Emergence of carbapenem resistance in persistent Shewanella algae bacteremia: the role of pdsS G547W mutation in adaptive subpopulation dynamics
Abstract This study elucidates the in vivo genetic mechanisms contributing to the emerging resistance to carbapenem in Shewanella algae through a lens of adaptive microbial evolution. Leveraging PacBio amplification-free sequencing, we tracked the evolution of β-lactam resistance in clinical isolate...
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| Format: | Article |
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BMC
2024-11-01
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| Series: | Annals of Clinical Microbiology and Antimicrobials |
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| Online Access: | https://doi.org/10.1186/s12941-024-00759-3 |
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| author | Yao-Ting Huang Po-Yu Liu |
| author_facet | Yao-Ting Huang Po-Yu Liu |
| author_sort | Yao-Ting Huang |
| collection | DOAJ |
| description | Abstract This study elucidates the in vivo genetic mechanisms contributing to the emerging resistance to carbapenem in Shewanella algae through a lens of adaptive microbial evolution. Leveraging PacBio amplification-free sequencing, we tracked the evolution of β-lactam resistance in clinical isolates from a persistent S. algae bacteremia case amidst antimicrobial therapy. Our investigation spotlighted a recurrent G547W mutation in the sensor histidine kinase (pdsS), which was associated with the overexpression of an OmpA-like protein (pdsO) within a proteobacteria-specific sortase system. Intriguingly, we observed a recurrent switch between wild-type and G547W alleles, revealing an adaptive expansion and contraction of underlying cell subpopulations in response to β-lactam exposure. Comparative transcriptome analyses further demonstrated the overexpression of genes pivotal for membrane integrity, biofilm formation, immune evasion, and β-lactamase activation in resistant samples. This underscores the pre-existence of resistant cells at minuscule frequencies even without antibiotic pressure, potentially explaining the within-host emergence of resistance during antibiotic treatments. Our findings provide pivotal insights into the dynamic genetic adaptations of S. algae under therapeutic pressures, unmasking intricate resistance mechanisms and highlighting the critical role of subpopulation dynamics in treatment outcomes. |
| format | Article |
| id | doaj-art-fca01d9049164128b4cd80362f19a0dd |
| institution | Kabale University |
| issn | 1476-0711 |
| language | English |
| publishDate | 2024-11-01 |
| publisher | BMC |
| record_format | Article |
| series | Annals of Clinical Microbiology and Antimicrobials |
| spelling | doaj-art-fca01d9049164128b4cd80362f19a0dd2024-11-24T12:14:32ZengBMCAnnals of Clinical Microbiology and Antimicrobials1476-07112024-11-012311910.1186/s12941-024-00759-3Emergence of carbapenem resistance in persistent Shewanella algae bacteremia: the role of pdsS G547W mutation in adaptive subpopulation dynamicsYao-Ting Huang0Po-Yu Liu1Department of Computer Science and Information Engineering, National Chung Cheng UniversityDivision of Infectious Diseases, Department of Internal Medicine, Taichung Veterans General HospitalAbstract This study elucidates the in vivo genetic mechanisms contributing to the emerging resistance to carbapenem in Shewanella algae through a lens of adaptive microbial evolution. Leveraging PacBio amplification-free sequencing, we tracked the evolution of β-lactam resistance in clinical isolates from a persistent S. algae bacteremia case amidst antimicrobial therapy. Our investigation spotlighted a recurrent G547W mutation in the sensor histidine kinase (pdsS), which was associated with the overexpression of an OmpA-like protein (pdsO) within a proteobacteria-specific sortase system. Intriguingly, we observed a recurrent switch between wild-type and G547W alleles, revealing an adaptive expansion and contraction of underlying cell subpopulations in response to β-lactam exposure. Comparative transcriptome analyses further demonstrated the overexpression of genes pivotal for membrane integrity, biofilm formation, immune evasion, and β-lactamase activation in resistant samples. This underscores the pre-existence of resistant cells at minuscule frequencies even without antibiotic pressure, potentially explaining the within-host emergence of resistance during antibiotic treatments. Our findings provide pivotal insights into the dynamic genetic adaptations of S. algae under therapeutic pressures, unmasking intricate resistance mechanisms and highlighting the critical role of subpopulation dynamics in treatment outcomes.https://doi.org/10.1186/s12941-024-00759-3Shewanella algaeCarbapenem resistanceAdaptive microbial evolutionβ-lactam antibiotics |
| spellingShingle | Yao-Ting Huang Po-Yu Liu Emergence of carbapenem resistance in persistent Shewanella algae bacteremia: the role of pdsS G547W mutation in adaptive subpopulation dynamics Annals of Clinical Microbiology and Antimicrobials Shewanella algae Carbapenem resistance Adaptive microbial evolution β-lactam antibiotics |
| title | Emergence of carbapenem resistance in persistent Shewanella algae bacteremia: the role of pdsS G547W mutation in adaptive subpopulation dynamics |
| title_full | Emergence of carbapenem resistance in persistent Shewanella algae bacteremia: the role of pdsS G547W mutation in adaptive subpopulation dynamics |
| title_fullStr | Emergence of carbapenem resistance in persistent Shewanella algae bacteremia: the role of pdsS G547W mutation in adaptive subpopulation dynamics |
| title_full_unstemmed | Emergence of carbapenem resistance in persistent Shewanella algae bacteremia: the role of pdsS G547W mutation in adaptive subpopulation dynamics |
| title_short | Emergence of carbapenem resistance in persistent Shewanella algae bacteremia: the role of pdsS G547W mutation in adaptive subpopulation dynamics |
| title_sort | emergence of carbapenem resistance in persistent shewanella algae bacteremia the role of pdss g547w mutation in adaptive subpopulation dynamics |
| topic | Shewanella algae Carbapenem resistance Adaptive microbial evolution β-lactam antibiotics |
| url | https://doi.org/10.1186/s12941-024-00759-3 |
| work_keys_str_mv | AT yaotinghuang emergenceofcarbapenemresistanceinpersistentshewanellaalgaebacteremiatheroleofpdssg547wmutationinadaptivesubpopulationdynamics AT poyuliu emergenceofcarbapenemresistanceinpersistentshewanellaalgaebacteremiatheroleofpdssg547wmutationinadaptivesubpopulationdynamics |