Characterization of holins, the membrane proteins of coliphage ASEC2201: a genomewide in silico approach

Drug-resistant Escherichia coli poses a significant healthcare burden, driving the search for novel antimicrobials. We have previously done the isolation and whole-genome sequencing of ASEC2201, a novel coliphage derived from multidrug-resistant clinical E. coli strains. Here, we report the identifi...

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Main Authors: Humaira Saeed, Sudhaker Padmesh, Aditi Singh, Sujeet Pratap Singh, Mohammed Haris Siddiqui, Manodeep Sen, Imran Hussain, Mirza Masroor Ali Beg
Format: Article
Language:English
Published: Frontiers Media S.A. 2025-07-01
Series:Frontiers in Microbiology
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Online Access:https://www.frontiersin.org/articles/10.3389/fmicb.2025.1550594/full
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author Humaira Saeed
Sudhaker Padmesh
Aditi Singh
Sujeet Pratap Singh
Mohammed Haris Siddiqui
Manodeep Sen
Imran Hussain
Mirza Masroor Ali Beg
author_facet Humaira Saeed
Sudhaker Padmesh
Aditi Singh
Sujeet Pratap Singh
Mohammed Haris Siddiqui
Manodeep Sen
Imran Hussain
Mirza Masroor Ali Beg
author_sort Humaira Saeed
collection DOAJ
description Drug-resistant Escherichia coli poses a significant healthcare burden, driving the search for novel antimicrobials. We have previously done the isolation and whole-genome sequencing of ASEC2201, a novel coliphage derived from multidrug-resistant clinical E. coli strains. Here, we report the identification and characterization of phage enzyme, holin by in silico approaches. Genome annotation using Prokka identified three putative holin genes (PROKKA_03659, PROKKA_04292, and PROKKA_04422) belonging to the Phage_holin_2_1 superfamily. Upstream promoter prediction revealed active regulatory elements at positions 112, 177, and 186 for these genes, indicating robust transcriptional activity. Transmembrane topology analysis using DeepTMHMM confirmed the presence of two to three α-helical membrane-spanning domains in each holin, essential for pore formation. Homology modeling with SWISS-MODEL yielded high-confidence three-dimensional structures characterized by conserved membrane-anchoring motifs, as supported by QMEAN and GMQE quality scores. In silico identification of cell-penetrating peptide motifs within the holin sequences suggests potential for enhanced intracellular delivery in CPP-fusion therapeutic constructs. Overall, our in-depth analysis elucidates the structural and functional properties of ASEC2201 holins, underscoring their biotechnological significance as scaffolds for developing novel antimicrobial strategies against MDR E. coli. It gives us an understanding on how the holins, with their inherent membrane-disrupting functions, can be explored in detail for future use as lysis modules in programmable bacterial systems, while their identified CPP motifs offer additional potential for engineering targeted therapeutic delivery vehicles. This study also demonstrates the potential of integrative in silico approaches in developing a comprehensive foundation for future experimental validation for proteins with no prior functional annotation.
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spelling doaj-art-ad7fbe00dfb74c0bb51d42dd87f564c12025-08-20T02:40:15ZengFrontiers Media S.A.Frontiers in Microbiology1664-302X2025-07-011610.3389/fmicb.2025.15505941550594Characterization of holins, the membrane proteins of coliphage ASEC2201: a genomewide in silico approachHumaira Saeed0Sudhaker Padmesh1Aditi Singh2Sujeet Pratap Singh3Mohammed Haris Siddiqui4Manodeep Sen5Imran Hussain6Mirza Masroor Ali Beg7Amity Institute of Biotechnology, Amity University Uttar Pradesh, Lucknow Campus, Lucknow, IndiaAmity Institute of Biotechnology, Amity University Uttar Pradesh, Lucknow Campus, Lucknow, IndiaAmity Institute of Biotechnology, Amity University Uttar Pradesh, Lucknow Campus, Lucknow, IndiaAmity Institute of Biotechnology, Amity University Uttar Pradesh, Lucknow Campus, Lucknow, IndiaDr. Ram Manohar Lohia Institute of Medical Sciences, Lucknow, IndiaIntegral Institute of Agricultural Science and Technology, Integral University, Lucknow, IndiaDepartment of Bioengineering, Faculty of Engineering and Information Technology, Integral University, Lucknow, IndiaFaculty of Medicine, Alatoo International University, Bishkek, KyrgyzstanDrug-resistant Escherichia coli poses a significant healthcare burden, driving the search for novel antimicrobials. We have previously done the isolation and whole-genome sequencing of ASEC2201, a novel coliphage derived from multidrug-resistant clinical E. coli strains. Here, we report the identification and characterization of phage enzyme, holin by in silico approaches. Genome annotation using Prokka identified three putative holin genes (PROKKA_03659, PROKKA_04292, and PROKKA_04422) belonging to the Phage_holin_2_1 superfamily. Upstream promoter prediction revealed active regulatory elements at positions 112, 177, and 186 for these genes, indicating robust transcriptional activity. Transmembrane topology analysis using DeepTMHMM confirmed the presence of two to three α-helical membrane-spanning domains in each holin, essential for pore formation. Homology modeling with SWISS-MODEL yielded high-confidence three-dimensional structures characterized by conserved membrane-anchoring motifs, as supported by QMEAN and GMQE quality scores. In silico identification of cell-penetrating peptide motifs within the holin sequences suggests potential for enhanced intracellular delivery in CPP-fusion therapeutic constructs. Overall, our in-depth analysis elucidates the structural and functional properties of ASEC2201 holins, underscoring their biotechnological significance as scaffolds for developing novel antimicrobial strategies against MDR E. coli. It gives us an understanding on how the holins, with their inherent membrane-disrupting functions, can be explored in detail for future use as lysis modules in programmable bacterial systems, while their identified CPP motifs offer additional potential for engineering targeted therapeutic delivery vehicles. This study also demonstrates the potential of integrative in silico approaches in developing a comprehensive foundation for future experimental validation for proteins with no prior functional annotation.https://www.frontiersin.org/articles/10.3389/fmicb.2025.1550594/fulltransmembrane domainphage-mediated lysisASEC2201protein 3D structurefunctional annotationholins
spellingShingle Humaira Saeed
Sudhaker Padmesh
Aditi Singh
Sujeet Pratap Singh
Mohammed Haris Siddiqui
Manodeep Sen
Imran Hussain
Mirza Masroor Ali Beg
Characterization of holins, the membrane proteins of coliphage ASEC2201: a genomewide in silico approach
Frontiers in Microbiology
transmembrane domain
phage-mediated lysis
ASEC2201
protein 3D structure
functional annotation
holins
title Characterization of holins, the membrane proteins of coliphage ASEC2201: a genomewide in silico approach
title_full Characterization of holins, the membrane proteins of coliphage ASEC2201: a genomewide in silico approach
title_fullStr Characterization of holins, the membrane proteins of coliphage ASEC2201: a genomewide in silico approach
title_full_unstemmed Characterization of holins, the membrane proteins of coliphage ASEC2201: a genomewide in silico approach
title_short Characterization of holins, the membrane proteins of coliphage ASEC2201: a genomewide in silico approach
title_sort characterization of holins the membrane proteins of coliphage asec2201 a genomewide in silico approach
topic transmembrane domain
phage-mediated lysis
ASEC2201
protein 3D structure
functional annotation
holins
url https://www.frontiersin.org/articles/10.3389/fmicb.2025.1550594/full
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