Does Phage Therapy Need a Pan-Phage?
Abstract
:1. Introduction
2. Host Range Determination Starts with the Initiation of Infection
2.1. Cell Surface Receptors of Bacteriophages
2.2. Receptors Located in the Cell Walls of Gram-Positive Bacteria
2.3. Receptors Located in the Cell Walls of Gram-Negative Bacteria
2.4. Receptors in Additional Structures of Gram-Positive and Gram-Negative Bacteria
3. How Broad the Host Range Can Be
4. Human Tract Infections from the Host Range’s Point of View
4.1. Urinary Tract Infections (UTIs)
- (a)
- There was a long-standing belief that the bladder and urethra of healthy individuals are devoid of bacteria or contain insufficient numbers to cause infections; however, recent reports have demonstrated the presence of numerous microorganisms in the bladder of healthy adults without clinical manifestations [119,120]. Further research is required to determine the significance and contribution of these microorganisms to health and disease [119,120].
- (b)
- UTIs are frequently caused by bacterial biofilms, which account for approximately 65% of nosocomial infections and 80% of all microbial infections [121]. Diverse bacteria disperse biofilms via a variety of mechanisms during their transmission [122]. Biofilms are also found within host cells, where they establish intracellular bacterial communities (IBCs) that serve as a protective barrier against neutrophils and antibiotics, thereby significantly contributing to the progression of recurrent urinary tract infections [123]. Specifically, in cases of catheter-associated UTIs (CAUTIs), which comprise 40% of all hospital-acquired infections, bacterial biofilms have a substantial effect on the development of UTIs [124]. Urothelium, prostate stones, and implanted biomedical devices are all potential sites for biofilm formation caused by both Gram-positive and Gram-negative bacteria [125]. In the early stages of CAUTIs, biofilms are often colonized by a single species; this is followed by the development of mixed communities, leading to the formation of a thick biofilm that renders antibiotic therapy ineffective [125].
4.2. Respiratory Tract Infections
4.3. Gastrointestinal Tract Infections
5. Broad-Range Phages Should Be Either Made by Expansion or by Synthetic Biology
5.1. (A) Methods for the Experimental Expansion of the Host Range
5.1.1. Single Phage Adaptation to a New Host (Examples of Host Range Expansion within Species)
5.1.2. Generating Phage Cocktails of Better Efficacy through Experimental Adaptation
5.2. (B) Expanding Host Range by Phage Engineering and Reverse Genetics
6. Conclusions
Author Contributions
Funding
Institutional Review Board Statement
Informed Consent Statement
Data Availability Statement
Acknowledgments
Conflicts of Interest
References
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A. Host Range to the Level of Species (Host Range Class I) | |||||
---|---|---|---|---|---|
Phage | Host | Host Range Results | Receptors | Family | Refs |
vB_Sau_Clo6 and vB_Sau_CG | Staphylococcus aureus RN4220 strain | High killing activity (89% and 81%, respectively) against 44 isolated strains and 3 reference strains, including 11 MRSAs. The activity was comparable to that of the broad-range staphylophage K. | The bioinformatics analysis of the RBP genes provided no explanation. | Myoviridae | [91,92] |
vB_SPuM_SP116 | Salmonella Pullorum SPu-116 | Broad lytic spectrum, infecting 27 out of 37 strains/several Salmonella strains, including 9 serotypes (Pullorum, Enteritidis, Indiana, Typhimurium, Infantis, Montevideo Heidelberg, Paratyphi A, Derby, and clinical isolates). However, there was no effect on other species of Enterobacteriaceae. | The authors speculated that the receptors of the SP116, like other Salmonella phages, including Felix O1, are located on the LPS, where different phages might bind with different moieties of the LPS. | Myoviridae | [93,94] |
φMR003 | Staphylococcus aureus RN4220 strain: Transformable strain, restriction-deficient (hsdR−), rsbU, agr- | Broad host range against 101 out of 104 (97%) MRSA clinical strains, broader than phages φSA012 (73%) and φΜR003 (57%). | Using bacterial deletion mutants and in silico analysis of φΜR003, the researchers suggested that the combined action of potential viral proteins contributes to a wide host range. Specifically, RBP belonging to the baseplate and tail proteins (ORF103) bind to the α-GlcNAc residues of RboP-WTA and to the WTA backbone (ORF105) of S. aureus, whereas the expression of a peptidoglycan hydrolase (ORF104) facilitates the infection. | Herelleviridae and Silviavirus | [95] |
vB_EfaS_Hef13 | 12 Enterococcus faecalis strains | Broader host spectrum than previously isolated E.faecalis lytic phages. Successfully infected 12 out of 17 clinical strains of E. faecalis but not E. faecium reference strains. | Host range may be attributed to the presence of two ORFs (ORF55 and ORF75), which code for the receptor-binding protein in the phage tail apparatus, and a DNA methyltransferase, which protects phages from the bacterial restriction-modification system. On the other side of the host, a broader spectrum of HEf13 appeared to be associated with the potential receptor, the bacterial cell wall membrane protein, and the PIPEF since all E. faecalis strains that produced clear-plaques possessed the same amino acid sequence in the variable region of this receptor protein. | Siphoviridae and Sap6virus | [96] |
Bp7 (T4-like phage) | Escherichia coli | Lytic activity against 16 out of 35 clinical strains of E. coli and 4 laboratory E. coli strains. | Host range was attributed to RBP gp38, which recognizes two OMPs (OmpC and LamB) as primary receptors and the heptose of the LPS core as a secondary receptor. RBP gp38 is located at the top of six long tail fibers (LTFs), recognizing suitable OMPs on the bacterial surface and binding to them reversibly, while small tail fibers (STFs) bind to the LPS irreversibly, allowing the phage to inject its genome into the host. So, the broad host range of Bp7 can be explained by the wide distribution of specific OMPs and the inner core of the LPS which is conserved among the several serotypes of E. coli. | Myoviridae (T4-like virus genus) | [97,98] |
SHWT1 | Salmonella Pullorum SP01 | Lytic activity against nine Salmonella serovars, such as Salmonella Pullorum, Salmonella Gallinarum, Salmonella Enteritidis, Salmonella Typhimurium, Salmonella Derby, Salmonella London, Salmonella Typhi, Salmonella Heidelberg, and Salmonella Paratyphi B The phage was able to lyse intracellular Salmonella within macrophages and successfully protected mice against Salmonella Enteritidis and Salmonella Typhimurium infection. | No further information was available regarding the nature of the receptors involved. | Siphoviridae | [99] |
vB_EcoM_KMB22 and vB_EcoM_KMB26 | Escherichia coli ST420 Escherichia coli ST131 | Vkmb22 lysed 18 (44%) and Vkmb26 lysed 33 (82.5%) out of 40 local E.coli strains isolated from urinary tract infections. The undiluted cocktail was composed of vKMB22, and vKMB26 was able to lyse 33 strains (82%), while in the hundredfold diluted cocktail, spot lysis was observed in 23 strains (57%). The phage cocktail was species-specific and was not able to lyse strains of the Enterobacter and Klebsiella genera. | Both phages showed homology with the T4 genome. The main differences between phage genomes were observed in regions encoding for the long tail fibers, which are responsible for host specificity. In agreement with these variabilities, the phages had different host specificities. The broader host specificity of vKMB2 may be attributed to its isolation on the E. coli ST131 strain, which belongs to the predominant E. coli lineage among extraintestinal pathogenic E. coli isolates worldwide. | Myoviridae | [100] |
ASEC2201 and ASEC2202 | Escherichia coli | ASEC2201 formed lytic plaques in 40% of 50 clinical MDR E. coli isolates, while ASEC2202 formed lytic plaques in 44% of them. Both phages had survival percentages of 88% and 98% at a pH of 4, respectively, were able to grow at a low temperature, and were found to be stable in chloroform. | No further information was available regarding the nature of the receptors involved. | Drexlerviridae | [101] |
B. Host Range to the Intragenus Level (Host Range Class II) | |||||
Phage | Host | Host Range Results | Receptors | Family | Refs |
ZoeJ (closely related to TM4) | Mycobacterium smegmatis mc 155 | Infected both fast- and slow-growing mycobacteria, including M. tuberculosis mc27000, M. avium Val14 (O), M. bovis BCG, and M. interjectum ATCC 51457, with a plating efficiency equivalent to that of M. smegmatis. No infection was observed on M. avium subsp. silvaticum, M. abscessus ATCC 19977, M. simiae, M. avium subsp. avium ATCC 25291, Mycobacterium nonchromogenicum ATCC 19530, or Mycobacterium terrae ATCC 15755, even when plated at high titer. | No further information was available regarding the nature of the receptors involved. | Cluster K | [102] |
19 phages | Various strains of Enterococcus | Lytic activity against clinical isolates of E. faecium and E. faecalis, including both vancomycin-resistant Enterococcus (VRE) and vancomycin-susceptible Enterococcus (VSE). Eleven of 19 phages were able to lyse several strains, while three of them lysed almost all strains of E. faecium and E. faecalis | Under selective pressure, mutations primarily in the exopolysaccharide synthesis genes of Enterococcus strains were observed, suggesting that phage resistance may evolve by preventing phage recognition and initial binding. | 10 Siphoviridae phages, 8 Myoviridae phages, and 1 Podoviridae phage | [103] |
JC1 (Bcep22-like phage) | Burkholderia cenocepacia clinical isolate Van1 | Impressively, it has a broad range against Burkholderia species, including B. cepacia, B. multivorans, B. cenocepacia, B. stabilis, B. vietnamiensis, B. dolsa, B. ambifaria, B. anthina, Bcc Group K, Burkholderia sp., and Ralstonia pickettii, which possesses high similarity to Bcc. There was lytic activity against 50 of the 85 strains, forming plaques on 29 of the 50 strains. | Using a collection of B. cenocepasia K56-2 LPS mutants, it was shown that the LPS inner core serves as the primary receptor. | Podoviridae | [104] |
C. Host Range to the Intergenus Level Within the Same Gram Category (Specificity Class III) | |||||
Phage | Host | Host Range Results | Receptors | Family | Refs |
6 Atoyac phages | 600 Gamma- proteobacteria retrieved from the same environment as isolated phages | Ιnfectious against bacteria from six different genera and three orders within the Gamma-proteobacteria class, namely, Aeromonas, Pseudomonas, Yersinia, Hafnia, Escherichia, and Serratia. | Although the comparative genome analysis identified the Atoyac phages as a novel viral group within the Podoviridae family, it could not provide more information about their remarkably broad host range spectrum. | Podoviridae | [105] |
ΦΕent | Salmonella enterica serovars | Infected 11 of 22 tested Salmonella strains from nine different serovars, namely, Belem, Cerro, Enteritidis, Typhimurium, Kentucky, Infantis, Hadar, Thompson, and Braenerup), and three Shigella strains from two species (S. dysenteriae and S. sonnei). | No further information was available regarding the nature of the receptors involved. | Siphoviridae | [106] |
10 T4-like phages | Six strains of prophage-free Escherichia coli: BL21, K12, EC101, DH5α, XL1 Blue, and Top10 | Infected 61 out 72 strains of an E. coli collection and E. coli strain O157:H7 Δstx as well as the S. sonnei strain 53G. | The authors suggested that the observed cross-species infectivity of these T4-like phages could be attributed to the ability of T4 phages to bind to rough-type (R-type) LPS receptors, which are common in Shigella spp. | Myoviridae | [107] |
EscoHU1 | Escherichia coli O157:H7 RIMD 0509939 | Able to form plaques not only in all E. coli O157:H7 strains tested but in strains belonging to other genera like Citrobacter freundii JCM 1657, Salmonella bongori CIP 82.33T, S. sonnei LMG 10473, and four serovars of S. enterica subsp. Enterica (Choleraesuis, Enteriditis, Infantis, and Typhimurium) | EscoHU1 binds to BtuB, which is a receptor that might contribute to its wide host range since the BtuB genes in E. coli and Salmonella are highly similar. | Demerecviridae | [108] |
vB_YpeM_ MHS112 (MHS112) and vB_YpeM_GMS130 (GMS130 | Yersinia pestis | Wide host range. Both phages infect the Yersinia genus, such as Y. pseudotuberculosis and Y. enterocolitica, as well as some species in the order of Enterobacteriales. More specifically, it infects Shigella flexneri, E. coli (ATCC 8739, ATCC 41446, and MG1655) and Salmonella cholerasuis. Furthermore, GMS130 was found to infect more non-Yersinia strains, including non-pathogenic E. coli (ATCC 25922 and FC 7792), enteroaggregative E. coli (EAEC), enterohemorrhagic E. coli (EHEC), Shigella dysenteriae, Shigella boydii, and Enterobacter cloacae, while the MHS112 phage was found to infect Shigella flexneri, E. coli (ATCC 8739, ATCC 41446, and MG1655), and Salmonella cholerasuis). | No further information was available regarding the nature of the receptors involved. | Myoviridae | [109] |
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Bozidis, P.; Markou, E.; Gouni, A.; Gartzonika, K. Does Phage Therapy Need a Pan-Phage? Pathogens 2024, 13, 522. https://doi.org/10.3390/pathogens13060522
Bozidis P, Markou E, Gouni A, Gartzonika K. Does Phage Therapy Need a Pan-Phage? Pathogens. 2024; 13(6):522. https://doi.org/10.3390/pathogens13060522
Chicago/Turabian StyleBozidis, Petros, Eleftheria Markou, Athanasia Gouni, and Konstantina Gartzonika. 2024. "Does Phage Therapy Need a Pan-Phage?" Pathogens 13, no. 6: 522. https://doi.org/10.3390/pathogens13060522