Genomic characterization of a multidrug-resistant uropathogenic <i>Escherichia coli</i> and evaluation of <i>Echeveria</i> plant extracts as antibacterials

Ana M. Castañeda-Meléndrez; José A. Magaña-Lizárraga; Marcela Martínez-Valenzuela; Aldo F. Clemente-Soto; Patricia C. García-Cervantes; Francisco Delgado-Vargas; Rodolfo Bernal-Reynaga; Ana M. Castañeda-Meléndrez; José A. Magaña-Lizárraga; Marcela Martínez-Valenzuela; Aldo F. Clemente-Soto; Patricia C. García-Cervantes; Francisco Delgado-Vargas; Rodolfo Bernal-Reynaga

doi:10.3934/microbiol.2024003

AIMS Microbiology

2024, Volume 10, Issue 1: 41-61. doi: 10.3934/microbiol.2024003

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Research article

Genomic characterization of a multidrug-resistant uropathogenic Escherichia coli and evaluation of Echeveria plant extracts as antibacterials

Unidad de Investigaciones en Salud Pública “Dra. Kaethe Willms”, Facultad de Ciencias Químico-Biológicas. Universidad Autónoma de Sinaloa. Ciudad Universitaria, Culiacán, Sinaloa, México
These two authors contributed equally

Received: 27 October 2023 Revised: 22 December 2023 Accepted: 10 January 2024 Published: 17 January 2024

Uropathogenic Escherichia coli (UPEC) is the most common bacterial agent associated with urinary tract infections, threatening public health systems with elevated medical costs and high morbidity rates. The successful establishment of the infection is associated with virulence factors encoded in its genome, in addition to antibacterial resistance genes, which could limit the treatment and resolution of the infection. In this sense, plant extracts from the genus Echeveria have traditionally been used to treat diverse infectious diseases. However, little is known about the effects of these extracts on bacteria and their potential mechanisms of action. This study aims to sequence a multidrug-resistant UPEC isolate (UTI-U7) and assess the multilocus sequence typing (MLST), virulence factors, antimicrobial resistance profile, genes, serotype, and plasmid content. Antimicrobial susceptibility profiling was performed using the Kirby-Bauer disk diffusion. The antibacterial and anti-adherent effects of the methanol extracts (ME) of Echeveria (E. craigiana, E. kimnachii, and E. subrigida) against UTI-U7 were determined. The isolate was characterized as an O25:H4-B2-ST2279-CH40 subclone and had resistant determinants to aminoglycosides, β-lactams, fluoroquinolones/quinolones, amphenicols, and tetracyclines, which matched with the antimicrobial resistance profile. The virulence genes identified encode adherence factors, iron uptake, protectins/serum resistance, and toxins. Identified plasmids belonged to the IncF group (IncFIA, IncFIB, and IncFII), alongside several prophage-like elements. After an extensive genome analysis that confirmed the pathogenic status of UTI-U7 isolate, Echeveria extracts were tested to determine their antibacterial effects; as an extract, E. subrigida (MIC, 5 mg/mL) displayed the best inhibitory effect. However, the adherence between UTI-U7 and HeLa cells was unaffected by the ME of the E. subrigida extract.
- Uropathogenic Escherichia coli,
- multidrug resistance,
- genome sequencing,
- Echeveria extract,
- antibacterial effect,
- bacterial adherence
Citation: Ana M. Castañeda-Meléndrez, José A. Magaña-Lizárraga, Marcela Martínez-Valenzuela, Aldo F. Clemente-Soto, Patricia C. García-Cervantes, Francisco Delgado-Vargas, Rodolfo Bernal-Reynaga. Genomic characterization of a multidrug-resistant uropathogenic Escherichia coli and evaluation of Echeveria plant extracts as antibacterials[J]. AIMS Microbiology, 2024, 10(1): 41-61. doi: 10.3934/microbiol.2024003

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Abstract

Uropathogenic Escherichia coli (UPEC) is the most common bacterial agent associated with urinary tract infections, threatening public health systems with elevated medical costs and high morbidity rates. The successful establishment of the infection is associated with virulence factors encoded in its genome, in addition to antibacterial resistance genes, which could limit the treatment and resolution of the infection. In this sense, plant extracts from the genus Echeveria have traditionally been used to treat diverse infectious diseases. However, little is known about the effects of these extracts on bacteria and their potential mechanisms of action. This study aims to sequence a multidrug-resistant UPEC isolate (UTI-U7) and assess the multilocus sequence typing (MLST), virulence factors, antimicrobial resistance profile, genes, serotype, and plasmid content. Antimicrobial susceptibility profiling was performed using the Kirby-Bauer disk diffusion. The antibacterial and anti-adherent effects of the methanol extracts (ME) of Echeveria (E. craigiana, E. kimnachii, and E. subrigida) against UTI-U7 were determined. The isolate was characterized as an O25:H4-B2-ST2279-CH40 subclone and had resistant determinants to aminoglycosides, β-lactams, fluoroquinolones/quinolones, amphenicols, and tetracyclines, which matched with the antimicrobial resistance profile. The virulence genes identified encode adherence factors, iron uptake, protectins/serum resistance, and toxins. Identified plasmids belonged to the IncF group (IncFIA, IncFIB, and IncFII), alongside several prophage-like elements. After an extensive genome analysis that confirmed the pathogenic status of UTI-U7 isolate, Echeveria extracts were tested to determine their antibacterial effects; as an extract, E. subrigida (MIC, 5 mg/mL) displayed the best inhibitory effect. However, the adherence between UTI-U7 and HeLa cells was unaffected by the ME of the E. subrigida extract.

Acknowledgments

We would like to thank to Programa de Fomento y Apoyo a Proyectos de Investigación (PROFAPI) 2022 of the Universidad Autónoma de Sinaloa grant number PRO_A2_006 for the financial support of this work. Also, we thank to M.Sc. Yesmi Ahumada, Dr. Gabriela López, Dr. Samuel López and Dr. Carolina Murúa for technical assessment during antibacterial assays, extracts preparation and adherence assays, respectively.

Conflict of interest

All authors declare no conflicts of interest in this paper.

Author contributions

Marcela Martínez, Patricia García, Francisco Delgado, Aldo Clemente and Rodolfo Bernal contributed to the conceptualization and design of the study. Ana Castañeda, Antonio Magaña and Patricia García performed the experiments, organized and analyzed data. Ana Castañeda and Antonio Magaña wrote the first draft of the article. Patricia García, Francisco Delgado and Rodolfo Bernal revised the draft and corrected the sections of the manuscript. Marcela Martínez, Aldo Clemente and Rodolfo Bernal administrated the project. All authors contributed to manuscript revision, read, and approved the submitted version.

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