Emergence of novel zoonotic and multidrug-resistant Streptococcus suis lineages

Abstract

Objectives Streptococcus suis is an emerging zoonotic porcine pathogen and a leading cause of adult bacterial meningitis in Southeast Asia, associated with raw pork consumption. Most zoonotic S. suis infections globally are caused by strains from lineage CC1 carrying a serotype 2 capsule. However, in Thailand, ∼40% of the reported zoonotic infections are caused by 2 endemic lineages, CC104 and CC233, which also have a serotype 2 capsule. In this study, we aimed to identify the drivers of the emergence and recent evolution of these two lineages. Methods We sequenced the whole genomes of 141 Thai S. suis zoonotic and porcine strains isolated over a 15-year period and combined them with a curated global dataset of 2761 published S. suis genomes. Using comparative genomics, Bayesian evolutionary models, and multivariate analysis, we investigated the emergence of zoonotic potential and multidrug resistance in CC104 and CC233. Results We estimated recent emergence dates for both CC104 (1990; 95% posterior: 1987–1992) and CC233 (2002; 95% posterior: 2000–2004). Both lineages acquired a serotype capsule 2 from CC1 through a capsule locus switching event, prior to their emergence. Both lineages have also experienced multiple antimicrobial resistance acquisition events, with some strains carrying 12 determinants encoding resistance against 8 classes of antibiotics. Most importantly, CC104 and CC233 lineages are the first zoonotic lineages to have acquired increased resistance to penicillin and ceftriaxone, which form the standard therapy to treat S. suis infections in humans. Conclusions Horizontal transfer of multiple genomic regions can cause rapid emergence of novel multidrug-resistant zoonotic S. suis lineages. As S. suis is mainly controlled and treated through the use of antibiotics in both pigs and humans, these findings highlight the urgent need for improved and enhanced surveillance, infection control, and treatments.