Streptococcus pasteurianus, an underreported opportunistic pathogen, is considered an increasingly recognized cause of meningitis and bacteremia in many animals and humans worldwide. However, except for some epidemiological studies, there is no report about the gene‐deletion mutagenesis, virulence factors, reservoir niches or animal infection models for this pathogen. In this study, we first isolated an S. pasteurianus strain from a newly weaned piglet's brain with meningitis. The genomic sequence of this swine isolate WUSP067 shared high homology with that of two human strains. The comparative genome analysis showed that strain WUSP067 contained a fucose utilization cluster absent in human strains, and it shared 91% identity with that of an integrative and conjugative element (ICE) ICEssuZJ20091101‐2 from Streptococcus suis, another important swine bacterial pathogen. Strain WUSP067 was resistant to erythromycin, tulathromycin, lincomycin, clindamycin, doxycycline and gentamycin, and ICEs are vehicles for harbouring antimicrobial resistance genes. The infection model was established using the 3‐week‐old newly weaned ICR mice. The 50% lethal dose value of strain WUSP067 was 4.0 × 107 colony‐forming units per mouse. The infected mice showed severe signs of meningitis and pathological changes in brains. Furthermore, the capsule‐deficient mutant was generated using natural transformation, and we showed that capsule was an essential virulence factor for S. pasteurianus. In addition, we found that tonsils and hilar lymph nodes of healthy pigs may be reservoir niches for this bacterium. Thus, our study provided valuable information about the pathogenetic characteristics and antimicrobial resistance of S. pasteurianus and paved the way for studying its pathogenesis.

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Streptococcus pasteurianus is a zoonotic pathogen causing meningitis and bacteremia in animals and humans. A lack of accurate and convenient detection methods hinders preventing and controlling diseases caused by S. pasteurianus. Additionally, there is limited knowledge about its pathogenicity and antimicrobial resistance characteristics, as there are only three complete genome sequences available. In this study, we established a multiplex PCR assay for the detection of S. pasteurianus, which was applied to six fecal samples from cattle with diarrhea and 285 samples from healthy pigs. Out of the samples tested, 24 were positive, including 5 from pig tonsils, 18 from pig hilar lymph nodes, and 1 from cattle feces. Two strains were isolated from positive samples, and their complete genomes were sequenced. The two strains were non-virulent in mice and multidrug-resistant by the antimicrobial susceptibility test. We first found the presence of genes tet(O/W/32/O) and lsa(E) in S. pasteurianus, leading to resistance to lincosamides and tetracyclines. The convenient and specific multiplex PCR assay provides essential technical support for epidemiological research, and the complete genome sequence of two non-virulent strains contributes to understanding this zoonotic bacterium’s genomic characteristics and pathogenesis.