Streptococcus suis is a zoonotic swine pathogen and a major public health concern in Southeast Asia and China. In the Netherlands, where S. suis infection is an occupational hazard, zoonotic S. suis infections are caused by serotype 2 (SS2), MLST-clonal complex (CC) 1 and CC20 strains, whilst invasive porcine infections are most often caused by SS9 CC16 strains. CC1 strains are responsible for the vast majority of zoonotic infections worldwide, but CC20 strains have only been reported from the Netherlands. In contrast, CC16 strains were never reported as a cause of zoonotic S. suis infections. We aimed to identify the genetic basis of zoonotic potential and virulence by comparative whole genome sequencing of invasive S. suis strains. We sequenced 24 strains from patients and 74 invasive porcine strains isolated within the same time frame in the Netherlands and included genome sequences from 18 reference strains in the analysis. A Bayesian Analysis of Population Structure based on the core genome alignment clustered the dataset into 7 groups, representing the major CCs. Phylogeny using Maximum Likelihood based on the core genome SNPs grouped the CC16 and CC20 strains together and away from the other genomes and reference strains. Molecular dating indicated that the CC16 and CC20 strains diverged around the year 1875 when different pig species were introduced in the Netherlands. Zoonotic CC1 and CC20 strains contained less genes compared to non-zoonotic CC16 strains. Moreover, we identified the SalK/SalR two-component signal transduction system (TCSTS) in 69 % of CC20 strains. This TCSTS is involved in virulence in Chinese outbreak strains, but was not detected in strains from outside Asia before. In conclusion, zoonotic CC20 and non-zoonotic CC16 isolates are genetically closely related but differ in their gene content and serotype, which indicates a loss/gain of genes and a capsule switch between the clonal complexes. We postulate that the separation of non-zoonotic CC16 and zoonotic CC20 strains occurred late 19th century. Finally, we identified genes unique to the zoonotic CC20 strains that may contribute to their evolution and their zoonotic potential.
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