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- Title
Genomic and functional determinants of host spectrum in Group B Streptococcus.
- Authors
Crestani, Chiara; Forde, Taya L.; Bell, John; Lycett, Samantha J.; Oliveira, Laura M. A.; Pinto, Tatiana C. A.; Cobo-Ángel, Claudia G.; Ceballos-Márquez, Alejandro; Phuoc, Nguyen N.; Sirimanapong, Wanna; Chen, Swaine L.; Jamrozy, Dorota; Bentley, Stephen D.; Fontaine, Michael; Zadoks, Ruth N.
- Abstract
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. Author summary: Group B Streptococcus (GBS) is a bacterium that represents a health and food security threat in three major host groups: humans (in particular neonates), bovines, and fishes. However, the genomic mechanisms driving adaptation to these hosts remain unclear. Here, we use powerful statistical approaches to compare genomes of GBS from around the world. We found that GBS' ability to exchange genes is a good indicator of how well it can adapt to different hosts. Additionally, three groups of genes appear crucial for GBS to infect either humans, cows, or fishes, regardless of the bacterial strain. These gene groups are also found in other similar bacteria that live in the same hosts or environments. Where a functional role is already known for two gene groups in humans and bovines, respectively, it is shown here for the first time for the third gene group in fishes. Our findings demonstrate the importance of considering the role of animals in the evolution of multi-host bacterial pathogens like GBS. Gene exchange between bacteria infecting multiple hosts represents a high threat to human health, as high-risk types of GBS could adapt and expand in animals, which could then act as reservoirs for highly pathogenic human infections.
- Subjects
BIOLOGICAL evolution; STREPTOCOCCUS agalactiae; GENE clusters; BACTERIAL evolution; FOOD security
- Publication
PLoS Pathogens, 2024, Vol 20, Issue 8, p1
- ISSN
1553-7366
- Publication type
Article
- DOI
10.1371/journal.ppat.1012400