Bacteriophages: Molecular and Virologic Review Study
DOI:
https://doi.org/10.63939/7zbcct09Keywords:
Bacteriophages, phages, Lytic cycle, Lysogenic cycle, Phage therapy, Phage immunogenicity, Microbiome, Anti-CRISPR proteinsAbstract
Earth's most common viruses, bacteriophages, infect bacteria and archaea. Protein capsids and sometimes lipid envelopes encase phage genomes, which vary in kind and structure. Most are double-stranded DNA phages, whereas Cystoviridae are RNA. Phages control bacterial populations, transfer horizontal genes, lyse molecules, and alter metabolism in different situations. Based on their structural morphotypes, which are largely determined by tail architecture, phages are classified as Podoviridae (short tails), Siphoviridae (long, flexible tails), and Myoviridae (long, contractile tails). They build genome transport and host recognition virions with portal proteins, tail fibers, and baseplates. DNA is transferred into capsids by ATP-dependent terminases during genome packing. The lysogenic cycle comprises temperate phages integrating into the host genome as prophages and replicating passively until stimulation activates the lytic phase. Phages with non-lytic chronic infections or carriers exist. Phages limit their host range by recognizing lipopolysaccharides, outer membrane proteins, teichoic acids, and flagella. They can make anti-CRISPR proteins to attack bacteria. Phages indirectly affect human health by influencing microbiota and immune systems. Immunoglobulin-like capsid domains connect them to mucosal surfaces for bacterial clearance and barrier protection. They can also enter tissues and circulation, where they are immunologically tolerated. Phages activate innate and adaptive immunity. Innate sensing and cytokine production are enabled by TLR3, TLR7, and TLR9. However, adaptive immunity produces neutralizing IgM, IgG, and IgA antibodies. Recurrent phage therapy can be reduced by phage-neutralizing antibodies. Phage biology is characterized by the discovery of "huge phages" with genomes that rival small bacterial genomes and encode complex functions like tRNAs, translation factors, CRISPR-Cas systems, and nucleus-like compartments that protect
phage genomes from host defenses. Phage-encoded CRISPR-Cas systems often lack spacer acquisition or interference genes, resulting in host apparatus repurposing or gene transcriptional silence. Targeting competing phages and host regulatory mechanisms is possible. Phages treat antibiotic-resistant microorganisms. Phage treatment has potential despite bacterial resistance and host immune neutralization. They also carry toxin genes (cholera, diphtheria) through lysogenic conversion, boosting bacterial pathogenicity. Dynamic evolutionary arms races affect microbial ecology through phage-host and phage-phage interactions. Recent metagenomics and meta transcriptomics advances have increased the variety of dsRNA and tailless dsDNA phages. This showed unique viral families and the prevalence of phages in human microbiomes, particularly crAss-like phages in the intestine. The molecular details of phage interactions with eukaryotic cells are still emerging, despite the vast knowledge of bacterial receptors for phage attachment. Mammalian cells can use endocytosis mechanisms to internalize phages for immunological regulation and therapeutic delivery. expanding the taxonomy of dsRNA phages, understanding non-lytic infection mechanisms, characterizing phage-host range and interactions, and using phages for biocontrol in agriculture and medicine. It is required to overcome immune clearance, understand phage immunogenicity, and understand the tri-kingdom interactions between phages, bacteria, and human hosts that maintain microbial and immunological homeostasis to maximize phage therapy. Bacteriophages are complex, diversified, and ecologically important viruses. Bacteria, horizontal gene transfer, immune system contact, and burgeoning biological uses including phage therapy and biotechnology are managed. Phages' complex life cycles, structural biology, and interactions with human and bacterial hosts are being understood beyond their role as bacterial predators. Briefly explain bacteriophages, which infect bacteria and archaea, their diversity, dsDNA and dsRNA phages, structure and replication mechanisms, ecological implications, mammalian immunity, and emerging therapeutic applications, including phage therapy. Phage viruses are assembled by complex structural proteins. Widely studied tailed phages including T7 (Autographviridae/Podoviridae-like), SPP1 (Siphoviridae-like), and T4 (Myoviridae-like) have tail and capsid shapes optimized for genome transport and host recognition Biomolecules such lipopolysaccharides and outer membrane proteins bind to baseplate and tail fibers. Genome packing motor ATPases assist phage DNA enter capsids. T4 phages employ the lytic cycle to rapidly multiply and lyse the host cell, while temperate phages use the lysogenic cycle to passively
integrate their genome into the host chromosome until induction activates lytic replication. Infection-causing pseudolysogenic or persistent phages do not lyse quickly. In bacterial pathogen phage treatment, these life choices affect phage ecology and application. To identify hosts, phages recognize polysaccharides, proteins, and flagella. Phage host range is limited by specificity. To escape bacterial defenses, phages can encode anti-CRISPR proteins and adapt genomically. Phages transfer toxin genes and other virulence factors to bacteria by lysogenic conversion. Phages influence microbiomes and immunity without infecting humans. Phages can infect tissues and cells via endocytosis, altering immune responses. Phages destroy bacteria to fight antibiotic-resistant illnesses, but immunological responses including neutralizing antibodies can hinder phage treatment. Recent discoveries include "huge phages" with microscopic bacteria genomes. Complex machinery is provided by tRNA, translation factor, and CRISPR-Cas phages. Metagenomic studies have found tailless dsDNA phages from new viral orders and families, enhancing our understanding of phage diversity. CRISPR-mediated phage-host and phage-phage interactions show dynamic evolutionary arms races. Biomedical applications, gene transfer, microbial community dynamics, and bacterial population regulation depend on bacteriophages. Research on their structural biology, trplicative cycles, and host immunological interactions determines their therapeutic and ecological potential. Bacteriophages are everywhere in the biosphere and influence bacterial ecology and evolution. DNA-containing bacteriophages in ecosystems are well-studied, whereas RNA-containing ones are often overlooked.
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1. Kim A, Shin TH, Shin SM, Pham CD, Choi DK et al. 2012. Cellular internalization mechanism and intracellular trafficking of filamentous M13 phages displaying a cell-penetrating transbody and TAT peptide. PLOS ONE 7: 12e51813
2. Boyd EF. Bacteriophage-encoded bacterial virulence factors and phage-pathogenicity island interactions. Adv Virus Res. 2012; 82:91-118.
3. Keller R, Zatzman M. 1956. Studies on the factors concerned in the disappearance of bacteriophage particles from the animal body. J. Immunol. 83:167–72
4. Bilzer M, Roggel F, Gerbes AL. 2006. Role of Kupffer cells in host defense and liver disease. Liver Int 26:101175–86
5. Bronte V, Pittet MJ. 2013. The spleen in local and systemic regulation of immunity. Immunity 39:806–18
6. Mäntynen, S.; Laanto, E.; Kohvakka, A.; Poranen, M.M.; Bamford, J.K.H.; Ravantti, J.J. New enveloped dsRNA phage from freshwater habitat. J. Gen. Virol. 2015, 96, 1180–1189
7. Crippen, C.S.; Zhou, B.; Andresen, S.; Patry, R.T.; Muszynski, A.; Parker, C.T.; Cooper, K.K.; Szymanski, C.M. RNA and sugars, unique properties of bacteriophages infecting multidrug resistant Acinetobacter radioresistens strain LH6. Viruses 2021, 13, 1652
8. Chen, Y.M.; Sadiq, S.; Tian, J.H.; Chen, X.; Lin, X.D.; Shen, J.J.; Chen, H.; Hao, Z.Y.; Wille, M.; Zhou, Z.C.; et al. RNA viromes from terrestrial sites across China expand environmental viral diversity. Nat. Microbiol. 2022, 7, 1312–1323
9. Li, L.; Zhong, Q.; Zhao, Y.; Bao, J.; Liu, B.; Zhong, Z.; Wang, J.; Yang, L.; Zhang, T.; Cheng, M.; et al. First-in-human application of double-stranded RNA bacteriophage in the treatment of pulmonary Pseudomonas aeruginosa infection. Microb. Biotechnol. 2023, 16, 862–867.
10. Pinheiro, L.A.M.; Pereira, C.; Frazao, C.; Balcao, V.M.; Almeida, A. Efficiency of phage phi6 for biocontrol of Pseudomonas syringae pv. syringae: An in vitro preliminary study. Microorganisms 2019, 7, 286.
11. Koonin, E.V.; Dolja, V.V.; Krupovic, M.; Varsani, A.; Wolf, Y.I.; Yutin, N.; Zerbini, F.M.; Kuhn, J.H. Global organization and proposed megataxonomy of the virus world. Microbiol. Mol. Biol. Rev. 2020, 84, e00061-19
12. Brum, J.R.; Schenck, R.O.; Sullivan, M.B. Global morphological analysis of marine viruses shows minimal regional variation and dominance of non-tailed viruses. ISME J. 2013, 7, 1738–1751
13. Kauffman, K.M.; Hussain, F.A.; Yang, J.; Arevalo, P.; Brown, J.M.; Chang, W.K.; VanInsberghe, D.; Elsherbini, J.; Sharma, R.S.; Cutler, M.B.; et al. A major lineage of non-tailed dsDNA viruses as unrecognized killers of marine bacteria. Nature 2018, 554, 118–122.
14. Krupovic, M.; Bamford, D.H. Virus evolution: How far does the double beta-barrel viral lineage extend? Nat. Rev. Microbiol. 2008, 6, 941–948.
15. Abrescia, N.G.; Bamford, D.H.; Grimes, J.M.; Stuart, D.I. Structure unifies the viral universe. Annu. Rev. Biochem. 2012, 81, 795–822.
16. Krupovic, M.; Koonin, E.V. Multiple origins of viral capsid proteins from cellular ancestors. Proc. Natl. Acad. Sci. USA 2017, 114, E2401–E2410.
17. Krupovic, M.; Makarova, K.S.; Koonin, E.V. Cellular homologs of the double jelly-roll major capsid proteins clarify the origins of an ancient virus kingdom. Proc. Natl. Acad. Sci. USA 2022, 119, e2120620119.
18. Yutin, N.; Backstrom, D.; Ettema, T.J.G.; Krupovic, M.; Koonin, E.V. Vast diversity of prokaryotic virus genomes encoding double jelly-roll major capsid proteins uncovered by genomic and metagenomic sequence analysis. Virol. J. 2018, 15, 67.
19. Mannisto, R.H.; Kivela, H.M.; Paulin, L.; Bamford, D.H.; Bamford, J.K. The complete genome sequence of PM2, the first lipid-containing bacterial virus to be isolated. Virology 1999, 262, 355–363.
20. Leigh, B.A.; Breitbart, M.; Oksanen, H.M.; Bamford, D.H.; Dishaw, L.J. Genome Sequence of PM2-like phage Cr39582, induced from a Pseudoalteromonas sp. isolated from the gut of Ciona robusta. Genome Announc. 2018, 6, e00368-18.
21. Kalatzis, P.G.; Carstens, A.B.; Katharios, P.; Castillo, D.; Hansen, L.H.; Middelboe, M. Complete genome sequence of Vibrio anguillarum nontailed bacteriophage NO16. Microbiol. Resour. Announc. 2019, 8, e00020-19.
22. Oksanen, H.M.; Ictv Report Consortium. ICTV virus taxonomy profile: Corticoviridae. J. Gen. Virol. 2017, 98, 888–889.
23. Krupovic, M.; Bamford, D.H. Putative prophages related to lytic tailless marine dsDNA phage PM2 are widespread in the genomes of aquatic bacteria. BMC Genom. 2007, 8, 236.
24. Manrique, P.; Bolduc, B.; Walk, S.T.; van der Oost, J.; de Vos, W.M.; Young, M.J. Healthy human gut phageome. Proc. Natl. Acad. Sci. USA 2016, 113, 10400–10405.
25. Townsend, E.M.; Kelly, L.; Muscatt, G.; Box, J.D.; Hargraves, N.; Lilley, D.; Jameson, E. The human gut phageome: Origins and roles in the human gut microbiome. Front. Cell Infect. Microbiol. 2021, 11, 643214.
26. Shkoporov, A.N.; Clooney, A.G.; Sutton, T.D.S.; Ryan, F.J.; Daly, K.M.; Nolan, J.A.; McDonnell, S.A.; Khokhlova, E.V.; Draper, L.A.; Forde, A.; et al. The human gut virome is highly diverse, stable, and individual specific. Cell Host Microbe 2019, 26, 527–541.e5.
27. Shkoporov, A.N.; Hill, C. Bacteriophages of the human gut: The “known unknown” of the microbiome. Cell Host Microbe 2019, 25, 195–209.
28. Yutin, N.; Makarova, K.S.; Gussow, A.B.; Krupovic, M.; Segall, A.; Edwards, R.A.; Koonin, E.V. Discovery of an expansive bacteriophage family that includes the most abundant viruses from the human gut. Nat. Microbiol. 2018, 3, 38–46.
29. Yutin, N.; Benler, S.; Shmakov, S.A.; Wolf, Y.I.; Tolstoy, I.; Rayko, M.; Antipov, D.; Pevzner, P.A.; Koonin, E.V. Analysis of metagenome-assembled viral genomes from the human gut reveals diverse putative CrAss-like phages with unique genomic features. Nat. Commun. 2021, in press
30. Guerin, E.; Shkoporov, A.; Stockdale, S.R.; Clooney, A.G.; Ryan, F.J.; Sutton, T.D.S.; Draper, L.A.; Gonzalez-Tortuero, E.; Ross, R.P.; Hill, C. Biology and taxonomy of crAss-like bacteriophages, the most abundant virus in the human gut. Cell Host Microbe 2018, 24, 653–664.e6. nShkoporov, A.N.; Khokhlova, E.V.; Fitzgerald, C.B.; Stockdale, S.R.; Draper, L.A.; Ross, R.P.; Hill, C. PhiCrAss001 represents the most abundant bacteriophage family in the human gut and infects Bacteroides intestinalis. Nat. Commun. 2018, 9, 4781.
31. Sausset, R.; Petit, M.A.; Gaboriau-Routhiau, V.; De Paepe, M. New insights into intestinal phages. Mucosal Immunol. 2020, 13, 205–215.
32. Yuan Y, Gao M. Jumbo bacteriophages: an overview. Front. Microbiol. 2017; 8:403.
33. Breitbart M, Bonnain C, Malki K, Sawaya NA. Phage puppet masters of the marine microbial realm. Nat. Microbiol. 2018; 3:754–766.
34. Rascovan N, Duraisamy R, Desnues C. Metagenomics and the human virome in asymptomatic individuals. Annu. Rev. Microbiol. 2016; 70:125–141.
35. Emerson JB, et al. Host-linked soil viral ecology along a permafrost thaw gradient. Nat. Microbiol. 2018; 3:870–880.
36. Balcazar JL. Bacteriophages as vehicles for antibiotic resistance genes in the environment. PLoS Pathog. 2014;10: e1004219.
37. Penadés JR, Chen J, Quiles-Puchalt N, Carpena N, Novick RP. Bacteriophage-mediated spread of bacterial virulence genes. Curr. Opin. Microbiol. 2015; 23:171–178.
38. Brown-Jaque M, et al. Detection of bacteriophage particles containing antibiotic resistance genes in the sputum of cystic fibrosis patients. Front. Microbiol. 2018; 9:856.
39. Shkoporov AN, Hill C. Bacteriophages of the human gut: the “known unknown” of the microbiome. Cell Host Microbe. 2019; 25:195–209.
40. Devoto AE, et al. Megaphages infect Prevotella and variants are widespread in gut microbiomes. Nat. Microbiol. 2019; 4:693–700.
41. Castelle CJ, et al. Biosynthetic capacity, metabolic variety and unusual biology in the CPR and DPANN radiations. Nat. Rev. Microbiol. 2018; 16:629–645.
42. Pérez-Brocal V, et al. A small microbial genome: the end of a long symbiotic relationship? Science. 2006; 314:312–313.
43. Nakabachi A, et al. The 160-kilobase genome of the bacterial endosymbiont Carsonella. Science. 2006; 314:267.
44. Basem Al-Shayeb, Rohan Sachdeva , Lin-Xing Chen , Fred Ward , Patrick Munk , Audra Devoto , Cindy J Castelle , Matthew R Olm , Keith Bouma-Gregson , Yuki Amano , Christine He , Raphaël Méheust , Brandon Brooks , Alex Thomas , Adi Lavy , Paula Matheus-Carnevali , Christine Sun , Daniela S A Goltsman , Mikayla A Borton , Allison Sharrar , Alexander L Jaffe , Tara C Nelson , Rose Kantor , Ray Keren , Katherine R Lane , Ibrahim F Farag , Shufei Lei , Kari Finstad , Ronald Amundson , Karthik Anantharaman , Jinglie Zhou , Alexander J Probst , Mary E Power, Susannah G Tringe , Wen-Jun Li , Kelly Wrighton , Sue Harrison , Michael Morowitz, David A Relman , Jennifer A Doudna , Anne-Catherine Lehours , Lesley Warren , Jamie H D Cate , Joanne M Santini, Jillian F Banfield Clades of huge phages from across Earth’s ecosystems Nature. 2020 Feb 12;578(7795):425–431.
45. Lobry JR. Asymmetric substitution patterns in the two DNA strands of bacteria. Mol. Biol. Evol. 1996; 13:660–665.
46. . Paez-Espino D, et al. Uncovering Earth’s virome. Nature. 2016; 536:425–430.
47. Paez-Espino D, et al. IMG/VR: a database of cultured and uncultured DNA viruses and retroviruses. Nucleic Acids Res. 2017;45: D457–D465
48. Ivanova NN, et al. Stop codon reassignments in the wild. Science. 2014; 344:909–913.
49. Ignatiou, A. ∙ Brasilès, S. ∙ El Sadek Fadel, M. Structural transitions during the scaffolding-driven assembly of a viral capsid Nat. Commun. 2019; 10:4840
50. Dröge, A. ∙ Santos, M.A. ∙ Stiege, A.C. Shape and DNA packaging activity of bacteriophage SPP1 procapsid: Protein components and interactions during assembly J. Mol. Biol. 2000; 296:117-132
51. Orlova, E.V. ∙ Gowen, B. Dröge, A. Structure of a viral DNA gatekeeper at 10 A resolution by cryo-electron microscopy EMBO J. 2003; 22:1255-1262
52. Veesler, D. ∙ Robin, G. ∙ Lichière, J. Crystal structure of bacteriophage SPP1 distal tail protein (gp19.1): A baseplate hub paradigm in gram-positive infecting phages J. Biol. Chem. 2010; 285:36666-36673
53. Mahony, J. ∙ Stockdale, S.R. ∙ Collins, B. Lactococcus lactis phage TP901–1 as a model for Siphoviridae virion assembly Bacteriophage. 2016; 6, e1123795
54. Kizziah, J.L. ∙ Manning, K.A. ∙ Dearborn, A.D. Structure of the host cell recognition and penetration machinery of a Staphylococcus aureus bacteriophage PLoS Pathog. 2020; 16, e1008314
55. Goulet, A. ∙ Spinelli, S. ∙ Mahony, J. ... Conserved and diverse traits of adhesion devices from siphoviridae recognizing proteinaceous or saccharidic receptors Viruses. 2020; 12:1-21
56. sx30.Xu, J. ∙ Hendrix, R.W. ∙ Duda, R.L. Chaperone-protein interactions that mediate assembly of the bacteriophage lambda tail to the correct length J. Mol. Biol. 2014; 426:1004-1018
57. Langlois, C. ∙ Ramboarina, S. ∙ Cukkemane, A. Bacteriophage SPP1 tail tube protein self-assembles into β-structure-rich tubes J. Biol. Chem. 2014; 290:3836-3849
58. Chaban, Y. ∙ Lurz, R. ∙ Brasilès, S. Structural rearrangements in the phage head-to-tail interface during assembly and infection Proc. Natl. Acad. Sci. U. S. A. 2015; 112:7009-7014
59. Boulanger, P. ∙ Jacquot, P. ∙ Plançon, L. Phage T5 straight tail fiber is a multifunctional protein acting as a tape measure and carrying fusogenic and muralytic activities J. Biol. Chem. 2008; 283:13556-13564
60. Fang, Q. ∙ Tang, W.C. ∙ Tao, P. Structural morphing in a symmetry-mismatched viral vertex Nat. Commun. 2020; 11:1713
61. sx39.Leiman, P.G. ∙ Kanamaru, S. ∙ Mesyanzhinov, V.V. Structure and morphogenesis of bacteriophage T4 Cell. Mol. Life Sci. 2003; 60:2356-2370
62. Qin, L. ∙ Fokine, A. ∙ O'Donnell, E. Structure of the small outer capsid protein, Soc: A clamp for stabilizing capsids of T4-like phages J. Mol. Biol. 2010; 395:728-741
63. Rossmann, M.G. ∙ Mesyanzhinov, V.V. ∙ Arisaka, F. The bacteriophage T4 DNA injection machine Curr. Opin. Struct. Biol. 2004; 14:171-180
64. Taylor, N.M. ∙ Prokhorov, N.S. ∙ Guerrero-Ferreira, R.C. ... Structure of the T4 baseplate and its function in triggering sheath contraction Nature. 2016; 533:346-352
65. Zheng, W. ∙ Wang, F. ∙ Taylor, N.M.I. ... Refined cryo-EM structure of the T4 tail tube: Exploring the lowest dose limit Structure. 2017; 25:1436-1441.e2
66. Fokine, A. ∙ Zhang, Z. ∙ Kanamaru, S. The molecular architecture of the bacteriophage T4 neck J. Mol. Biol. 2013; 425:1731-1744
67. Yap, M.L. ∙ Klose, T. ∙ Arisaka, F. ... Role of bacteriophage T4 baseplate in regulating assembly and infection Proc. Natl. Acad. Sci. U. S. A. 2016; 113:2654-2659
68. Washizaki, A. ∙ Yonesaki, T. ∙ Otsuka, Y. Characterization of the interactions between Escherichia coli receptors, LPS and OmpC, and bacteriophage T4 long tail fibers Microbiologyopen. 2016; 5:1003-1015
69. Hu, B. ∙ Margolin, W. ∙ Molineux, I.J. Structural remodeling of bacteriophage T4 and host membranes during infection initiation Proc. Natl. Acad. Sci. U. S. A. 2015; 112:E4919-E4928
70. 1.sCai, X.; Tian, F.; Teng, L.; Liu, H.; Tong, Y.; Le, S.; Zhang, T. Cultivation of a lytic double-stranded RNA bacteriophage infecting Microvirgula aerodenitrificans reveals a mutualistic parasitic lifestyle. J. Virol. 2021, 95, 0039921.
71. Li, D.; Li, Y.; Li, P.; Han, Q.; Zhang, T.; Yang, B.; Wu, W.; Yang, H. Phage phiZ98: A novel tri-segmented dsRNA cystovirus for controlling Pseudomonas strains with defective lipopolysaccharides in foods. Food Res. Int. 2022, 162, 112197.
72. Ilca, S.L.; Sun, X.; El Omari, K.; Kotecha, A.; de Haas, F.; DiMaio, F.; Grimes, J.M.; Stuart, D.I.; Poranen, M.M.; Huiskonen, J.T. Multiple liquid crystalline geometries of highly compacted nucleic acid in a dsRNA virus. Nature 2019, 570, 252–256.
73. Jäälinoja, H.T.; Huiskonen, J.T.; Butcher, S.J. Electron cryomicroscopy comparison of the architectures of the enveloped bacteriophages phi6 and phi8. Structure 2007, 15, 157–167.
74. Hu, G.B.; Wei, H.; Rice, W.J.; Stokes, D.L.; Gottlieb, P. Electron cryo-tomographic structure of cystovirus phi12. Virology 2008, 372, 1–9.
75. Huiskonen, J.T.; de Haas, F.; Bubeck, D.; Bamford, D.H.; Fuller, S.D.; Butcher, S.J. Structure of the bacteriophage phi6 nucleocapsid suggests a mechanism for sequential RNA packaging. Structure 2006, 14, 1039–1048.
76. Sun, Z.; El Omari, K.; Sun, X.; Ilca, S.L.; Kotecha, A.; Stuart, D.I.; Poranen, M.M.; Huiskonen, J.T. Double-stranded RNA virus outer shell assembly by bona fide domain-swapping. Nat. Commun. 2017, 8, 14814.
77. Ilca, S.L.; Kotecha, A.; Sun, X.; Poranen, M.M.; Stuart, D.I.; Huiskonen, J.T. Localized reconstruction of subunits from electron cryomicroscopy images of macromolecular complexes. Nat. Commun. 2015, 6, 8843.
78. El Omari, K.; Sutton, G.; Ravantti, J.J.; Zhang, H.; Walter, T.S.; Grimes, J.M.; Bamford, D.H.; Stuart, D.I.; Mancini, E.J. Plate tectonics of virus shell assembly and reorganization in phage phi8, a distant relative of mammalian reoviruses. Structure 2013, 21, 1384–1395.
79. Miyazaki, N.; Salaipeth, L.; Kanematsu, S.; Iwasaki, K.; Suzuki, N. Megabirnavirus structure reveals a putative 120-subunit capsid formed by asymmetrical dimers with distinctive large protrusions. J. Gen. Virol. 2015, 96, 2435–
80. Mönttinen, H.A.M.; Ravantti, J.J.; Poranen, M.M. Structure unveils relationships between RNA virus polymerases. Viruses 2021, 13, 313.
81. Gottlieb, P.; Alimova, A. RNA packaging in the cystovirus bacteriophages: Dynamic interactions during capsid maturation. Int. J. Mol. Sci. 2022, 23, 2677.
82. Zhang, C.; Li, Y.; Samad, A.; Zheng, P.; Ji, Z.; Chen, F.; Zhang, H.; Jin, T. Structure and mutation analysis of the hexameric P4 from Pseudomonas aeruginosa phage phiYY. Int. J. Biol. Macromol. 2022, 194, 42–49
83. Mäntynen, S.; Sundberg, L.R.; Poranen, M.M. Recognition of six additional cystoviruses: Pseudomonas virus phi6 is no longer the sole species of the family Cystoviridae. Arch. Virol. 2018, 163, 1117–1124.
84. Poranen, M.M.; Tuma, R.; Bamford, D.H. Assembly of double-stranded RNA bacteriophages. Adv. Virus Res. 2005, 64, 15–43.
85. Poranen, M.M.; Mäntynen, S. Cystoviridae. In The Online Report of the International Committee on Taxonomy of Viruses; International Committee on Taxonomy of Viruses (ICTV): Online, 2019; Available online: http://taxonomy.cvr.gla.ac.uk/PDF/Cystoviridae.pdf (accessed on 1 September 2023).
86. International Committee on Taxonomy of Viruses Executive. The new scope of virus taxonomy: Partitioning the virosphere into 15 hierarchical ranks. Nat. Microbiol. 2020, 5, 668–674.
87. Simmonds, P.; Adriaenssens, E.M.; Zerbini, F.M.; Abrescia, N.G.A.; Aiewsakun, P.; Alfenas-Zerbini, P.; Bao, Y.; Barylski, J.; Drosten, C.; Duffy, S.; et al. Four principles to establish a universal virus taxonomy. PLoS Biol. 2023, 21, e3001922.
88. Yang, Y.; Lu, S.; Shen, W.; Zhao, X.; Shen, M.; Tan, Y.; Li, G.; Li, M.; Wang, J.; Hu, F.; et al. Characterization of the first double-stranded RNA bacteriophage infecting Pseudomonas aeruginosa. Sci. Rep. 2016, 6, 38795.
89. Neri, U.; Wolf, Y.I.; Roux, S.; Camargo, A.P.; Lee, B.; Kazlauskas, D.; Chen, I.M.; Ivanova, N.; Zeigler Allen, L.; Paez-Espino, D.; et al. Expansion of the global RNA virome reveals diverse clades of bacteriophages. Cell 2022, 185, 4023–4037.e18.
90. Abedon ST (October 2019). "Look Who's Talking: T-Even Phage Lysis Inhibition, the Granddaddy of Virus-Virus Intercellular Communication Research". Viruses. 11 (10): 951.
91. Mason KA, Losos JB, Singer SR, Raven PH, Johnson GB (2011). Biology. New York: McGraw-Hill. p. 533. ISBN 978-0-07-893649-4.
92. 71.g Charles RC, Ryan ET (October 2011). "Cholera in the 21st century". Current Opinion in Infectious Diseases. 24 (5): 472–477.
93. Keen EC (December 2012). "Paradigms of pathogenesis: targeting the mobile genetic elements of disease". Frontiers in Cellular and Infection Microbiology. 2: 161
94. Drulis-Kawa Z, Majkowska-Skrobek G, Maciejewska B (2015). "Bacteriophages and phage-derived proteins--application approaches". Current Medicinal Chemistry. 22 (14): 1757–1773
95. Maghsoodi A, Chatterjee A, Andricioaei I, Perkins NC (December 2019). "How the phage T4 injection machinery works including energetics, forces, and dynamic pathway". Proceedings of the National Academy of Sciences of the United States of America. 116 (50): 25097–25105. Bibcode: 2019 PNAS.11625097M.
96. Mizuno CM, Guyomar C, Roux S, Lavigne R, Rodriguez-Valera F, Sullivan MB, et al. (February 2019). "Numerous cultivated and uncultivated viruses encode ribosomal proteins". Nature Communications. 10 (1) 752. Bibcode:2019 NatCo..10..752M. .
97. Edgar RS Conditional lethals: in Phage and the Origins of Molecular Biology (2007) Edited by John Cairns, Gunther S. Stent, and James D. Watson, Cold Spring Harbor Laboratory of Quantitative Biology, Cold Spring Harbor, Long Island, New York ISBN 978-0-87969-800-3
98. Henrot C, Petit MA (November 2022). "Signals triggering prophage induction in the gut microbiota". Molecular Microbiology. 118 (5): 494–502.
99. Nguyen S, Baker K, Padman BS, Mazel D, Cambillau C, Desnues C, et al. Endocytosis of Bacteriophages. J Virol. 2022 Feb;96(3):e0112421.
100. Frunzke J, Mußmann K, Liess B, et al. Internalization of a polysialic acid-binding Escherichia coli bacteriophage into eukaryotic neuroblastoma cells. Nat Commun. 2017 Dec 3;8(1):1508.
101. Piotukh K, Persson MA, Liu B, Paschen A, Hammarström S, Fredericson M, et al. Cellular Internalization Mechanism and Intracellular Trafficking of Filamentous M13 Phages Displaying a Cell-Penetrating Transbody and TAT Peptide. PLoS One. 2012 Dec 13;7(12):e51813.
102. Nguyen S, Baker K, Padman BS, Mazel D, Cambillau C, Desnues C, et al. Mammalian cells internalize bacteriophages and use them as a resource to enhance cellular growth and survival. PLoS Biol. 2023 Oct 26;21(10): e3002341.
103. Frunzke J, Mußmann K, Liess B, et al. Internalization of a polysialic acid-binding Escherichia coli bacteriophage into eukaryotic neuroblastoma cells. Nat Commun. 2017 Dec 3;8(1):1508.
104. Piotukh K, Persson MA, Liu B, Paschen A, Hammarström S, Fredericson M, et al. Cellular Internalization Mechanism and Intracellular Trafficking of Filamentous M13 Phages Displaying a Cell-Penetrating Transbody and TAT Peptide. PLoS One. 2012 Dec 13;7(12): e51813.
105. Frunzke J, Mußmann K, Liess B, et al. Internalization of a polysialic acid-binding Escherichia coli bacteriophage into eukaryotic neuroblastoma cells. Nat Commun. 2017 Dec 3;8(1):1508.
106. Bertozzi Silva J, Storms Z, Sauvageau D. Host receptors for bacteriophage adsorption. FEMS Microbiol Lett. 2016 May;363(4): fnv121.
107. Piotukh K, Persson MA, Liu B, Paschen A, Hammarström S, Fredericson M, et al. Cellular Internalization Mechanism and Intracellular Trafficking of Filamentous M13 Phages Displaying a Cell-Penetrating Transbody and TAT Peptide. PLoS One. 2012 Dec 13;7(12): e51813.
108. Majewska J, Kaźmierczak Z, Legut M, et al. Interactions of Bacteriophages with Animal and Human Organisms. Int J Mol Sci. 2021 Aug 19;22(16):8937.
109. De Sordi L, Lourenço M, Debarbieux L. The Battle Within: Interactions of Bacteriophages and Bacteria in the Gastrointestinal Tract. Cell Host Microbe. 2019 Feb 13;25(2):210-218.
110. Christin JR, Beckert MV. Origins and Applications of CRISPR-Mediated Genome Editing. Einstein J Biol Med. 2016;31(1-2):2-5.
111. Maciejewska B, Olszak T, Drulis-Kawa Z. Applications of bacteriophages versus phage enzymes to combat and cure bacterial infections: an ambitious and also a realistic application? Appl Microbiol Biotechnol. 2018 Mar;102(6):2563-2581.
112. Górski A, et al. Use of Bacteriophages to Target Intracellular Pathogens. Clin Infect Dis. 2023;77(Suppl_5): S423-S431.
113. Barr JJ. Phages in the Human Body. Front Microbiol. 2017; 8:566.
114. Lehti TA, et al. Interactions between Bacteriophages and Eukaryotic Cells. J Immunol. 2020; 2020:3589316.
115. Roach DR, Debarbieux L. Interactions between Bacteriophage, Bacteria, and the Mammalian Immune System. Viruses. 2018;10(1):10.
116. Shkoporov AN, Hill C. Bacteriophages as New Human Viral Pathogens. Viruses. 2018;10(6):317.
117. Hargreaves KR, et al. Special Issue: Phage–Bacteria Interplay in Health and Disease. Viruses. 2022;14(5):970.
118. McCallin S, Oechslin F. Bacteriophage strategies for overcoming host antiviral immunity. Front Microbiol. 2023; 14:1211793.
119. Phages in the Human Body," Frontiers in Microbiology, 2017.
120. "New Insights Regarding Bacteriophage-Mammalian Cell Interactions," PubMed, 2021.
121. "Phages and Human Health: More Than Idle Hitchhikers," PMC, 2019.
122. "Use of Bacteriophages to Target Intracellular Pathogens," Clinical Infectious Diseases, 2023.
123. "Interactions between Bacteriophages and Eukaryotic Cells," Wiley, 2020.
124. "Interactions of Bacteriophages with Animal and Human Organisms-Safety Issues," PubMed, 2021.
125. "Therapeutic Phages as Modulators of the Immune Response," Clinical Infectious Diseases, 2023.
126. "Special Issue: Phage–Bacteria Interplay in Health and Disease," PMC, 2022.
127. Pham TD, Nguyen TH, Iwashita H, Takemura T, Morita K, Yamashiro T. Comparative analyses of CTX prophage region of Vibrio cholerae seventh pandemic wave 1 strains isolated in Asia. Microbiol Immunol. 2018 Oct;62(10):635-650
128. Motlagh AM, Bhattacharjee AS, Goel R. Biofilm control with natural and genetically-modified phages. World J Microbiol Biotechnol. 2016 Apr;32(4):67.
129. Laura M. Kasman; La Donna Porter. Creative Commons Attribution-NonCommercial-NoDerivatives 4.0 International (CC BY-NC-ND 4.0) Bookshelf ID: NBK493185 PMID: 29630237 ( http://creativecommons.org/licenses/by-nc-nd/4.0/ ),
130. Vaca Pacheco S, Garcıća González O, Paniagua Contreras GL 2006. The lom gene of bacteriophage λ is involved in Escherichia coli K12 adhesion to human buccal epithelial cells. FEMS Microbiol. Lett. 156:1129–32
131. Secor PR, Sweere JM, Michaels LA, Malkovskiy AV, Lazzareschi D et al. 2015. Filamentous bacteriophage promotes biofilm assembly and function. Cell Host Microbe 18:549–59
132. do Vale A, Cabanes D, Sousa S. 2016. Bacterial toxins as pathogen weapons against phagocytes. Front. Microbiol. 1:42
133. asechnek A, Rabinovich L, Stadnyuk O, Azulay G, Mioduser J et al. 2020. Active lysogeny in Listeria monocytogenes is a bacteria-phage adaptive response in the mammalian environment. Cell Rep 32:4107956
134. Goh S, Hussain H, Chang BJ, Emmett W, Riley TV, Mullany P 2013. Phage ϕC2 mediates transduction of Tn6215, encoding erythromycin resistance, between Clostridium difficile strains. mBio 4:6e00840-13
135. Wang X, Kim Y, Ma Q, Hong SH, Pokusaeva K et al. 2010. Cryptic prophages help bacteria cope with adverse environments. Nat. Commun. 1:9147
136. Gebhart D, Williams SR, Bishop-Lilly KA, Govoni GR, Willner KM et al. 2012. Novel high-molecular-weight, R-type bacteriocins of Clostridium difficile. J. Bacteriol. 194:226240–47
137. Barr JJ, Auro R, Furlan M, Whiteson KL, Erb ML et al. 2013. Bacteriophage adhering to mucus provide a non-host-derived immunity. PNAS 110:2610771–76T4 phages are shown to interact with mammalian mucosa through capsid immunoglobulin-like domains.
138. Fraser JS, Yu Z, Maxwell KL, Davidson AR. 2006. Ig-like domains on bacteriophages: a tale of promiscuity and deceit. J. Mol. Biol. 359:2496–507
139. Almeida GMF, Laanto E, Ashrafi R, Sundberg LR. 2019. Bacteriophage adherence to mucus mediates preventive protection against pathogenic bacteria. mBio 10:601984-19
140. Barr JJ, Auro R, Sam-Soon N, Kassegne S, Peters G et al. 2015. Subdiffusive motion of bacteriophage in mucosal surfaces increases the frequency of bacterial encounters. PNAS 112:4413675–80
141. Yang JY, Kim MS, Kim E, Cheon JH, Lee YS et al. 2016. Enteric viruses ameliorate gut inflammation via Toll-like receptor 3 and Toll-like receptor 7-mediated interferon-β production. Immunity 44:4889–900
142. Gogokhia L, Buhrke K, Bell R, Casjens SR, Longman RS, Round JL. 2019. Expansion of bacteriophages is linked to aggravated intestinal inflammation and colitis. Cell Host Microbe 25:285–99Germ-free mice treated with a phage cocktail exhibit TLR9-dependent immune cell activation
143. Barr JJ. 2017. A bacteriophages journey through the human body. Immunol. Rev. 279:1106–22
144. Pacífico C, Hilbert M, Sofka D, Dinhopl N, Pap IJ et al. 2019. Natural occurrence of Escherichia coli-infecting bacteriophages in clinical samples. Front. Microbiol. 10:2484
145. Guillot A, Tacke F. 2019. Liver macrophages: old dogmas and new insights. Hepatol. Commun. 3:6730–43
146. Hodyra-Stefaniak K, Miernikiewicz P, Drapała J, Drab M, Jonczyk-Matysiak E et al. 2015. Mammalian host-versus-phage immune response determines phage fate in vivo. Sci. Rep. 5:114802
147. Ghose C, Ly M, Schwanemann LK, Shin JH, Atab K et al. 2019. The virome of cerebrospinal fluid: viruses where we once thought there were none. Front. Microbiol. 10:2061
148. ecor PR, Michaels LA, Smigiel KS, Rohani MG, Jennings LK et al. 2017. Filamentous bacteriophage produced by Pseudomonas aeruginosa alters the inflammatory response and promotes noninvasive infection in vivo. Infect. Immun. 85:1e00648-16
149. Zaczek M, Górski A, Skaradzińska A, Łusiak-Szelachowska M, Weber-D'browska B. 2019. Phage penetration of eukaryotic cells: practical implications. Future Virol 14:745–60
150. Tian Y, Wu M, Liu X, Liu Z, Zhou Q et al. 2015. Probing the endocytic pathways of the filamentous bacteriophage in live cells using ratiometric pH fluorescent indicator. Adv. Healthc. Mater. 4:3413–19
151. Dedrick RM, Guerrero-Bustamante CA, Garlena RA, Russell DA, Ford K et al. 2019. Engineered bacteriophages for treatment of a patient with a disseminated drug-resistant Mycobacterium abscessus. Nat. Med. 25:5730–33
152. Manickan E, Karem KL, Rouse BT. 2017. DNA vaccines—a modern gimmick or a boon to vaccinology? Crit. Rev. Immunol. 37:2–6483–98
153. Bodner K, Melkonian AL, Covert MW. 2021. The enemy of my enemy: new insights regarding bacteriophage–mammalian cell interactions. Trends Microbiol 29:6528–41
154. Hess KL, Jewell CM. 2020. Phage display as a tool for vaccine and immunotherapy development. Bioeng. Transl. Med. 5:1e10142
155. Kawasaki T, Kawai T. 2014. Toll-like receptor signaling pathways. Front. Immunol. 5:461
156. Hashiguchi S, Yamaguchi Y, Takeuchi O, Akira S, Sugimura K. 2010. Immunological basis of M13 phage vaccine: regulation under MyD88 and TLR9 signaling. Biochem. Biophys. Res. Commun. 402:119–22
157. Sweere JM, Van Belleghem JD, Ishak H, Bach MS, Popescu M et al. 2019. Bacteriophage trigger antiviral immunity and prevent clearance of bacterial infection. Science 363:6434 eaat 9691 Filamentous Pf phage downregulates myeloid cell inflammation in a TLR3-dependent manner
158. Basu R, Zhai L, Contreras A, Tumban E. 2018. Immunization with phage virus-like particles displaying Zika virus potential B-cell epitopes neutralizes Zika virus infection of monkey kidney cells. Vaccine 36:101256–64
159. Wang L, Gao J, Lan X, Zhao H, Shang X et al. 2019. Identification of combined T-cell and B-cell reactive Echinococcus granulosus 95 antigens for the potential development of a multi-epitope vaccine. Ann. Transl. Med. 7:22652
160. Popescu et al., "Bacteriophages and the Immune System," Annual Review of Virology, 2021.
161. Majewska et al., "Mammalian Host-Versus-Phage Immune Response," Scientific Reports, 2015.
162. Popescu et al., "Phage Interaction with Adaptive Immune Cells," Frontiers in Microbiology, 2023.
163. Gorski et al., "Therapeutic Phages as Modulators of the Immune Response," Clinical Infectious Diseases, 2023.
164. Roach and Debarbieux, "Bacteriophages and the Immune System," PubMed, 2021.
165. Huo et al., "Phage-specific antibodies: are they a hurdle for the success of phage therapy?" Essays in Biochemistry, 2024.
166. Majewska et al., "Induction of Phage-Specific Antibodies by Two Therapeutic Staphylococcal Bacteriophages," Frontiers in Immunology, 2019.
167. Merril et al., "Anti-phage serum antibody responses and the outcome of phage therapy," Frontiers in Immunology, 2020.
168. Klimuk et al., "Phage K exposure generates phage-neutralizing activity," Antimicrobial Agents and Chemotherapy, 2024.
169. Gorski et al., "Contribution of the Immune Response to Phage Therapy," Journal of Immunology, 2018
170. Danis-Wlodarczyk et al., "Induction of Phage-Specific Antibodies by Therapeutic Phages," Frontiers in Immunology, 2019.
171. Górski et al., "Pharmacokinetics and Biodistribution of Phages and their Applications," PMC, 2023.
172. Brandtzaeg, "Translocalized IgA mediates neutralization and stimulates innate immunity," PNAS, 2014.
173. Danis-Wlodarczyk et al., Frontiers in Immunology, 2019.
174. Górski et al., PMC, 2023.
175. Brandtzaeg, PNAS, 2014.
176. Bunker JJ et al., "Microbiota-antibody interactions that regulate gut homeostasis," Cell Host Microbe, 2021.
177. Barr JJ et al., "Bacteriophage adhering to mucus provide a non–host-derived immunity," PNAS, 2013.
178. Gutzeit C et al., "Roles of Secretory Immunoglobulin A in Host-Microbiota Interactions in the Gut Ecosystem," Frontiers in Microbiology, 2022.
179. Carvalho GB, Costa LE, Lage DP, Ramos FF, Santos TTO et al. 2019. High-through identification of T cell-specific phage-exposed mimotopes using PBMCs from tegumentary leishmaniasis patients and their use as vaccine candidates against Leishmania amazonensis infection. Parasitology 146:3322–32
180. Iwagami Y, Casulli S, Nagaoka K, Kim M, Carlson RI et al. 2017. Lambda phage-based vaccine induces antitumor immunity in hepatocellular carcinoma. Heliyon 3:900407
181. Kumar AB, Mishrad AAK, Prakash C, Priyadarshini A, Rawat M 2018. Immunization with Salmonella Abortusequi phage lysate protects guinea pig against the virulent challenge of SAE-742. Biologicals 56:24–28
182. Bodner K, Melkonian AL, Barth AIM, Kudo T, Tanouchi Y, Covert MW. 2020. Engineered fluorescent E. coli lysogens allow live-cell imaging of functional prophage induction triggered inside macrophages. Cell Syst 10:3254–64
183. Tiwari BR, Kim S, Rahman M, Kim J. 2011. Antibacterial efficacy of lytic Pseudomonas bacteriophage in normal and neutropenic mice models. J. Microbiol. 49:6994–99
184. Roach DR, Leung CY, Henry M, Morello E, Singh D et al. 2017. Synergy between the host immune system and bacteriophage is essential for successful phage therapy against an acute respiratory pathogen. Cell Host Microbe 22:138–47. e4Phages work synergistically with neutrophils to protect in a murine model of Pseudomonas aeruginosa pneumonia.
185. Jończyk-Matysiak E, Łusiak Szelachowska M, Kłak M, Bubak B, Międzybrodzki R et al. 2015. The effect of bacteriophage preparations on intracellular killing of bacteria by phagocytes. J. Immunol. Res. 2015:482863
186. Bocian K, Borysowski J, Zarzycki M, Wierzbicki P, Klosowska D et al. 2016. LPS-activated monocytes are unresponsive to T4 phage and T4-generated Escherichia coli lysate. Front. Microbiol. 7:1356
187. Zhvania P, Hoyle NS, Nadareishvili L, Nizharadze D, Kutateladze M. 2017. Phage therapy in a 16-year-old boy with Netherton syndrome. Front. Med. 4:94
188. Burgener EB, Sweere JM, Bach MS, Secor PR, Haddock N et al. 2019. Filamentous bacteriophages are associated with chronic Pseudomonas lung infections and antibiotic resistance in cystic fibrosis. Sci. Transl. Med. 11:488eaau9748
189. Jahn MT, Arkhipova K, Markert SM, Stigloher C, Lachnit T et al. 2019. A phage protein aids bacterial symbionts in eukaryote immune evasion. Cell Host Microbe 26:4542–50.e5
190. Van elleghem JD, Clement F, Merabishvili M, Lavigne R, Vaneechoutte M et al. 2017. Pro- and anti-inflammatory responses of peripheral blood mononuclear cells induced by Staphylococcus aureus and Pseudomonas aeruginosa phages. Sci. Rep 7:18004
191. Tao P, Zhu J, Mahalingam M, Batra H, Rao VB. 2019. Bacteriophage T4 nanoparticles for vaccine delivery against infectious diseases. Adv. Drug Deliv. Rev. 145:57–72
192. Dufour N, Henry M, Ricard J-D, Debarbieux L, Khan Mirzaei M et al. 2016. Commentary: morphologically distinct Escherichia coli bacteriophages differ in their efficacy and ability to stimulate cytokine release in vitro. Front. Microbiol. 7:1029
193. Dąbrowska K, Miernikiewicz P, Piotrowicz A, Hodyra K, Owczarek B et al. 2014. Immunogenicity studies of proteins forming the T4 phage head surface. J. Virol. 88:2112551–57
194. Lotfi Z, Golchin M, Khalili-Yazdi A, Khalili M. 2019. Immunological properties of the SLLTEVET epitope of Influenza A virus in multiple display on filamentous M13 phage. Comp. Immunol. Microbiol. Infect. Dis. 65:76–80
195. Majewska J, Kaźmierczak Z, Lahutta K, Lecion D, Szymczak A et al. 2019. Induction of phage-specific antibodies by two therapeutic staphylococcal bacteriophages administered per os. Front. Immunol. 14:102607
196. Hodyra Stefaniak K, Lahutta K, Majewska J, Kaźmierczak Z, Lecion D et al. 2019. Bacteriophages engineered to display foreign peptides may become short-circulating phages. Microb. Biotechnol. 12:4730–41
197. Sartorius R, Pisu P, D'Apice L, Pizzella L, Romano C et al. 2008. The use of filamentous bacteriophage fd to deliver MAGE-A10 or MAGE-A3 HLA-A2-restricted peptides and to induce strong antitumor CTL responses. J. Immunol. 180:63719–28
198. Medeea Popescu1,2, Jonas D. Van Belleghem1, Arya Khosravi1 and Paul L. Bollyky1 ANNUAL REVIEW OF VIROLOGY Volume 8, 2021 Vol. 8:415-435
199. Yan, W. X. et al. Functionally diverse type V CRISPR–Cas systems. Science 363, 88–91 (2019).
200. Shmakov, S. et al. Diversity and evolution of class 2 CRISPR–Cas systems. Nat. Rev. Microbiol. 15, 169–182 (2017).
201. Stachler, A.-E. & Marchfelder, A. Gene repression in Haloarchaea using the CRISPR (clustered regularly interspaced short palindromic repeats)–Cas I-B system. J. Biol. Chem. 291, 15226–15242 (2016).
202. Toms, A. & Barrangou, R. On the global CRISPR array behavior in class I systems. Biol. Direct 12, 20 (2017).
203. Popescu M, Van Belleghem JD, Khosravi A, Bollyky PL. Bacteriophages and the Immune System. Annu Rev Virol. 2021;8(1):415–35.
204. Majewska J, Kaźmierczak Z, Legut M, et al. Interactions of Bacteriophages with Animal and Human Organisms. Int J Mol Sci. 2021 Aug 19;22(16):8937. Górski A, Miȩdzybrodzki R, Borysowski J, et al. Phage therapy: Concepts and applications. Folia Microbiol (Praha). 2019;64(2):123–31.
205. Roach DR, Debarbieux L. Phage therapy: awakening a sleeping giant. Emerg Top Life Sci. 2017;1(1):93–103.
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