Municipal wastewater monitoring revealed the predominance of bla GES genes with diverse variants among carbapenemase-producing organisms: high occurrence and persistence of Aeromonas caviae harboring the new bla GES variant bla GES-48
ABSTRACT We characterized carbapenemase-producing organism (CPO) detected in municipal wastewater to better understand the epidemiology of CPOs in the community. In total, 36 samples were collected at six sampling sites every other month from December 2020 to October 2021. CPOs were not recovered fr...
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| Format: | Article |
| Language: | English |
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American Society for Microbiology
2023-12-01
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| Series: | Microbiology Spectrum |
| Subjects: | |
| Online Access: | https://journals.asm.org/doi/10.1128/spectrum.02188-23 |
| _version_ | 1797393633595359232 |
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| author | Mizuki Tanabe Yo Sugawara Tomohiro Denda Kanae Sakaguchi Shino Takizawa Shota Koide Wataru Hayashi Liansheng Yu Shizuo Kayama Motoyuki Sugai Yukiko Nagano Noriyuki Nagano |
| author_facet | Mizuki Tanabe Yo Sugawara Tomohiro Denda Kanae Sakaguchi Shino Takizawa Shota Koide Wataru Hayashi Liansheng Yu Shizuo Kayama Motoyuki Sugai Yukiko Nagano Noriyuki Nagano |
| author_sort | Mizuki Tanabe |
| collection | DOAJ |
| description | ABSTRACT We characterized carbapenemase-producing organism (CPO) detected in municipal wastewater to better understand the epidemiology of CPOs in the community. In total, 36 samples were collected at six sampling sites every other month from December 2020 to October 2021. CPOs were not recovered from influent taken from inlet A receiving separated sewer line, treated effluents, and river water samples upstream and downstream of the effluent outlet. By contrast, 75 CPOs were detected in all influent samples taken from inlets B and C receiving combined sewer lines collecting both domestic/industrial wastewater and rainwater runoff. Aeromonas caviae was the dominant species (25/75, 33.3%), and the other 11 Aeromonas spp. together accounted for 48% of CPOs. The remaining 39 Enterobacterales strains mainly comprised 17 Klebsiella spp. and 10 Raoultella spp. CPOs carrying bla GES carbapenemase genes were overwhelmingly dominant, accounting for 72 of 75 isolates, including two isolates harboring both bla GES-24 and bla IMP-1 (96%), followed by three bla IMPs-positive isolates, where those carbapenemase genes were mainly carried in diverse class 1 integrons. Among bla GES variants, including six new variants (bla GES-47, bla GES-48, bla GES-49, bla GES-50, bla GES-51, and bla GES-54), bla GES-5 was detected in 28 CPOs, with Aeromonas spp. accounting for 53.6% of these organisms. Quantitative analysis revealed that the repeated detection of bla GES-48-positive A. caviae ST1056 from both inlets B and C ranked the total number of this bacterial clone highest in the wastewater influent. In summary, our study revealed the high prevalence and persistence of diverse bla GES carbapenemase genes among CPOs isolated from influent inlets connected to combined sewer systems. IMPORTANCE The emergence and spread of carbapenemase-producing organisms (CPOs) represent a global health threat because they are associated with limited treatment options and poor clinical outcomes. Wastewater is considered a hotspot for the evolution and dissemination of antimicrobial resistance. Thus, analyses of municipal wastewater are critical for understanding the circulation of these CPOs and carbapenemase genes in local communities, which remains scarcely known in Japan. This study resulted in several key observations: (i) the vast majority of bla GES genes, including six new bla GES variants, and less frequent bla IMP genes were carbapenemase genes encountered exclusively in wastewater influent; (ii) the most dominant CPO species were Aeromonas spp., in which a remarkable diversity of new sequence types was observed; and (iii) CPOs were detected from combined sewer wastewater, but not from separate sewer wastewater, suggesting that the load of CPOs from unrecognized environmental sources could greatly contribute to their detection in influent wastewater. |
| first_indexed | 2024-03-09T00:05:33Z |
| format | Article |
| id | doaj.art-d50dd017450c418bb3e1b3132ca0f628 |
| institution | Directory Open Access Journal |
| issn | 2165-0497 |
| language | English |
| last_indexed | 2024-03-09T00:05:33Z |
| publishDate | 2023-12-01 |
| publisher | American Society for Microbiology |
| record_format | Article |
| series | Microbiology Spectrum |
| spelling | doaj.art-d50dd017450c418bb3e1b3132ca0f6282023-12-12T13:17:21ZengAmerican Society for MicrobiologyMicrobiology Spectrum2165-04972023-12-0111610.1128/spectrum.02188-23Municipal wastewater monitoring revealed the predominance of bla GES genes with diverse variants among carbapenemase-producing organisms: high occurrence and persistence of Aeromonas caviae harboring the new bla GES variant bla GES-48Mizuki Tanabe0Yo Sugawara1Tomohiro Denda2Kanae Sakaguchi3Shino Takizawa4Shota Koide5Wataru Hayashi6Liansheng Yu7Shizuo Kayama8Motoyuki Sugai9Yukiko Nagano10Noriyuki Nagano11Department of Health and Medical Sciences, Graduate School of Medicine, Shinshu University , Matsumoto, Nagano, JapanAntimicrobial Resistance Research Center, National Institute of Infectious Diseases , Higashimurayama, Tokyo, JapanDepartment of Health and Medical Sciences, Graduate School of Medicine, Shinshu University , Matsumoto, Nagano, JapanDepartment of Health and Medical Sciences, Graduate School of Medicine, Shinshu University , Matsumoto, Nagano, JapanDepartment of Health and Medical Sciences, Graduate School of Medicine, Shinshu University , Matsumoto, Nagano, JapanDepartment of Medical Sciences, Shinshu University, Graduate School of Medicine, Science and Technology , Matsumoto, Nagano, JapanDepartment of Medical Sciences, Shinshu University, Graduate School of Medicine, Science and Technology , Matsumoto, Nagano, JapanAntimicrobial Resistance Research Center, National Institute of Infectious Diseases , Higashimurayama, Tokyo, JapanAntimicrobial Resistance Research Center, National Institute of Infectious Diseases , Higashimurayama, Tokyo, JapanAntimicrobial Resistance Research Center, National Institute of Infectious Diseases , Higashimurayama, Tokyo, JapanDepartment of Health and Medical Sciences, Graduate School of Medicine, Shinshu University , Matsumoto, Nagano, JapanDepartment of Health and Medical Sciences, Graduate School of Medicine, Shinshu University , Matsumoto, Nagano, JapanABSTRACT We characterized carbapenemase-producing organism (CPO) detected in municipal wastewater to better understand the epidemiology of CPOs in the community. In total, 36 samples were collected at six sampling sites every other month from December 2020 to October 2021. CPOs were not recovered from influent taken from inlet A receiving separated sewer line, treated effluents, and river water samples upstream and downstream of the effluent outlet. By contrast, 75 CPOs were detected in all influent samples taken from inlets B and C receiving combined sewer lines collecting both domestic/industrial wastewater and rainwater runoff. Aeromonas caviae was the dominant species (25/75, 33.3%), and the other 11 Aeromonas spp. together accounted for 48% of CPOs. The remaining 39 Enterobacterales strains mainly comprised 17 Klebsiella spp. and 10 Raoultella spp. CPOs carrying bla GES carbapenemase genes were overwhelmingly dominant, accounting for 72 of 75 isolates, including two isolates harboring both bla GES-24 and bla IMP-1 (96%), followed by three bla IMPs-positive isolates, where those carbapenemase genes were mainly carried in diverse class 1 integrons. Among bla GES variants, including six new variants (bla GES-47, bla GES-48, bla GES-49, bla GES-50, bla GES-51, and bla GES-54), bla GES-5 was detected in 28 CPOs, with Aeromonas spp. accounting for 53.6% of these organisms. Quantitative analysis revealed that the repeated detection of bla GES-48-positive A. caviae ST1056 from both inlets B and C ranked the total number of this bacterial clone highest in the wastewater influent. In summary, our study revealed the high prevalence and persistence of diverse bla GES carbapenemase genes among CPOs isolated from influent inlets connected to combined sewer systems. IMPORTANCE The emergence and spread of carbapenemase-producing organisms (CPOs) represent a global health threat because they are associated with limited treatment options and poor clinical outcomes. Wastewater is considered a hotspot for the evolution and dissemination of antimicrobial resistance. Thus, analyses of municipal wastewater are critical for understanding the circulation of these CPOs and carbapenemase genes in local communities, which remains scarcely known in Japan. This study resulted in several key observations: (i) the vast majority of bla GES genes, including six new bla GES variants, and less frequent bla IMP genes were carbapenemase genes encountered exclusively in wastewater influent; (ii) the most dominant CPO species were Aeromonas spp., in which a remarkable diversity of new sequence types was observed; and (iii) CPOs were detected from combined sewer wastewater, but not from separate sewer wastewater, suggesting that the load of CPOs from unrecognized environmental sources could greatly contribute to their detection in influent wastewater.https://journals.asm.org/doi/10.1128/spectrum.02188-23carbapenemasewastewaterbla GESsbla IMPsAeromonas spp.Enterobacterales |
| spellingShingle | Mizuki Tanabe Yo Sugawara Tomohiro Denda Kanae Sakaguchi Shino Takizawa Shota Koide Wataru Hayashi Liansheng Yu Shizuo Kayama Motoyuki Sugai Yukiko Nagano Noriyuki Nagano Municipal wastewater monitoring revealed the predominance of bla GES genes with diverse variants among carbapenemase-producing organisms: high occurrence and persistence of Aeromonas caviae harboring the new bla GES variant bla GES-48 Microbiology Spectrum carbapenemase wastewater bla GESs bla IMPs Aeromonas spp. Enterobacterales |
| title | Municipal wastewater monitoring revealed the predominance of bla GES genes with diverse variants among carbapenemase-producing organisms: high occurrence and persistence of Aeromonas caviae harboring the new bla GES variant bla GES-48 |
| title_full | Municipal wastewater monitoring revealed the predominance of bla GES genes with diverse variants among carbapenemase-producing organisms: high occurrence and persistence of Aeromonas caviae harboring the new bla GES variant bla GES-48 |
| title_fullStr | Municipal wastewater monitoring revealed the predominance of bla GES genes with diverse variants among carbapenemase-producing organisms: high occurrence and persistence of Aeromonas caviae harboring the new bla GES variant bla GES-48 |
| title_full_unstemmed | Municipal wastewater monitoring revealed the predominance of bla GES genes with diverse variants among carbapenemase-producing organisms: high occurrence and persistence of Aeromonas caviae harboring the new bla GES variant bla GES-48 |
| title_short | Municipal wastewater monitoring revealed the predominance of bla GES genes with diverse variants among carbapenemase-producing organisms: high occurrence and persistence of Aeromonas caviae harboring the new bla GES variant bla GES-48 |
| title_sort | municipal wastewater monitoring revealed the predominance of bla ges genes with diverse variants among carbapenemase producing organisms high occurrence and persistence of aeromonas caviae harboring the new bla ges variant bla ges 48 |
| topic | carbapenemase wastewater bla GESs bla IMPs Aeromonas spp. Enterobacterales |
| url | https://journals.asm.org/doi/10.1128/spectrum.02188-23 |
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