Genomic Traits Associated with Virulence and Antimicrobial Resistance of Invasive Group B Streptococcus Isolates with Reduced Penicillin Susceptibility from Elderly Adults
ABSTRACT This study aimed to investigate genomic traits underlying the antimicrobial resistance and virulence of multidrug-resistant (MDR) group B streptococci with reduced penicillin susceptibility (PRGBS) recovered from elderly patients with bloodstream infections, which remain poorly characterize...
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| Format: | Article |
| Language: | English |
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American Society for Microbiology
2022-06-01
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| Series: | Microbiology Spectrum |
| Subjects: | |
| Online Access: | https://journals.asm.org/doi/10.1128/spectrum.00568-22 |
| _version_ | 1818546823637237760 |
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| author | Shota Koide Yukiko Nagano Shino Takizawa Kanae Sakaguchi Eiji Soga Wataru Hayashi Mizuki Tanabe Tomohiro Denda Kouji Kimura Yoshichika Arakawa Noriyuki Nagano |
| author_facet | Shota Koide Yukiko Nagano Shino Takizawa Kanae Sakaguchi Eiji Soga Wataru Hayashi Mizuki Tanabe Tomohiro Denda Kouji Kimura Yoshichika Arakawa Noriyuki Nagano |
| author_sort | Shota Koide |
| collection | DOAJ |
| description | ABSTRACT This study aimed to investigate genomic traits underlying the antimicrobial resistance and virulence of multidrug-resistant (MDR) group B streptococci with reduced penicillin susceptibility (PRGBS) recovered from elderly patients with bloodstream infections, which remain poorly characterized. The pangenome was found to be open, with the predicted pan- and core genome sizes being 3,531 and 1,694 genes, respectively. Accessory and unique genes were enriched for the Clusters of Orthologous Groups (COG) categories L, Replication, recombination, and repair, and K, Transcription. All MDR PRGBS isolates retained a core virulence gene repertoire (bibA, fbsA/-B/-C, cspA, cfb, hylB, scpB, lmb, and the cyl operon), supporting an invasive ability similar to that of the other invasive GBS, penicillin-susceptible GBS (PSGBS), and noninvasive PRGBS isolates. The putative sequence type 1 (ST1)-specific AlpST-1 virulence gene was also retained among the serotype Ia/ST1 PRGBS isolates. In addition to tet(M) and erm(B), mef(A)-msr(D) elements or the high-level gentamicin resistance gene aac(6′)-aph(2″), which are both rare in PSGBS, were detected among those MDR PRGBS isolates. In the core single-nucleotide polymorphism (SNP) phylogenetic tree, all invasive ST1 PRGBS isolates with serotypes Ia and III were placed together in a clade with a recombination rate of 3.97, which was 36 times higher than the value found for a clade formed by serotype V/ST1 PSGBS isolates derived mostly from human blood. ST1 has been the predominant sequence type among the PRGBS isolates in Japan, and serotypes Ia and III have been very rare among the ST1 PSGBS isolates. Thus, these lineages that mostly consisted of serotypes Ia/ST1 and III/ST1 PRGBS could possibly emerge through recombination within the ST1 populations. IMPORTANCE Streptococcus agalactiae, or group B Streptococcus (GBS), is recognized as the leading cause of neonatal invasive infections. However, an increasing incidence of invasive GBS infections among nonpregnant adults, particularly the elderly and those with underlying diseases, has been observed. There is a trend toward the increasing occurrence of penicillin nonsusceptibility among GBS clinical isolates, from 4.8% in 2008 to 5.8% in 2020 in Japan. Also, in the United States, the frequency of adult invasive GBS isolates suggestive of β-lactam nonsusceptibility increased from 0.7% in 2015 to 1.0% in 2016. In adults, mortality has been significantly higher among patients with bacteremia than among those without bacteremia. Our study revealed that invasive GBS with reduced penicillin susceptibility (PRGBS) isolates harbor major virulence and resistance genes known among GBS, highlighting the need for large population-based genomic surveillance studies to better understand the clinical relevance of invasive PRGBS isolates. |
| first_indexed | 2024-12-12T07:58:23Z |
| format | Article |
| id | doaj.art-49eff6cd3e2d43ac815f0c0cf8523b14 |
| institution | Directory Open Access Journal |
| issn | 2165-0497 |
| language | English |
| last_indexed | 2024-12-12T07:58:23Z |
| publishDate | 2022-06-01 |
| publisher | American Society for Microbiology |
| record_format | Article |
| series | Microbiology Spectrum |
| spelling | doaj.art-49eff6cd3e2d43ac815f0c0cf8523b142022-12-22T00:32:13ZengAmerican Society for MicrobiologyMicrobiology Spectrum2165-04972022-06-0110310.1128/spectrum.00568-22Genomic Traits Associated with Virulence and Antimicrobial Resistance of Invasive Group B Streptococcus Isolates with Reduced Penicillin Susceptibility from Elderly AdultsShota Koide0Yukiko Nagano1Shino Takizawa2Kanae Sakaguchi3Eiji Soga4Wataru Hayashi5Mizuki Tanabe6Tomohiro Denda7Kouji Kimura8Yoshichika Arakawa9Noriyuki Nagano10Department of Medical Sciences, Shinshu University Graduate School of Medicine, Science and Technology, Matsumoto, JapanDepartment of Health and Medical Sciences, Shinshu University Graduate School of Medicine, Matsumoto, JapanDepartment of Health and Medical Sciences, Shinshu University Graduate School of Medicine, Matsumoto, JapanDepartment of Health and Medical Sciences, Shinshu University Graduate School of Medicine, Matsumoto, JapanDepartment of Health and Medical Sciences, Shinshu University Graduate School of Medicine, Matsumoto, JapanDepartment of Medical Sciences, Shinshu University Graduate School of Medicine, Science and Technology, Matsumoto, JapanDepartment of Health and Medical Sciences, Shinshu University Graduate School of Medicine, Matsumoto, JapanDepartment of Health and Medical Sciences, Shinshu University Graduate School of Medicine, Matsumoto, JapanNagoya University Graduate School of Medicine, Nagoya, JapanNagoya University Graduate School of Medicine, Nagoya, JapanDepartment of Medical Sciences, Shinshu University Graduate School of Medicine, Science and Technology, Matsumoto, JapanABSTRACT This study aimed to investigate genomic traits underlying the antimicrobial resistance and virulence of multidrug-resistant (MDR) group B streptococci with reduced penicillin susceptibility (PRGBS) recovered from elderly patients with bloodstream infections, which remain poorly characterized. The pangenome was found to be open, with the predicted pan- and core genome sizes being 3,531 and 1,694 genes, respectively. Accessory and unique genes were enriched for the Clusters of Orthologous Groups (COG) categories L, Replication, recombination, and repair, and K, Transcription. All MDR PRGBS isolates retained a core virulence gene repertoire (bibA, fbsA/-B/-C, cspA, cfb, hylB, scpB, lmb, and the cyl operon), supporting an invasive ability similar to that of the other invasive GBS, penicillin-susceptible GBS (PSGBS), and noninvasive PRGBS isolates. The putative sequence type 1 (ST1)-specific AlpST-1 virulence gene was also retained among the serotype Ia/ST1 PRGBS isolates. In addition to tet(M) and erm(B), mef(A)-msr(D) elements or the high-level gentamicin resistance gene aac(6′)-aph(2″), which are both rare in PSGBS, were detected among those MDR PRGBS isolates. In the core single-nucleotide polymorphism (SNP) phylogenetic tree, all invasive ST1 PRGBS isolates with serotypes Ia and III were placed together in a clade with a recombination rate of 3.97, which was 36 times higher than the value found for a clade formed by serotype V/ST1 PSGBS isolates derived mostly from human blood. ST1 has been the predominant sequence type among the PRGBS isolates in Japan, and serotypes Ia and III have been very rare among the ST1 PSGBS isolates. Thus, these lineages that mostly consisted of serotypes Ia/ST1 and III/ST1 PRGBS could possibly emerge through recombination within the ST1 populations. IMPORTANCE Streptococcus agalactiae, or group B Streptococcus (GBS), is recognized as the leading cause of neonatal invasive infections. However, an increasing incidence of invasive GBS infections among nonpregnant adults, particularly the elderly and those with underlying diseases, has been observed. There is a trend toward the increasing occurrence of penicillin nonsusceptibility among GBS clinical isolates, from 4.8% in 2008 to 5.8% in 2020 in Japan. Also, in the United States, the frequency of adult invasive GBS isolates suggestive of β-lactam nonsusceptibility increased from 0.7% in 2015 to 1.0% in 2016. In adults, mortality has been significantly higher among patients with bacteremia than among those without bacteremia. Our study revealed that invasive GBS with reduced penicillin susceptibility (PRGBS) isolates harbor major virulence and resistance genes known among GBS, highlighting the need for large population-based genomic surveillance studies to better understand the clinical relevance of invasive PRGBS isolates.https://journals.asm.org/doi/10.1128/spectrum.00568-22group B streptococcipenicillin nonsusceptiblebacteremiaelderly adults |
| spellingShingle | Shota Koide Yukiko Nagano Shino Takizawa Kanae Sakaguchi Eiji Soga Wataru Hayashi Mizuki Tanabe Tomohiro Denda Kouji Kimura Yoshichika Arakawa Noriyuki Nagano Genomic Traits Associated with Virulence and Antimicrobial Resistance of Invasive Group B Streptococcus Isolates with Reduced Penicillin Susceptibility from Elderly Adults Microbiology Spectrum group B streptococci penicillin nonsusceptible bacteremia elderly adults |
| title | Genomic Traits Associated with Virulence and Antimicrobial Resistance of Invasive Group B Streptococcus Isolates with Reduced Penicillin Susceptibility from Elderly Adults |
| title_full | Genomic Traits Associated with Virulence and Antimicrobial Resistance of Invasive Group B Streptococcus Isolates with Reduced Penicillin Susceptibility from Elderly Adults |
| title_fullStr | Genomic Traits Associated with Virulence and Antimicrobial Resistance of Invasive Group B Streptococcus Isolates with Reduced Penicillin Susceptibility from Elderly Adults |
| title_full_unstemmed | Genomic Traits Associated with Virulence and Antimicrobial Resistance of Invasive Group B Streptococcus Isolates with Reduced Penicillin Susceptibility from Elderly Adults |
| title_short | Genomic Traits Associated with Virulence and Antimicrobial Resistance of Invasive Group B Streptococcus Isolates with Reduced Penicillin Susceptibility from Elderly Adults |
| title_sort | genomic traits associated with virulence and antimicrobial resistance of invasive group b streptococcus isolates with reduced penicillin susceptibility from elderly adults |
| topic | group B streptococci penicillin nonsusceptible bacteremia elderly adults |
| url | https://journals.asm.org/doi/10.1128/spectrum.00568-22 |
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