Comparative genomic analyses of the clinically-derived Winkia strain NY0527: the reassignment of W. neuii subsp. neuii and W. neuii subsp. antitratus into two separate species and insights into their virulence characteristics
BackgroundWinkia neuii, previously known as Actinomyces neuii, is increasingly recognized as a causative agent of various human infections, while its taxonomy and genomic insights are still understudied.MethodsA Winkia strain NY0527 was isolated from the hip abscess of a patient, and its antibiotic...
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Frontiers Media S.A.
2023-04-01
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| Series: | Frontiers in Microbiology |
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| Online Access: | https://www.frontiersin.org/articles/10.3389/fmicb.2023.1147469/full |
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| author | Xunchao Cai Yao Peng Meng Li Yifeng Qiu Yuhan Wang Long Xu Qi Hou Qi Hou |
| author_facet | Xunchao Cai Yao Peng Meng Li Yifeng Qiu Yuhan Wang Long Xu Qi Hou Qi Hou |
| author_sort | Xunchao Cai |
| collection | DOAJ |
| description | BackgroundWinkia neuii, previously known as Actinomyces neuii, is increasingly recognized as a causative agent of various human infections, while its taxonomy and genomic insights are still understudied.MethodsA Winkia strain NY0527 was isolated from the hip abscess of a patient, and its antibiotic susceptibility was assessed. The genome was hybrid assembled from long-reads and short-reads sequencing. Whole-genome-based analyses on taxa assignment, strain diversity, and pathogenesis were conducted.ResultsThe strain was found to be highly susceptible to beta-lactam antibiotics, but resistant to erythromycin, clindamycin, and amikacin. The complete genome sequences of this strain were assembled and found to consist of a circular chromosome and a circular plasmid. Sequence alignment to the NCBI-nt database revealed that the plasmid had high sequence identity (>90%) to four Corynebacterium plasmids, with 40–50% query sequence coverage. Furthermore, the plasmid was discovered to possibly originate from the sequence recombination events of two Corynebacterium plasmid families. Phylogenomic tree and genomic average nucleotide identity analyses indicated that many Winkia sp. strains were still erroneously assigned as Actinomyces sp. strains, and the documented subspecies within W. neuii should be reclassified as two separate species (i.e., W. neuii and W. anitratus). The core genome of each species carried a chromosome-coded beta-lactamase expression repressor gene, which may account for their broadly observed susceptibility to beta-lactam antibiotics in clinical settings. Additionally, an ermX gene that expresses fluoroquinolone resistance was shared by some W. neuii and W. anitratus strains, possibly acquired by IS6 transposase-directed gene transfer events. In contrast, tetracycline resistance genes were exclusively carried by W. neuii strains. In particular, W. neuii was found to be more pathogenic than W. anitratus by encoding more virulence factors (i.e., 35–38 in W. neuii vs 27–31 in W. anitratus). Moreover, both species encoded two core pathogenic virulence factors, namely hemolysin and sialidase, which may facilitate their infections by expressing poreformation, adhesion, and immunoglobulin deglycosylation activities.ConclusionThis study highlights the underappreciated taxonomic diversity of Winkia spp. and provides populational genomic insights into their antibiotic susceptibility and pathogenesis for the first time, which could be helpful in the clinical diagnosis and treatment of Winkia spp. infections. |
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| last_indexed | 2024-04-09T17:02:14Z |
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| spelling | doaj.art-98cf1939c6d8477ca34d62ade069e48f2023-04-21T04:36:50ZengFrontiers Media S.A.Frontiers in Microbiology1664-302X2023-04-011410.3389/fmicb.2023.11474691147469Comparative genomic analyses of the clinically-derived Winkia strain NY0527: the reassignment of W. neuii subsp. neuii and W. neuii subsp. antitratus into two separate species and insights into their virulence characteristicsXunchao Cai0Yao Peng1Meng Li2Yifeng Qiu3Yuhan Wang4Long Xu5Qi Hou6Qi Hou7Department of Gastroenterology and Hepatology, Shenzhen University General Hospital, Shenzhen University, Shenzhen, ChinaDepartment of Gastroenterology and Hepatology, Shenzhen University General Hospital, Shenzhen University, Shenzhen, ChinaDepartment of Laboratory Medicine, Shenzhen University General Hospital, Shenzhen University, Shenzhen, ChinaDepartment of Urology, Shenzhen University General Hospital, Shenzhen University, Shenzhen, ChinaDepartment of Urology, Shenzhen University General Hospital, Shenzhen University, Shenzhen, ChinaDepartment of Gastroenterology and Hepatology, Shenzhen University General Hospital, Shenzhen University, Shenzhen, ChinaDepartment of Urology, Shenzhen University General Hospital, Shenzhen University, Shenzhen, ChinaInternational Cancer Center, Shenzhen Key Laboratory, Hematology Institution of Shenzhen University, Shenzhen, ChinaBackgroundWinkia neuii, previously known as Actinomyces neuii, is increasingly recognized as a causative agent of various human infections, while its taxonomy and genomic insights are still understudied.MethodsA Winkia strain NY0527 was isolated from the hip abscess of a patient, and its antibiotic susceptibility was assessed. The genome was hybrid assembled from long-reads and short-reads sequencing. Whole-genome-based analyses on taxa assignment, strain diversity, and pathogenesis were conducted.ResultsThe strain was found to be highly susceptible to beta-lactam antibiotics, but resistant to erythromycin, clindamycin, and amikacin. The complete genome sequences of this strain were assembled and found to consist of a circular chromosome and a circular plasmid. Sequence alignment to the NCBI-nt database revealed that the plasmid had high sequence identity (>90%) to four Corynebacterium plasmids, with 40–50% query sequence coverage. Furthermore, the plasmid was discovered to possibly originate from the sequence recombination events of two Corynebacterium plasmid families. Phylogenomic tree and genomic average nucleotide identity analyses indicated that many Winkia sp. strains were still erroneously assigned as Actinomyces sp. strains, and the documented subspecies within W. neuii should be reclassified as two separate species (i.e., W. neuii and W. anitratus). The core genome of each species carried a chromosome-coded beta-lactamase expression repressor gene, which may account for their broadly observed susceptibility to beta-lactam antibiotics in clinical settings. Additionally, an ermX gene that expresses fluoroquinolone resistance was shared by some W. neuii and W. anitratus strains, possibly acquired by IS6 transposase-directed gene transfer events. In contrast, tetracycline resistance genes were exclusively carried by W. neuii strains. In particular, W. neuii was found to be more pathogenic than W. anitratus by encoding more virulence factors (i.e., 35–38 in W. neuii vs 27–31 in W. anitratus). Moreover, both species encoded two core pathogenic virulence factors, namely hemolysin and sialidase, which may facilitate their infections by expressing poreformation, adhesion, and immunoglobulin deglycosylation activities.ConclusionThis study highlights the underappreciated taxonomic diversity of Winkia spp. and provides populational genomic insights into their antibiotic susceptibility and pathogenesis for the first time, which could be helpful in the clinical diagnosis and treatment of Winkia spp. infections.https://www.frontiersin.org/articles/10.3389/fmicb.2023.1147469/fullabscessWinkia neuiibacterial infectionscomplete genomevirulence traits |
| spellingShingle | Xunchao Cai Yao Peng Meng Li Yifeng Qiu Yuhan Wang Long Xu Qi Hou Qi Hou Comparative genomic analyses of the clinically-derived Winkia strain NY0527: the reassignment of W. neuii subsp. neuii and W. neuii subsp. antitratus into two separate species and insights into their virulence characteristics Frontiers in Microbiology abscess Winkia neuii bacterial infections complete genome virulence traits |
| title | Comparative genomic analyses of the clinically-derived Winkia strain NY0527: the reassignment of W. neuii subsp. neuii and W. neuii subsp. antitratus into two separate species and insights into their virulence characteristics |
| title_full | Comparative genomic analyses of the clinically-derived Winkia strain NY0527: the reassignment of W. neuii subsp. neuii and W. neuii subsp. antitratus into two separate species and insights into their virulence characteristics |
| title_fullStr | Comparative genomic analyses of the clinically-derived Winkia strain NY0527: the reassignment of W. neuii subsp. neuii and W. neuii subsp. antitratus into two separate species and insights into their virulence characteristics |
| title_full_unstemmed | Comparative genomic analyses of the clinically-derived Winkia strain NY0527: the reassignment of W. neuii subsp. neuii and W. neuii subsp. antitratus into two separate species and insights into their virulence characteristics |
| title_short | Comparative genomic analyses of the clinically-derived Winkia strain NY0527: the reassignment of W. neuii subsp. neuii and W. neuii subsp. antitratus into two separate species and insights into their virulence characteristics |
| title_sort | comparative genomic analyses of the clinically derived winkia strain ny0527 the reassignment of w neuii subsp neuii and w neuii subsp antitratus into two separate species and insights into their virulence characteristics |
| topic | abscess Winkia neuii bacterial infections complete genome virulence traits |
| url | https://www.frontiersin.org/articles/10.3389/fmicb.2023.1147469/full |
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