Genomic epidemiology and resistome dynamics of Enterobacter species in a Portuguese Open Air Laboratory: the emergence of the FRI-8 carbapenemase
Interconnected reservoirs contribute to the global spread of antimicrobial resistance (AMR), including carbapenem- and colistin-resistant Enterobacterales, highlighting the need for a One Health approach. We assessed the genomic epidemiology, diversity and AMR mechanisms of Enterobacter spp. across...
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Frontiers Media S.A.
2025-07-01
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| author | Pedro Teixeira Miguel Ramos Rani Rivière Mónica Azevedo Mónica Azevedo Mónica Azevedo Mário Ferreira Maria Manuela Cano Patrícia Vieira Lígia Reis Rui Matias João Rodrigues Carina Menezes Tânia Rosado António Sequeira Olga Moreira Werner Ruppitsch Werner Ruppitsch Adriana Cabal-Rosel Solveig Sølverød Mo Elsa Dias Elsa Dias Elsa Dias Markus Woegerbauer Manuela Caniça Manuela Caniça Manuela Caniça Manuela Caniça Vera Manageiro Vera Manageiro Vera Manageiro |
| author_facet | Pedro Teixeira Miguel Ramos Rani Rivière Mónica Azevedo Mónica Azevedo Mónica Azevedo Mário Ferreira Maria Manuela Cano Patrícia Vieira Lígia Reis Rui Matias João Rodrigues Carina Menezes Tânia Rosado António Sequeira Olga Moreira Werner Ruppitsch Werner Ruppitsch Adriana Cabal-Rosel Solveig Sølverød Mo Elsa Dias Elsa Dias Elsa Dias Markus Woegerbauer Manuela Caniça Manuela Caniça Manuela Caniça Manuela Caniça Vera Manageiro Vera Manageiro Vera Manageiro |
| author_sort | Pedro Teixeira |
| collection | DOAJ |
| description | Interconnected reservoirs contribute to the global spread of antimicrobial resistance (AMR), including carbapenem- and colistin-resistant Enterobacterales, highlighting the need for a One Health approach. We assessed the genomic epidemiology, diversity and AMR mechanisms of Enterobacter spp. across interconnected human, animal, plant, and environmental reservoirs in a Portuguese Open Air Laboratory. Over a one year monitoring period, samples from 12 different compartments were collected and processed using selective media to isolate Enterobacter spp., which were subjected to antibiotic susceptibility testing, whole-genome sequencing and subsequent analyses to identify AMR determinants, characterize plasmids and phylogenetic relationships. We established a collection of 61 Enterobacter isolates spanning nine species and 32 sequence types, including 16 novel ones, across nine compartments (river water, wastewater, soil, manure, feed, air, farmers, pigs, wild animals), reflecting the diversity and ubiquity of Enterobacter species. Core-genome analysis revealed eight genetic clusters, suggesting clonal transmission across compartments. In total, 29 antibiotic resistance genes were detected across all isolates. Notably, this is the first documentation of blaFRI-harbouring Enterobacterales in European environmental settings and the first to describe blaFRI, blaIMI and mcr-10 genes in Portugal. blaFRI-8 was detected in all E. vonholyi isolates (n = 17), located on four different IncFII(Yp) plasmids, and blaIMI-6 in an E. asburiae isolate, flanked by IS3 family transposases. E. vonholyi and the blaIMI-6-harbouring E. asburiae isolate were resistant to carbapenems. A mcr-10.1 gene was identified in an E. roggenkampii isolate on an IncFII(pECLA) plasmid. These plasmids exhibited high sequence similarity with global counterparts, indicating potential for horizontal gene transfer. Other antimicrobial resistance genes included qnrE1, sul1, and aadA2. Our findings underscore the importance of Enterobacter as vectors for AMR and the critical role of environmental compartments in its dissemination, reinforcing the importance of adopting a One Health approach to fully understand AMR dynamics. |
| format | Article |
| id | doaj-art-d5313e3c106b42c9a61df9cf2f6df17a |
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| language | English |
| publishDate | 2025-07-01 |
| publisher | Frontiers Media S.A. |
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| series | Frontiers in Microbiology |
| spelling | doaj-art-d5313e3c106b42c9a61df9cf2f6df17a2025-07-31T05:37:43ZengFrontiers Media S.A.Frontiers in Microbiology1664-302X2025-07-011610.3389/fmicb.2025.15938721593872Genomic epidemiology and resistome dynamics of Enterobacter species in a Portuguese Open Air Laboratory: the emergence of the FRI-8 carbapenemasePedro Teixeira0Miguel Ramos1Rani Rivière2Mónica Azevedo3Mónica Azevedo4Mónica Azevedo5Mário Ferreira6Maria Manuela Cano7Patrícia Vieira8Lígia Reis9Rui Matias10João Rodrigues11Carina Menezes12Tânia Rosado13António Sequeira14Olga Moreira15Werner Ruppitsch16Werner Ruppitsch17Adriana Cabal-Rosel18Solveig Sølverød Mo19Elsa Dias20Elsa Dias21Elsa Dias22Markus Woegerbauer23Manuela Caniça24Manuela Caniça25Manuela Caniça26Manuela Caniça27Vera Manageiro28Vera Manageiro29Vera Manageiro30National Reference Laboratory of Antibiotic Resistances and Healthcare Associated Infections, Department of Infectious Diseases, National Institute of Health Dr. Ricardo Jorge (INSA), Lisbon, PortugalNational Reference Laboratory of Antibiotic Resistances and Healthcare Associated Infections, Department of Infectious Diseases, National Institute of Health Dr. Ricardo Jorge (INSA), Lisbon, PortugalNational Reference Laboratory of Antibiotic Resistances and Healthcare Associated Infections, Department of Infectious Diseases, National Institute of Health Dr. Ricardo Jorge (INSA), Lisbon, PortugalNational Reference Laboratory of Antibiotic Resistances and Healthcare Associated Infections, Department of Infectious Diseases, National Institute of Health Dr. Ricardo Jorge (INSA), Lisbon, PortugalCentre for the Studies of Animal Science, Institute of Agrarian and Agri-Food Sciences and Technologies, University of Porto, Porto, PortugalAL4AnimalS, Associate Laboratory for Animal and Veterinary Sciences, Lisbon, PortugalNational Reference Laboratory of Antibiotic Resistances and Healthcare Associated Infections, Department of Infectious Diseases, National Institute of Health Dr. Ricardo Jorge (INSA), Lisbon, PortugalAir Quality Laboratory, Department of Health Environmental Health, INSA, Lisbon, PortugalNational Reference Laboratory of Antibiotic Resistances and Healthcare Associated Infections, Department of Infectious Diseases, National Institute of Health Dr. Ricardo Jorge (INSA), Lisbon, PortugalNational Reference Laboratory of Antibiotic Resistances and Healthcare Associated Infections, Department of Infectious Diseases, National Institute of Health Dr. Ricardo Jorge (INSA), Lisbon, PortugalLaboratory of Microbiology, Department of Infectious Diseases, INSA, Lisbon, PortugalLaboratory of Microbiology, Department of Infectious Diseases, INSA, Lisbon, PortugalLaboratory of Biology and Ecotoxicology, Department of Environmental Health, INSA, Lisbon, PortugalLaboratory of Biology and Ecotoxicology, Department of Environmental Health, INSA, Lisbon, PortugalStrategic Research Unit for Animal Production and Health, National Institute of Agrarian and Veterinary Research, I.P. (INIAV), Pólo de Investigação da Fonte Boa, Lisbon, PortugalStrategic Research Unit for Animal Production and Health, National Institute of Agrarian and Veterinary Research, I.P. (INIAV), Pólo de Investigação da Fonte Boa, Lisbon, PortugalAustrian Agency for Health and Food Safety, Department for Risk Assessment, Vienna, AustriaFaculty of Food Technology, Food Safety and Ecology, University of Donja Gorica, Podgorica, MontenegroAustrian Agency for Health and Food Safety, Department for Risk Assessment, Vienna, Austria0Department of Animal Health, Welfare and Food Safety, Norwegian Veterinary Institute, Ås, NorwayCentre for the Studies of Animal Science, Institute of Agrarian and Agri-Food Sciences and Technologies, University of Porto, Porto, PortugalAL4AnimalS, Associate Laboratory for Animal and Veterinary Sciences, Lisbon, PortugalLaboratory of Biology and Ecotoxicology, Department of Environmental Health, INSA, Lisbon, PortugalAustrian Agency for Health and Food Safety, Department for Risk Assessment, Vienna, AustriaNational Reference Laboratory of Antibiotic Resistances and Healthcare Associated Infections, Department of Infectious Diseases, National Institute of Health Dr. Ricardo Jorge (INSA), Lisbon, PortugalCentre for the Studies of Animal Science, Institute of Agrarian and Agri-Food Sciences and Technologies, University of Porto, Porto, PortugalAL4AnimalS, Associate Laboratory for Animal and Veterinary Sciences, Lisbon, Portugal1Faculty of Veterinary Medicine, CIISA, Center for Interdisciplinary Research in Animal Health, University of Lisbon, Lisbon, PortugalNational Reference Laboratory of Antibiotic Resistances and Healthcare Associated Infections, Department of Infectious Diseases, National Institute of Health Dr. Ricardo Jorge (INSA), Lisbon, PortugalCentre for the Studies of Animal Science, Institute of Agrarian and Agri-Food Sciences and Technologies, University of Porto, Porto, PortugalAL4AnimalS, Associate Laboratory for Animal and Veterinary Sciences, Lisbon, PortugalInterconnected reservoirs contribute to the global spread of antimicrobial resistance (AMR), including carbapenem- and colistin-resistant Enterobacterales, highlighting the need for a One Health approach. We assessed the genomic epidemiology, diversity and AMR mechanisms of Enterobacter spp. across interconnected human, animal, plant, and environmental reservoirs in a Portuguese Open Air Laboratory. Over a one year monitoring period, samples from 12 different compartments were collected and processed using selective media to isolate Enterobacter spp., which were subjected to antibiotic susceptibility testing, whole-genome sequencing and subsequent analyses to identify AMR determinants, characterize plasmids and phylogenetic relationships. We established a collection of 61 Enterobacter isolates spanning nine species and 32 sequence types, including 16 novel ones, across nine compartments (river water, wastewater, soil, manure, feed, air, farmers, pigs, wild animals), reflecting the diversity and ubiquity of Enterobacter species. Core-genome analysis revealed eight genetic clusters, suggesting clonal transmission across compartments. In total, 29 antibiotic resistance genes were detected across all isolates. Notably, this is the first documentation of blaFRI-harbouring Enterobacterales in European environmental settings and the first to describe blaFRI, blaIMI and mcr-10 genes in Portugal. blaFRI-8 was detected in all E. vonholyi isolates (n = 17), located on four different IncFII(Yp) plasmids, and blaIMI-6 in an E. asburiae isolate, flanked by IS3 family transposases. E. vonholyi and the blaIMI-6-harbouring E. asburiae isolate were resistant to carbapenems. A mcr-10.1 gene was identified in an E. roggenkampii isolate on an IncFII(pECLA) plasmid. These plasmids exhibited high sequence similarity with global counterparts, indicating potential for horizontal gene transfer. Other antimicrobial resistance genes included qnrE1, sul1, and aadA2. Our findings underscore the importance of Enterobacter as vectors for AMR and the critical role of environmental compartments in its dissemination, reinforcing the importance of adopting a One Health approach to fully understand AMR dynamics.https://www.frontiersin.org/articles/10.3389/fmicb.2025.1593872/fullEnterobacter vonholyicarbapenem-resistant Enterobacteralescolistin-resistanceFRI-8 and IMI-6 carbapenemasesMCR-10one health |
| spellingShingle | Pedro Teixeira Miguel Ramos Rani Rivière Mónica Azevedo Mónica Azevedo Mónica Azevedo Mário Ferreira Maria Manuela Cano Patrícia Vieira Lígia Reis Rui Matias João Rodrigues Carina Menezes Tânia Rosado António Sequeira Olga Moreira Werner Ruppitsch Werner Ruppitsch Adriana Cabal-Rosel Solveig Sølverød Mo Elsa Dias Elsa Dias Elsa Dias Markus Woegerbauer Manuela Caniça Manuela Caniça Manuela Caniça Manuela Caniça Vera Manageiro Vera Manageiro Vera Manageiro Genomic epidemiology and resistome dynamics of Enterobacter species in a Portuguese Open Air Laboratory: the emergence of the FRI-8 carbapenemase Frontiers in Microbiology Enterobacter vonholyi carbapenem-resistant Enterobacterales colistin-resistance FRI-8 and IMI-6 carbapenemases MCR-10 one health |
| title | Genomic epidemiology and resistome dynamics of Enterobacter species in a Portuguese Open Air Laboratory: the emergence of the FRI-8 carbapenemase |
| title_full | Genomic epidemiology and resistome dynamics of Enterobacter species in a Portuguese Open Air Laboratory: the emergence of the FRI-8 carbapenemase |
| title_fullStr | Genomic epidemiology and resistome dynamics of Enterobacter species in a Portuguese Open Air Laboratory: the emergence of the FRI-8 carbapenemase |
| title_full_unstemmed | Genomic epidemiology and resistome dynamics of Enterobacter species in a Portuguese Open Air Laboratory: the emergence of the FRI-8 carbapenemase |
| title_short | Genomic epidemiology and resistome dynamics of Enterobacter species in a Portuguese Open Air Laboratory: the emergence of the FRI-8 carbapenemase |
| title_sort | genomic epidemiology and resistome dynamics of enterobacter species in a portuguese open air laboratory the emergence of the fri 8 carbapenemase |
| topic | Enterobacter vonholyi carbapenem-resistant Enterobacterales colistin-resistance FRI-8 and IMI-6 carbapenemases MCR-10 one health |
| url | https://www.frontiersin.org/articles/10.3389/fmicb.2025.1593872/full |
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