TY - JOUR
T1 - Genomic and functional determinants of host spectrum in Group B Streptococcus
AU - Crestani, Chiara
AU - Forde, Taya L.
AU - Bell, John
AU - Lycett, Samantha J.
AU - Oliveira, Laura M.A.
AU - Pinto, Tatiana C.A.
AU - Cobo-Ángel, Claudia G.
AU - Ceballos-Márquez, Alejandro
AU - Phuoc, Nguyen N.
AU - Sirimanapong, Wanna
AU - Chen, Swaine L.
AU - Jamrozy, Dorota
AU - Bentley, Stephen D.
AU - Fontaine, Michael
AU - Zadoks, Ruth N.
N1 - Publisher 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.
PY - 2024/8
Y1 - 2024/8
N2 - 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.
AB - 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.
UR - http://www.scopus.com/inward/record.url?scp=85201045578&partnerID=8YFLogxK
U2 - 10.1371/journal.ppat.1012400
DO - 10.1371/journal.ppat.1012400
M3 - Article
AN - SCOPUS:85201045578
SN - 1553-7366
VL - 20
JO - PLoS Pathogens
JF - PLoS Pathogens
IS - 8 August
M1 - e1012400
ER -