

Taya L Forde (TL)

Institute of Biodiversity, Animal Health & Comparative Medicine, University of Glasgow, Glasgow, Scotland, United Kingdom.

John Bell (J)

Moredun Research Institute, Penicuik, Scotland, United Kingdom.

Samantha J Lycett (SJ)

The Roslin Institute, University of Edinburgh, Midlothian, Scotland, United Kingdom.

Laura M A Oliveira (LMA)

Instituto de Microbiologia Paulo de Goes, Federal University of Rio de Janeiro, Rio de Janeiro, State of Rio de Janeiro, Brazil.

Tatiana C A Pinto (TCA)

Instituto de Microbiologia Paulo de Goes, Federal University of Rio de Janeiro, Rio de Janeiro, State of Rio de Janeiro, Brazil.

Claudia G Cobo-Ángel (CG)

CLEV research group, Universidad de Caldas, Manizales, Caldas, Colombia.

Alejandro Ceballos-Márquez (A)

CLEV research group, Universidad de Caldas, Manizales, Caldas, Colombia.

Nguyen N Phuoc (NN)

Faculty of Fisheries, University of Agriculture and Forestry, Hue University, Hue, Vietnam.

Wanna Sirimanapong (W)

Faculty of Veterinary Science, Mahidol University, Nakhon Pathom, Thailand.

Swaine L Chen (SL)

Infectious Diseases Translational Research Programme, Department of Medicine, Division of Infectious Diseases, Yong Loo Lin School of Medicine, National University of Singapore, Singapore.
Laboratory of Bacterial Genomics, Genome Institute of Singapore, Singapore.

Dorota Jamrozy (D)

Parasites and Microbes Programme, Wellcome Sanger Institute, Hinxton, England, United Kingdom.

Stephen D Bentley (SD)

Parasites and Microbes Programme, Wellcome Sanger Institute, Hinxton, England, United Kingdom.

Michael Fontaine (M)

Moredun Research Institute, Penicuik, Scotland, United Kingdom.

Ruth N Zadoks (RN)

Institute of Biodiversity, Animal Health & Comparative Medicine, University of Glasgow, Glasgow, Scotland, United Kingdom.
Moredun Research Institute, Penicuik, Scotland, United Kingdom.
Sydney School of Veterinary Science, Faculty of Science, University of Sydney, Camden, NSW, Australia.

Classifications MeSH