The phylogenomic landscape of extended-spectrum β-lactamase producing Citrobacter species isolated from surface water
Abstract Background Citrobacter species are Gram-negative opportunistic pathogens commonly reported in nosocomial-acquired infections. This study characterised four Citrobacter species that were isolated from surface water in the North West Province, South Africa. Results Phenotypic antimicrobial su...
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| Format: | Article |
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BMC
2023-12-01
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| Series: | BMC Genomics |
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| Online Access: | https://doi.org/10.1186/s12864-023-09867-4 |
| _version_ | 1797398163977404416 |
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| author | Lee-Hendra Chenhaka Deidré A.B. Van Wyk Charlotte Mienie Cornelius C. Bezuidenhout Kgaugelo E. Lekota |
| author_facet | Lee-Hendra Chenhaka Deidré A.B. Van Wyk Charlotte Mienie Cornelius C. Bezuidenhout Kgaugelo E. Lekota |
| author_sort | Lee-Hendra Chenhaka |
| collection | DOAJ |
| description | Abstract Background Citrobacter species are Gram-negative opportunistic pathogens commonly reported in nosocomial-acquired infections. This study characterised four Citrobacter species that were isolated from surface water in the North West Province, South Africa. Results Phenotypic antimicrobial susceptibility profiles of the isolates demonstrated their ability to produce the extended-spectrum β-lactamase (ESBL). Whole genomes were sequenced to profile antibiotic resistance and virulence genes, as well as mobile genetic elements. In silico taxonomic identification was conducted by using multi-locus sequence typing and average nucleotide identity. A pangenome was used to determine the phylogenomic landscape of the Citrobacter species by using 109 publicly available genomes. The strains S21 and S23 were identified as C. braakii, while strains S24 and S25 were C. murliniae and C. portucalensis, respectively. Comparative genomics and sequenced genomes of the ESBL-producing isolates consisted of n = 91; 83% Citrobacter species in which bla- CMY−101 (n = 19; 32,2%) and bla- CMY−59 (n = 12; 38,7%) were prevalent in C. braakii, and C. portucalensis strains, respectively. Macrolide (acrAB-TolC, and mdtG) and aminoglycoside (acrD) efflux pumps genes were identified in the four sequenced Citrobacter spp. isolates. The quinolone resistance gene, qnrB13, was exclusive to the C. portucalensis S25 strain. In silico analysis detected plasmid replicon types IncHI1A, IncP, and Col(VCM04) in C. murliniae S24 and C. portucalensis S25, respectively. These potentially facilitate the T4SS secretion system in Citrobacter species. In this study, the C. braakii genomes could be distinguished from C. murliniae and C. portucalensis on the basis of gene encoding for cell surface localisation of the CPS (vexC) and identification of genes involved in capsule polymer synthesis (tviB and tviE). A cluster for the salmochelin siderophore system (iro-BCDEN) was found in C. murliniae S24. This is important when it comes to the pathogenicity pathway that confers an advantage in colonisation. Conclusions The emerging and genomic landscapes of these ESBL-producing Citrobacter species are of significant concern due to their dissemination potential in freshwater systems. The presence of these ESBL and multidrug-resistant (MDR) pathogens in aquatic environments is of One Health importance, since they potentially impact the clinical domain, that is, in terms of human health and the agricultural domain, that is, in terms of animal health and food production as well as the environmental domain. |
| first_indexed | 2024-03-09T01:21:44Z |
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| institution | Directory Open Access Journal |
| issn | 1471-2164 |
| language | English |
| last_indexed | 2024-03-09T01:21:44Z |
| publishDate | 2023-12-01 |
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| spelling | doaj.art-b771592cf43b4bfc9467a769bdbfdfa42023-12-10T12:08:32ZengBMCBMC Genomics1471-21642023-12-0124111510.1186/s12864-023-09867-4The phylogenomic landscape of extended-spectrum β-lactamase producing Citrobacter species isolated from surface waterLee-Hendra Chenhaka0Deidré A.B. Van Wyk1Charlotte Mienie2Cornelius C. Bezuidenhout3Kgaugelo E. Lekota4Unit for Environment Science and Management, Microbiology, North-West UniversityUnit for Environment Science and Management, Microbiology, North-West UniversityUnit for Environment Science and Management, Microbiology, North-West UniversityUnit for Environment Science and Management, Microbiology, North-West UniversityUnit for Environment Science and Management, Microbiology, North-West UniversityAbstract Background Citrobacter species are Gram-negative opportunistic pathogens commonly reported in nosocomial-acquired infections. This study characterised four Citrobacter species that were isolated from surface water in the North West Province, South Africa. Results Phenotypic antimicrobial susceptibility profiles of the isolates demonstrated their ability to produce the extended-spectrum β-lactamase (ESBL). Whole genomes were sequenced to profile antibiotic resistance and virulence genes, as well as mobile genetic elements. In silico taxonomic identification was conducted by using multi-locus sequence typing and average nucleotide identity. A pangenome was used to determine the phylogenomic landscape of the Citrobacter species by using 109 publicly available genomes. The strains S21 and S23 were identified as C. braakii, while strains S24 and S25 were C. murliniae and C. portucalensis, respectively. Comparative genomics and sequenced genomes of the ESBL-producing isolates consisted of n = 91; 83% Citrobacter species in which bla- CMY−101 (n = 19; 32,2%) and bla- CMY−59 (n = 12; 38,7%) were prevalent in C. braakii, and C. portucalensis strains, respectively. Macrolide (acrAB-TolC, and mdtG) and aminoglycoside (acrD) efflux pumps genes were identified in the four sequenced Citrobacter spp. isolates. The quinolone resistance gene, qnrB13, was exclusive to the C. portucalensis S25 strain. In silico analysis detected plasmid replicon types IncHI1A, IncP, and Col(VCM04) in C. murliniae S24 and C. portucalensis S25, respectively. These potentially facilitate the T4SS secretion system in Citrobacter species. In this study, the C. braakii genomes could be distinguished from C. murliniae and C. portucalensis on the basis of gene encoding for cell surface localisation of the CPS (vexC) and identification of genes involved in capsule polymer synthesis (tviB and tviE). A cluster for the salmochelin siderophore system (iro-BCDEN) was found in C. murliniae S24. This is important when it comes to the pathogenicity pathway that confers an advantage in colonisation. Conclusions The emerging and genomic landscapes of these ESBL-producing Citrobacter species are of significant concern due to their dissemination potential in freshwater systems. The presence of these ESBL and multidrug-resistant (MDR) pathogens in aquatic environments is of One Health importance, since they potentially impact the clinical domain, that is, in terms of human health and the agricultural domain, that is, in terms of animal health and food production as well as the environmental domain.https://doi.org/10.1186/s12864-023-09867-4ESBL-producing CitrobacterWhole-genome sequencingAntibiotic resistanceSurface water |
| spellingShingle | Lee-Hendra Chenhaka Deidré A.B. Van Wyk Charlotte Mienie Cornelius C. Bezuidenhout Kgaugelo E. Lekota The phylogenomic landscape of extended-spectrum β-lactamase producing Citrobacter species isolated from surface water BMC Genomics ESBL-producing Citrobacter Whole-genome sequencing Antibiotic resistance Surface water |
| title | The phylogenomic landscape of extended-spectrum β-lactamase producing Citrobacter species isolated from surface water |
| title_full | The phylogenomic landscape of extended-spectrum β-lactamase producing Citrobacter species isolated from surface water |
| title_fullStr | The phylogenomic landscape of extended-spectrum β-lactamase producing Citrobacter species isolated from surface water |
| title_full_unstemmed | The phylogenomic landscape of extended-spectrum β-lactamase producing Citrobacter species isolated from surface water |
| title_short | The phylogenomic landscape of extended-spectrum β-lactamase producing Citrobacter species isolated from surface water |
| title_sort | phylogenomic landscape of extended spectrum β lactamase producing citrobacter species isolated from surface water |
| topic | ESBL-producing Citrobacter Whole-genome sequencing Antibiotic resistance Surface water |
| url | https://doi.org/10.1186/s12864-023-09867-4 |
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