Genome Analysis and Antibiofilm Activity of Phage 590B against Multidrug-Resistant and Extensively Drug-Resistant Uropathogenic <i>Escherichia coli</i> Isolates, India
Urinary tract infections (UTIs) are among the most common bacterial infections in humans. Uropathogenic <i>Escherichia coli</i> (UPEC), which are the most frequent agents causing community as well as hospital-acquired UTIs, have become highly drug-resistant, thus making the treatment of...
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MDPI AG
2022-11-01
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| Series: | Pathogens |
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| author | Naveen Chaudhary Ravi Kumar Maurya Dharminder Singh Balvinder Mohan Neelam Taneja |
| author_facet | Naveen Chaudhary Ravi Kumar Maurya Dharminder Singh Balvinder Mohan Neelam Taneja |
| author_sort | Naveen Chaudhary |
| collection | DOAJ |
| description | Urinary tract infections (UTIs) are among the most common bacterial infections in humans. Uropathogenic <i>Escherichia coli</i> (UPEC), which are the most frequent agents causing community as well as hospital-acquired UTIs, have become highly drug-resistant, thus making the treatment of these infections challenging. Recently, the use of bacteriophages (or ‘phages’) against multidrug-resistant (MDR) and extensively drug-resistant (XDR) microorganisms has garnered significant global attention. Bacterial biofilms play a vital role in the pathogenesis of UTIs caused by UPEC. Phages have the potential to disrupt bacterial biofilms using lytic enzymes such as EPS depolymerases and endolysins. We isolated a lytic phage (590B) from community sewage in Chandigarh, which was active against multiple MDR and XDR biofilm-forming UPEC strains. During whole-genome sequencing, the 44.3 kb long genome of phage 590B encoded 75 ORFs, of which 40 were functionally annotated based on homology with similar phage proteins in the database. Comparative analysis of associated phage genomes indicated that phage 590B evolved independently and had a distinct taxonomic position within the genus <i>Kagunavirus</i> in the subfamily <i>Guernseyvirinae</i> of <i>Siphoviridae</i>. The phage disrupted biofilm mass effectively when applied to 24 h old biofilms formed on the Foley silicon catheter and coverslip biofilm models. To study the effect of intact biofilm architecture on phage predation, the biofilms were disrupted. The phage reduced the viable cells by 0.6–1.0 order of magnitude after 24 h of incubation. Regrowth and intact bacterial cells were observed in the phage-treated planktonic culture and biofilms, respectively, which indicated the emergence of phage-resistant bacterial variants. The phage genome encoded an endolysin which might have a role in the disruption and inhibition of bacterial biofilms. Moreover, the genome lacked genes encoding toxins, virulence factors, antibiotic resistance, or lysogeny. Therefore, lytic phage 590B may be a good alternative to antibiotics and can be included in phage cocktails for the treatment of UTIs caused by biofilm-forming MDR and XDR UPEC strains. |
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| language | English |
| last_indexed | 2024-03-09T15:59:18Z |
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| spelling | doaj.art-5e541301847a4144884540f842edc0a22023-11-24T17:12:53ZengMDPI AGPathogens2076-08172022-11-011112144810.3390/pathogens11121448Genome Analysis and Antibiofilm Activity of Phage 590B against Multidrug-Resistant and Extensively Drug-Resistant Uropathogenic <i>Escherichia coli</i> Isolates, IndiaNaveen Chaudhary0Ravi Kumar Maurya1Dharminder Singh2Balvinder Mohan3Neelam Taneja4Department of Medical Microbiology, Postgraduate Institute of Medical Education and Research (PGIMER), Chandigarh 160012, IndiaDepartment of Medical Microbiology, Postgraduate Institute of Medical Education and Research (PGIMER), Chandigarh 160012, IndiaDepartment of Medical Microbiology, Postgraduate Institute of Medical Education and Research (PGIMER), Chandigarh 160012, IndiaDepartment of Medical Microbiology, Postgraduate Institute of Medical Education and Research (PGIMER), Chandigarh 160012, IndiaDepartment of Medical Microbiology, Postgraduate Institute of Medical Education and Research (PGIMER), Chandigarh 160012, IndiaUrinary tract infections (UTIs) are among the most common bacterial infections in humans. Uropathogenic <i>Escherichia coli</i> (UPEC), which are the most frequent agents causing community as well as hospital-acquired UTIs, have become highly drug-resistant, thus making the treatment of these infections challenging. Recently, the use of bacteriophages (or ‘phages’) against multidrug-resistant (MDR) and extensively drug-resistant (XDR) microorganisms has garnered significant global attention. Bacterial biofilms play a vital role in the pathogenesis of UTIs caused by UPEC. Phages have the potential to disrupt bacterial biofilms using lytic enzymes such as EPS depolymerases and endolysins. We isolated a lytic phage (590B) from community sewage in Chandigarh, which was active against multiple MDR and XDR biofilm-forming UPEC strains. During whole-genome sequencing, the 44.3 kb long genome of phage 590B encoded 75 ORFs, of which 40 were functionally annotated based on homology with similar phage proteins in the database. Comparative analysis of associated phage genomes indicated that phage 590B evolved independently and had a distinct taxonomic position within the genus <i>Kagunavirus</i> in the subfamily <i>Guernseyvirinae</i> of <i>Siphoviridae</i>. The phage disrupted biofilm mass effectively when applied to 24 h old biofilms formed on the Foley silicon catheter and coverslip biofilm models. To study the effect of intact biofilm architecture on phage predation, the biofilms were disrupted. The phage reduced the viable cells by 0.6–1.0 order of magnitude after 24 h of incubation. Regrowth and intact bacterial cells were observed in the phage-treated planktonic culture and biofilms, respectively, which indicated the emergence of phage-resistant bacterial variants. The phage genome encoded an endolysin which might have a role in the disruption and inhibition of bacterial biofilms. Moreover, the genome lacked genes encoding toxins, virulence factors, antibiotic resistance, or lysogeny. Therefore, lytic phage 590B may be a good alternative to antibiotics and can be included in phage cocktails for the treatment of UTIs caused by biofilm-forming MDR and XDR UPEC strains.https://www.mdpi.com/2076-0817/11/12/1448phage therapyurinary tract infectionsphage cocktailmultidrug resistanceuropathogenic <i>Escherichia coli</i> |
| spellingShingle | Naveen Chaudhary Ravi Kumar Maurya Dharminder Singh Balvinder Mohan Neelam Taneja Genome Analysis and Antibiofilm Activity of Phage 590B against Multidrug-Resistant and Extensively Drug-Resistant Uropathogenic <i>Escherichia coli</i> Isolates, India Pathogens phage therapy urinary tract infections phage cocktail multidrug resistance uropathogenic <i>Escherichia coli</i> |
| title | Genome Analysis and Antibiofilm Activity of Phage 590B against Multidrug-Resistant and Extensively Drug-Resistant Uropathogenic <i>Escherichia coli</i> Isolates, India |
| title_full | Genome Analysis and Antibiofilm Activity of Phage 590B against Multidrug-Resistant and Extensively Drug-Resistant Uropathogenic <i>Escherichia coli</i> Isolates, India |
| title_fullStr | Genome Analysis and Antibiofilm Activity of Phage 590B against Multidrug-Resistant and Extensively Drug-Resistant Uropathogenic <i>Escherichia coli</i> Isolates, India |
| title_full_unstemmed | Genome Analysis and Antibiofilm Activity of Phage 590B against Multidrug-Resistant and Extensively Drug-Resistant Uropathogenic <i>Escherichia coli</i> Isolates, India |
| title_short | Genome Analysis and Antibiofilm Activity of Phage 590B against Multidrug-Resistant and Extensively Drug-Resistant Uropathogenic <i>Escherichia coli</i> Isolates, India |
| title_sort | genome analysis and antibiofilm activity of phage 590b against multidrug resistant and extensively drug resistant uropathogenic i escherichia coli i isolates india |
| topic | phage therapy urinary tract infections phage cocktail multidrug resistance uropathogenic <i>Escherichia coli</i> |
| url | https://www.mdpi.com/2076-0817/11/12/1448 |
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