The Burden of Survivors: How Can Phage Infection Impact Non-Infected Bacteria?
Abstract
:1. Introduction
2. POSEs Mediated by Phage Particles or Phage Structural Proteins
2.1. Phage Infection Influencing the Microbial Community’s Spatial Organization
2.2. Phage Virions and Phage Proteins Serving as Structural Components of Bacterial Cells and Biofilms
2.3. Other POSE Mediated by Phage Particles
3. POSE Mediated by Quorum-Sensing (QS) Signals
4. Phages Modulating the Biofilm Development
5. Other Possible Mediators of POSEs
5.1. Normal or Phage-Induced Metabolites
5.2. Peptides
5.3. Small RNAs
5.4. Extracellular Membrane Vesicles
6. Influence of Phage Selection on the Genetic Heterogeneity of Resistant Populations
7. Concluding Remarks
Author Contributions
Funding
Acknowledgments
Conflicts of Interest
References
- Twort, F.W. An investigation on the nature of ultra-microscopic viruses. Lancet 1915, 186, 1241–1243. [Google Scholar] [CrossRef]
- d’Herelle, F. Sur un microbe invisible antagonistic des bacilles disenterique. Comptes Rendus Soc. Acad. Sci. Paris 1917, 165, 373–375. [Google Scholar]
- Letarov, A.V. History of Early Bacteriophage Research and Emergence of Key Concepts in Virology. Biochemistry 2020, 85, 1093–1112. [Google Scholar] [CrossRef]
- Clokie, M.R.; Millard, A.D.; Letarov, A.V.; Heaphy, S. Phages in nature. Bacteriophage 2011, 1, 31–45. [Google Scholar] [CrossRef]
- Koskella, B.; Hernandez, C.A.; Wheatley, R.M. Understanding the Impacts of Bacteriophage Viruses: From Laboratory Evolution to Natural Ecosystems. Annu. Rev. Virol. 2022, 9, 57–78. [Google Scholar] [CrossRef] [PubMed]
- Roux, S.; Emerson, J.B. Diversity in the soil virosphere: To infinity and beyond? Trends Microbiol. 2022, 30, 1025–1035. [Google Scholar] [CrossRef]
- Weinbauer, M.G. Ecology of prokaryotic viruses. FEMS Microbiol. Rev. 2004, 28, 127–181. [Google Scholar] [CrossRef] [PubMed]
- Correa, A.M.S.; Howard-Varona, C.; Coy, S.R.; Buchan, A.; Sullivan, M.B.; Weitz, J.S. Revisiting the rules of life for viruses of microorganisms. Nat. Rev. Microbiol. 2021, 19, 501–513. [Google Scholar] [CrossRef]
- Tuttle, M.J.; Buchan, A. Lysogeny in the oceans: Lessons from cultivated model systems and a reanalysis of its prevalence. Environ. Microbiol. 2020, 22, 4919–4933. [Google Scholar] [CrossRef]
- Summers, W.C. From culture as organism to organism as cell: Historical origins of bacterial genetics. J. Hist. Biol. 1991, 24, 171–190. [Google Scholar] [CrossRef]
- Penesyan, A.; Paulsen, I.T.; Kjelleberg, S.; Gillings, M.R. Three faces of biofilms: A microbial lifestyle, a nascent multicellular organism, and an incubator for diversity. NPJ Biofilms Microbiomes 2021, 7, 80. [Google Scholar] [CrossRef]
- Moormeier, D.E.; Bayles, K.W. Staphylococcus aureus biofilm: A complex developmental organism. Mol. Microbiol. 2017, 104, 365–376. [Google Scholar] [CrossRef]
- Mercier, R.; Mignot, T. Regulations governing the multicellular lifestyle of Myxococcus xanthus. Curr. Opin. Microbiol. 2016, 34, 104–110. [Google Scholar] [CrossRef] [PubMed]
- Herrero, A.; Stavans, J.; Flores, E. The multicellular nature of filamentous heterocyst-forming cyanobacteria. FEMS Microbiol. Rev. 2016, 40, 831–854. [Google Scholar] [CrossRef]
- Romero, D. Unicellular but not asocial. Life in community of a bacterium. Int. Microbiol. 2016, 19, 81–90. [Google Scholar] [CrossRef]
- Lyons, N.A.; Kolter, R. On the evolution of bacterial multicellularity. Curr. Opin. Microbiol. 2015, 24, 21–28. [Google Scholar] [CrossRef] [PubMed]
- d’Herelle, F. Bacteriophage as a Treatment in Acute Medical and Surgical Infections. Bull. N. Y. Acad. Med. 1931, 7, 329–348. [Google Scholar] [PubMed]
- d’Herelle, F. Bacteriophage and Phenomenon of Recovery; Tiflis University, Ed.; Tbilisis State UNiversity Publishing House: Tbilisi, Georgia, 1935; 274p. (In Russian) [Google Scholar]
- Mousavi, S.M.; Babakhani, S.; Moradi, L.; Karami, S.; Shahbandeh, M.; Mirshekar, M.; Mohebi, S.; Moghadam, M.T. Bacteriophage as a Novel Therapeutic Weapon for Killing Colistin-Resistant Multi-Drug-Resistant and Extensively Drug-Resistant Gram-Negative Bacteria. Curr. Microbiol. 2021, 78, 4023–4036. [Google Scholar] [CrossRef]
- Kaur, M.; Williams, M.; Bissett, A.; Ross, T.; Bowman, J.P. Effect of abattoir, livestock species and storage temperature on bacterial community dynamics and sensory properties of vacuum packaged red meat. Food Microbiol. 2021, 94, 103648. [Google Scholar] [CrossRef] [PubMed]
- Vlassov, V.V.; Tikunova, N.V.; Morozova, V.V. Bacteriophages as Therapeutic Preparations: What Restricts Their Application in Medicine. Biochemistry 2020, 85, 1350–1361. [Google Scholar] [CrossRef] [PubMed]
- Islam, M.R.; Martinez-Soto, C.E.; Lin, J.T.; Khursigara, C.M.; Barbut, S.; Anany, H. A systematic review from basics to omics on bacteriophage applications in poultry production and processing. Crit. Rev. Food Sci. Nutr. 2021, 1–33. [Google Scholar] [CrossRef]
- Eid, S.; Tolba, H.M.N.; Hamed, R.I.; Al-Atfeehy, N.M. Bacteriophage therapy as an alternative biocontrol against emerging multidrug resistant E. coli in broilers. Saudi J. Biol. Sci. 2022, 29, 3380–3389. [Google Scholar] [CrossRef]
- Niu, Y.D.; Hyun, J.E.; Nguyen, N. Bacteriophage Effectiveness for Biocontrol of Foodborne Pathogens Evaluated via High-Throughput Settings. J. Vis. Exp. 2021, 174, e62812. [Google Scholar] [CrossRef]
- Kering, K.K.; Kibii, B.J.; Wei, H. Biocontrol of phytobacteria with bacteriophage cocktails. Pest. Manag. Sci. 2019, 75, 1775–1781. [Google Scholar] [CrossRef]
- Chin, W.H.; Kett, C.; Cooper, O.; Museler, D.; Zhang, Y.; Bamert, R.S.; Patwa, R.; Woods, L.C.; Devendran, C.; Korneev, D.; et al. Bacteriophages evolve enhanced persistence to a mucosal surface. Proc. Natl. Acad. Sci. USA 2022, 119, e2116197119. [Google Scholar] [CrossRef] [PubMed]
- Savvichev, A.S.; Babenko, V.V.; Lunina, O.N.; Letarova, M.A.; Boldyreva, D.I.; Veslopolova, E.F.; Demidenko, N.A.; Kokryatskaya, N.M.; Krasnova, E.D.; Gaisin, V.A.; et al. Sharp water column stratification with an extremely dense microbial population in a small meromictic lake, Trekhtzvetnoe. Environ. Microbiol. 2018, 20, 3784–3797. [Google Scholar] [CrossRef] [PubMed]
- Chevallereau, A.; Pons, B.J.; van Houte, S.; Westra, E.R. Interactions between bacterial and phage communities in natural environments. Nat. Rev. Microbiol. 2022, 20, 49–62. [Google Scholar] [CrossRef]
- Mangalea, M.R.; Duerkop, B.A. Fitness Trade-Offs Resulting from Bacteriophage Resistance Potentiate Synergistic Antibacterial Strategies. Infect. Immun. 2020, 88, e00926-19. [Google Scholar] [CrossRef]
- Letarov, A.V. Current Concepts in Bacteriophage Biology; Ulyanovsk State Agricultural Academy: Moscow, Russia, 2019; 384p. (In Russian) [Google Scholar]
- Drobiazko, A.Y.; Kasimova, A.A.; Evseev, P.V.; Shneider, M.M.; Klimuk, E.I.; Shashkov, A.S.; Dmitrenok, A.S.; Chizhov, A.O.; Slukin, P.V.; Skryabin, Y.P.; et al. Capsule-Targeting Depolymerases Derived from Acinetobacter baumannii Prophage Regions. Int. J. Mol. Sci. 2022, 23, 4971. [Google Scholar] [CrossRef]
- Oliveira, H.; Mendes, A.; Fraga, A.G.; Ferreira, A.; Pimenta, A.I.; Mil-Homens, D.; Fialho, A.M.; Pedrosa, J.; Azeredo, J. K2 Capsule Depolymerase Is Highly Stable, Is Refractory to Resistance, and Protects Larvae and Mice from Acinetobacter baumannii Sepsis. Appl. Environ. Microbiol. 2019, 85, e00934-19. [Google Scholar] [CrossRef]
- Visnapuu, A.; Van der Gucht, M.; Wagemans, J.; Lavigne, R. Deconstructing the Phage-Bacterial Biofilm Interaction as a Basis to Establish New Antibiofilm Strategies. Viruses 2022, 14, 1057. [Google Scholar] [CrossRef]
- Lu, T.K.; Collins, J.J. Dispersing biofilms with engineered enzymatic bacteriophage. Proc. Natl. Acad. Sci. USA 2007, 104, 11197–11202. [Google Scholar] [CrossRef]
- Sauer, K.; Stoodley, P.; Goeres, D.M.; Hall-Stoodley, L.; Burmolle, M.; Stewart, P.S.; Bjarnsholt, T. The biofilm life cycle: Expanding the conceptual model of biofilm formation. Nat. Rev. Microbiol. 2022, 20, 608–620. [Google Scholar] [CrossRef] [PubMed]
- Dawan, J.; Ahn, J. Bacterial Stress Responses as Potential Targets in Overcoming Antibiotic Resistance. Microorganisms 2022, 10, 1385. [Google Scholar] [CrossRef] [PubMed]
- Jennings, M.P.; Day, C.J.; Atack, J.M. How bacteria utilize sialic acid during interactions with the host: Snip, snatch, dispatch, match and attach. Microbiology 2022, 168, 001157. [Google Scholar] [CrossRef] [PubMed]
- Konishi, H.; Hio, M.; Kobayashi, M.; Takase, R.; Hashimoto, W. Bacterial chemotaxis towards polysaccharide pectin by pectin-binding protein. Sci. Rep. 2020, 10, 3977. [Google Scholar] [CrossRef] [PubMed]
- Asadpoor, M.; Ithakisiou, G.N.; Henricks, P.A.J.; Pieters, R.; Folkerts, G.; Braber, S. Non-Digestible Oligosaccharides and Short Chain Fatty Acids as Therapeutic Targets against Enterotoxin-Producing Bacteria and Their Toxins. Toxins 2021, 13, 175. [Google Scholar] [CrossRef] [PubMed]
- Chutipongtanate, S.; Morrow, A.L.; Newburg, D.S. Human Milk Oligosaccharides: Potential Applications in COVID-19. Biomedicines 2022, 10, 346. [Google Scholar] [CrossRef]
- Bae, B.; Kim, H.; Park, H.; Koh, Y.J.; Bae, S.J.; Ha, K.T. Anti-Angiogenic Property of Free Human Oligosaccharides. Biomolecules 2021, 11, 775. [Google Scholar] [CrossRef] [PubMed]
- Rice, S.A.; Tan, C.H.; Mikkelsen, P.J.; Kung, V.; Woo, J.; Tay, M.; Hauser, A.; McDougald, D.; Webb, J.S.; Kjelleberg, S. The biofilm life cycle and virulence of Pseudomonas aeruginosa are dependent on a filamentous prophage. ISME J. 2009, 3, 271–282. [Google Scholar] [CrossRef]
- Ismail, M.H.; Michie, K.A.; Goh, Y.F.; Noorian, P.; Kjelleberg, S.; Duggin, I.G.; McDougald, D.; Rice, S.A. The Repressor C Protein, Pf4r, Controls Superinfection of Pseudomonas aeruginosa PAO1 by the Pf4 Filamentous Phage and Regulates Host Gene Expression. Viruses 2021, 13, 1614. [Google Scholar] [CrossRef] [PubMed]
- Kulikov, E.E.; Golomidova, A.K.; Efimov, A.D.; Belalov, I.S.; Letarova, M.A.; Zdorovenko, E.L.; Knirel, Y.A.; Dmitrenok, A.S.; Letarov, A.V. Equine Intestinal O-Seroconverting Temperate Coliphage Hf4s: Genomic and Biological Characterization. Appl. Environ. Microbiol. 2021, 87, e0112421. [Google Scholar] [CrossRef]
- Mitarai, N.; Brown, S.; Sneppen, K. Population Dynamics of Phage and Bacteria in Spatially Structured Habitats Using Phage lambda and Escherichia coli. J. Bacteriol. 2016, 198, 1783–1793. [Google Scholar] [CrossRef] [PubMed]
- Hnatko, S.I. Concentric ring formation about plaques of M. phlei bacteriophage. Can. J. Public Health 1952, 43, 54–59. [Google Scholar] [PubMed]
- Yao, T.; Coleman, S.; Nguyen, T.V.P.; Golding, I.; Igoshin, O.A. Bacteriophage self-counting in the presence of viral replication. Proc. Natl. Acad. Sci. USA 2021, 118, e2104163118. [Google Scholar] [CrossRef]
- Murchland, I.M.; Ahlgren-Berg, A.; Pietsch, J.M.J.; Isabel, A.; Dodd, I.B.; Shearwin, K.E. Instability of CII is needed for efficient switching between lytic and lysogenic development in bacteriophage 186. Nucleic Acids Res. 2020, 48, 12030–12041. [Google Scholar] [CrossRef]
- Benler, S.; Koonin, E.V. Phage lysis-lysogeny switches and programmed cell death: Danse macabre. Bioessays 2020, 42, e2000114. [Google Scholar] [CrossRef]
- Casjens, S.R.; Hendrix, R.W. Bacteriophage lambda: Early pioneer and still relevant. Virology 2015, 479–480, 310–330. [Google Scholar] [CrossRef]
- Gama, J.A.; Reis, A.M.; Domingues, I.; Mendes-Soares, H.; Matos, A.M.; Dionisio, F. Temperate bacterial viruses as double-edged swords in bacterial warfare. PLoS ONE 2013, 8, e59043. [Google Scholar] [CrossRef]
- Brown, S.P.; Le Chat, L.; De Paepe, M.; Taddei, F. Ecology of microbial invasions: Amplification allows virus carriers to invade more rapidly when rare. Curr. Biol. 2006, 16, 2048–2052. [Google Scholar] [CrossRef]
- You, X.; Kallies, R.; Kuhn, I.; Schmidt, M.; Harms, H.; Chatzinotas, A.; Wick, L.Y. Phage co-transport with hyphal-riding bacteria fuels bacterial invasion in a water-unsaturated microbial model system. ISME J. 2022, 16, 1275–1283. [Google Scholar] [CrossRef]
- Mitchell, J.; Siboo, I.R.; Takamatsu, D.; Chambers, H.F.; Sullam, P.M. Mechanism of cell surface expression of the Streptococcus mitis platelet binding proteins PblA and PblB. Mol. Microbiol. 2007, 64, 844–857. [Google Scholar] [CrossRef]
- Bensing, B.A.; Siboo, I.R.; Sullam, P.M. Proteins PblA and PblB of Streptococcus mitis, which promote binding to human platelets, are encoded within a lysogenic bacteriophage. Infect. Immun. 2001, 69, 6186–6192. [Google Scholar] [CrossRef]
- Seo, H.S.; Xiong, Y.Q.; Mitchell, J.; Seepersaud, R.; Bayer, A.S.; Sullam, P.M. Bacteriophage lysin mediates the binding of streptococcus mitis to human platelets through interaction with fibrinogen. PLoS Pathog. 2010, 6, e1001047. [Google Scholar] [CrossRef]
- Hay, I.D.; Lithgow, T. Filamentous phages: Masters of a microbial sharing economy. EMBO Rep. 2019, 20, e47427. [Google Scholar] [CrossRef]
- Rakonjac, J.; Bennett, N.J.; Spagnuolo, J.; Gagic, D.; Russel, M. Filamentous bacteriophage: Biology, phage display and nanotechnology applications. Curr. Issues Mol. Biol. 2011, 13, 51–76. [Google Scholar] [PubMed]
- Tarafder, A.K.; von Kugelgen, A.; Mellul, A.J.; Schulze, U.; Aarts, D.; Bharat, T.A.M. Phage liquid crystalline droplets form occlusive sheaths that encapsulate and protect infectious rod-shaped bacteria. Proc. Natl. Acad. Sci. USA 2020, 117, 4724–4731. [Google Scholar] [CrossRef] [PubMed]
- Secor, P.R.; Jennings, L.K.; Michaels, L.A.; Sweere, J.M.; Singh, P.K.; Parks, W.C.; Bollyky, P.L. Biofilm assembly becomes crystal clear—Filamentous bacteriophage organize the Pseudomonas aeruginosa biofilm matrix into a liquid crystal. Microb. Cell 2015, 3, 49–52. [Google Scholar] [CrossRef] [PubMed]
- Secor, P.R.; Sweere, J.M.; Michaels, L.A.; Malkovskiy, A.V.; Lazzareschi, D.; Katznelson, E.; Rajadas, J.; Birnbaum, M.E.; Arrigoni, A.; Braun, K.R.; et al. Filamentous Bacteriophage Promote Biofilm Assembly and Function. Cell Host Microbe 2015, 18, 549–559. [Google Scholar] [CrossRef]
- Letarov, A.; Kulikov, E. The bacteriophages in human- and animal body-associated microbial communities. J. Appl. Microbiol. 2009, 107, 1–13. [Google Scholar] [CrossRef]
- Brady, J.M.; Gray, W.A.; Caldwell, M.A. The electron microscopy of bacteriophage-like particles in dental plaque. J. Dent. Res. 1977, 56, 991–993. [Google Scholar] [CrossRef] [PubMed]
- Kerebel, B.; Clergeau-Guerithault, S.; Forlot, P. Ultrastructural study of bacterial plaques from caries-free human subjects (author’s transl). Ann. Microbiol. 1975, 126, 203–229. [Google Scholar]
- Szafranski, S.P.; Slots, J.; Stiesch, M. The human oral phageome. Periodontol. 2000 2021, 86, 79–96. [Google Scholar] [CrossRef] [PubMed]
- Secor, P.R.; Burgener, E.B.; Kinnersley, M.; Jennings, L.K.; Roman-Cruz, V.; Popescu, M.; Van Belleghem, J.D.; Haddock, N.; Copeland, C.; Michaels, L.A.; et al. Pf Bacteriophage and Their Impact on Pseudomonas Virulence, Mammalian Immunity, and Chronic Infections. Front. Immunol. 2020, 11, 244. [Google Scholar] [CrossRef] [PubMed]
- Zuppi, M.; Hendrickson, H.L.; O’Sullivan, J.M.; Vatanen, T. Phages in the Gut Ecosystem. Front. Cell Infect. Microbiol. 2021, 11, 822562. [Google Scholar] [CrossRef]
- Popescu, M.; Van Belleghem, J.D.; Khosravi, A.; Bollyky, P.L. Bacteriophages and the Immune System. Annu. Rev. Virol. 2021, 8, 415–435. [Google Scholar] [CrossRef]
- Krieger, I.V.; Kuznetsov, V.; Chang, J.Y.; Zhang, J.; Moussa, S.H.; Young, R.F.; Sacchettini, J.C. The Structural Basis of T4 Phage Lysis Control: DNA as the Signal for Lysis Inhibition. J. Mol. Biol. 2020, 432, 4623–4636. [Google Scholar] [CrossRef]
- Abedon, S.T. Look Who’s Talking: T-Even Phage Lysis Inhibition, the Granddaddy of Virus-Virus Intercellular Communication Research. Viruses 2019, 11, 951. [Google Scholar] [CrossRef]
- Chevallereau, A.; Meaden, S.; Fradet, O.; Landsberger, M.; Maestri, A.; Biswas, A.; Gandon, S.; van Houte, S.; Westra, E.R. Exploitation of the Cooperative Behaviors of Anti-CRISPR Phages. Cell Host Microbe 2020, 27, 189–198.e186. [Google Scholar] [CrossRef]
- Wang, Y.; Dai, J.; Wang, X.; Wang, Y.; Tang, F. Mechanisms of interactions between bacteria and bacteriophage mediate by quorum sensing systems. Appl. Microbiol. Biotechnol. 2022, 106, 2299–2310. [Google Scholar] [CrossRef]
- Erez, Z.; Steinberger-Levy, I.; Shamir, M.; Doron, S.; Stokar-Avihail, A.; Peleg, Y.; Melamed, S.; Leavitt, A.; Savidor, A.; Albeck, S.; et al. Communication between viruses guides lysis-lysogeny decisions. Nature 2017, 541, 488–493. [Google Scholar] [CrossRef] [PubMed]
- Stokar-Avihail, A.; Tal, N.; Erez, Z.; Lopatina, A.; Sorek, R. Widespread Utilization of Peptide Communication in Phages Infecting Soil and Pathogenic Bacteria. Cell Host Microbe 2019, 25, 746–755.e5. [Google Scholar] [CrossRef] [PubMed] [Green Version]
- Bernard, C.; Li, Y.; Lopez, P.; Bapteste, E. Beyond arbitrium: Identification of a second communication system in Bacillus phage phi3T that may regulate host defense mechanisms. ISME J. 2021, 15, 545–549. [Google Scholar] [CrossRef]
- Bru, J.L.; Rawson, B.; Trinh, C.; Whiteson, K.; Hoyland-Kroghsbo, N.M.; Siryaporn, A. PQS Produced by the Pseudomonas aeruginosa Stress Response Repels Swarms Away from Bacteriophage and Antibiotics. J. Bacteriol. 2019, 201, e00383-19. [Google Scholar] [CrossRef] [PubMed]
- León-Félix, J.; Villicaña, C. The Impact of Quorum Sensing on the Modulation of Phage-Host Interactions. J. Bacteriol. 2021, 203. [Google Scholar] [CrossRef]
- Chang, C.; Yu, X.; Guo, W.; Guo, C.; Guo, X.; Li, Q.; Zhu, Y. Bacteriophage-Mediated Control of Biofilm: A Promising New Dawn for the Future. Front. Microbiol. 2022, 13, 825828. [Google Scholar] [CrossRef] [PubMed]
- Mgomi, F.C.; Yuan, L.; Chen, C.W.; Zhang, Y.S.; Yang, Z.Q. Bacteriophages: A weapon against mixed-species biofilms in the food processing environment. J. Appl. Microbiol. 2022, 133, 2107–2121. [Google Scholar] [CrossRef]
- Ferriol-Gonzalez, C.; Domingo-Calap, P. Phages for Biofilm Removal. Antibiotics 2020, 9, 268. [Google Scholar] [CrossRef]
- Wu, S.; Li, X.; Gunawardana, M.; Maguire, K.; Guerrero-Given, D.; Schaudinn, C.; Wang, C.; Baum, M.M.; Webster, P. Beta- lactam antibiotics stimulate biofilm formation in non-typeable haemophilus influenzae by up-regulating carbohydrate metabolism. PLoS ONE 2014, 9, e99204. [Google Scholar] [CrossRef]
- Strelkova, E.A.; Zhurina, M.V.; Plakunov, V.K.; Belyaev, S.S. Stimulation of biofilm formation by antibiotics. Microbiology 2012, 81, 259–262. [Google Scholar] [CrossRef]
- Tan, D.; Dahl, A.; Middelboe, M. Vibriophages Differentially Influence Biofilm Formation by Vibrio anguillarum Strains. Appl. Environ. Microbiol. 2015, 81, 4489–4497. [Google Scholar] [CrossRef]
- Tan, D.; Svenningsen, S.L.; Middelboe, M. Quorum Sensing Determines the Choice of Antiphage Defense Strategy in Vibrio anguillarum. mBio 2015, 6, e00627. [Google Scholar] [CrossRef] [Green Version]
- Zhang, B.; Yu, P.; Wang, Z.; Alvarez, P.J.J. Hormetic Promotion of Biofilm Growth by Polyvalent Bacteriophages at Low Concentrations. Environ. Sci. Technol. 2020, 54, 12358–12365. [Google Scholar] [CrossRef] [PubMed]
- Picardo, S.L.; Coburn, B.; Hansen, A.R. The microbiome and cancer for clinicians. Crit. Rev. Oncol. Hematol. 2019, 141, 1–12. [Google Scholar] [CrossRef] [PubMed]
- Talapko, J.; Skrlec, I. The Principles, Mechanisms, and Benefits of Unconventional Agents in the Treatment of Biofilm Infection. Pharmaceuticals 2020, 13, 299. [Google Scholar] [CrossRef]
- Hosseinidoust, Z.; Tufenkji, N.; van de Ven, T.G. Formation of biofilms under phage predation: Considerations concerning a biofilm increase. Biofouling 2013, 29, 457–468. [Google Scholar] [CrossRef] [PubMed]
- Fernandez, L.; Gonzalez, S.; Campelo, A.B.; Martinez, B.; Rodriguez, A.; Garcia, P. Low-level predation by lytic phage phiIPLA-RODI promotes biofilm formation and triggers the stringent response in Staphylococcus aureus. Sci. Rep. 2017, 7, 40965. [Google Scholar] [CrossRef]
- Holger, D.; Kebriaei, R.; Morrisette, T.; Lev, K.; Alexander, J.; Rybak, M. Clinical Pharmacology of Bacteriophage Therapy: A Focus on Multidrug-Resistant Pseudomonas aeruginosa Infections. Antibiotics 2021, 10, 556. [Google Scholar] [CrossRef]
- Danis-Wlodarczyk, K.; Dabrowska, K.; Abedon, S.T. Phage Therapy: The Pharmacology of Antibacterial Viruses. Curr. Issues Mol. Biol. 2021, 40, 81–164. [Google Scholar] [CrossRef]
- Spari, D.; Beldi, G. Extracellular ATP as an Inter-Kingdom Signaling Molecule: Release Mechanisms by Bacteria and Its Implication on the Host. Int. J. Mol. Sci. 2020, 21, 5590. [Google Scholar] [CrossRef]
- Mempin, R.; Tran, H.; Chen, C.; Gong, H.; Kim Ho, K.; Lu, S. Release of extracellular ATP by bacteria during growth. BMC Microbiol. 2013, 13, 301. [Google Scholar] [CrossRef]
- Xi, C.; Wu, J. dATP/ATP, a multifunctional nucleotide, stimulates bacterial cell lysis, extracellular DNA release and biofilm development. PLoS ONE 2010, 5, e13355. [Google Scholar] [CrossRef] [PubMed] [Green Version]
- Jacobson, T.B.; Callaghan, M.M.; Amador-Noguez, D. Hostile Takeover: How Viruses Reprogram Prokaryotic Metabolism. Annu. Rev. Microbiol. 2021, 75, 515–539. [Google Scholar] [CrossRef]
- Warwick-Dugdale, J.; Buchholz, H.H.; Allen, M.J.; Temperton, B. Host-hijacking and planktonic piracy: How phages command the microbial high seas. Virol. J. 2019, 16, 15. [Google Scholar] [CrossRef] [PubMed]
- Weigele, P.; Raleigh, E.A. Biosynthesis and Function of Modified Bases in Bacteria and Their Viruses. Chem. Rev. 2016, 116, 12655–12687. [Google Scholar] [CrossRef] [PubMed]
- Kulikov, E.E.; Golomidova, A.K.; Letarova, M.A.; Kostryukova, E.S.; Zelenin, A.S.; Prokhorov, N.S.; Letarov, A.V. Genomic sequencing and biological characteristics of a novel Escherichia coli bacteriophage 9g, a putative representative of a new Siphoviridae genus. Viruses 2014, 6, 5077–5092. [Google Scholar] [CrossRef] [PubMed]
- Thiaville, J.J.; Kellner, S.M.; Yuan, Y.; Hutinet, G.; Thiaville, P.C.; Jumpathong, W.; Mohapatra, S.; Brochier-Armanet, C.; Letarov, A.V.; Hillebrand, R.; et al. Novel genomic island modifies DNA with 7-deazaguanine derivatives. Proc. Natl. Acad. Sci. USA 2016, 113, E1452–E1459. [Google Scholar] [CrossRef]
- Nagaraja, S.; Cai, M.W.; Sun, J.; Varet, H.; Sarid, L.; Trebicz-Geffen, M.; Shaulov, Y.; Mazumdar, M.; Legendre, R.; Coppee, J.Y.; et al. Queuine Is a Nutritional Regulator of Entamoeba histolytica Response to Oxidative Stress and a Virulence Attenuator. mBio 2021, 12, e03549-20. [Google Scholar] [CrossRef] [PubMed]
- Marchetti, M.; Capela, D.; Poincloux, R.; Benmeradi, N.; Auriac, M.C.; Le Ru, A.; Maridonneau-Parini, I.; Batut, J.; Masson-Boivin, C. Queuosine biosynthesis is required for sinorhizobium meliloti-induced cytoskeletal modifications on HeLa Cells and symbiosis with Medicago truncatula. PLoS ONE 2013, 8, e56043. [Google Scholar] [CrossRef] [PubMed]
- Letarova, M.A.; Kulikov, E.E.; Golomidova, A.K.; Prokhorov, N.S.; Kutuzova, N.M.; Letarov, A.V.; Strelkova, D.M.; Bakumova, A.D. Metastable associations formed in the phage-host system, isolated from the horse feces. Her. Ulyanovsk. Agric. Acad. 2013, 3, 57–61. (In Russian) [Google Scholar]
- Bull, J.J.; Vegge, C.S.; Schmerer, M.; Chaudhry, W.N.; Levin, B.R. Phenotypic resistance and the dynamics of bacterial escape from phage control. PLoS ONE 2014, 9, e94690. [Google Scholar] [CrossRef] [PubMed]
- Deo, S.; Turton, K.L.; Kainth, T.; Kumar, A.; Wieden, H.J. Strategies for improving antimicrobial peptide production. Biotechnol. Adv. 2022, 59, 107968. [Google Scholar] [CrossRef]
- Zhu, Y.; Hao, W.; Wang, X.; Ouyang, J.; Deng, X.; Yu, H.; Wang, Y. Antimicrobial peptides, conventional antibiotics, and their synergistic utility for the treatment of drug-resistant infections. Med. Res. Rev. 2022, 42, 1377–1422. [Google Scholar] [CrossRef] [PubMed]
- Heilbronner, S.; Krismer, B.; Brotz-Oesterhelt, H.; Peschel, A. The microbiome-shaping roles of bacteriocins. Nat. Rev. Microbiol. 2021, 19, 726–739. [Google Scholar] [CrossRef] [PubMed]
- Wu, Y.; Pang, X.; Wu, Y.; Liu, X.; Zhang, X. Enterocins: Classification, Synthesis, Antibacterial Mechanisms and Food Applications. Molecules 2022, 27, 2258. [Google Scholar] [CrossRef]
- Frimodt-Moller, J.; Campion, C.; Nielsen, P.E.; Lobner-Olesen, A. Translocation of non-lytic antimicrobial peptides and bacteria penetrating peptides across the inner membrane of the bacterial envelope. Curr. Genet. 2022, 68, 83–90. [Google Scholar] [CrossRef]
- de la Fuente-Nunez, C.; Reffuveille, F.; Haney, E.F.; Straus, S.K.; Hancock, R.E. Broad-spectrum anti-biofilm peptide that targets a cellular stress response. PLoS Pathog. 2014, 10, e1004152. [Google Scholar] [CrossRef]
- De Smet, J.; Wagemans, J.; Boon, M.; Ceyssens, P.J.; Voet, M.; Noben, J.P.; Andreeva, J.; Ghilarov, D.; Severinov, K.; Lavigne, R. The bacteriophage LUZ24 “Igy” peptide inhibits the Pseudomonas DNA gyrase. Cell Rep. 2021, 36, 109567. [Google Scholar] [CrossRef]
- Wagemans, J.; Delattre, A.S.; Uytterhoeven, B.; De Smet, J.; Cenens, W.; Aertsen, A.; Ceyssens, P.J.; Lavigne, R. Antibacterial phage ORFans of Pseudomonas aeruginosa phage LUZ24 reveal a novel MvaT inhibiting protein. Front. Microbiol. 2015, 6, 1242. [Google Scholar] [CrossRef]
- Meyer, J.R.; Dobias, D.T.; Weitz, J.S.; Barrick, J.E.; Quick, R.T.; Lenski, R.E. Repeatability and contingency in the evolution of a key innovation in phage lambda. Science 2012, 335, 428–432. [Google Scholar] [CrossRef]
- Christen, M.; Beusch, C.; Bosch, Y.; Cerletti, D.; Flores-Tinoco, C.E.; Del Medico, L.; Tschan, F.; Christen, B. Quantitative Selection Analysis of Bacteriophage phiCbK Susceptibility in Caulobacter crescentus. J. Mol. Biol. 2016, 428, 419–430. [Google Scholar] [CrossRef] [PubMed]
- Kashiwagi, A.; Kitamura, H.; Sano Tsushima, F. Characterization of a single mutation in TraQ in a strain of Escherichia coli partially resistant to Qbeta infection. Front. Microbiol. 2015, 6, 124. [Google Scholar] [CrossRef] [PubMed]
- Lacqua, A.; Wanner, O.; Colangelo, T.; Martinotti, M.G.; Landini, P. Emergence of biofilm-forming subpopulations upon exposure of Escherichia coli to environmental bacteriophages. Appl. Environ. Microbiol. 2006, 72, 956–959. [Google Scholar] [CrossRef] [PubMed] [Green Version]
- Janissen, R.; Arens, M.M.A.; Vtyurina, N.N.; Rivai, Z.; Sunday, N.D.; Eslami-Mossallam, B.; Gritsenko, A.A.; Laan, L.; de Ridder, D.; Artsimovitch, I.; et al. Global DNA Compaction in Stationary-Phase Bacteria Does Not Affect Transcription. Cell 2018, 174, 1188–1199.e14. [Google Scholar] [CrossRef] [PubMed]
- Park, C.; Jin, Y.; Kim, Y.J.; Jeong, H.; Seong, B.L. RNA-binding as chaperones of DNA binding proteins from starved cells. Biochem. Biophys. Res. Commun. 2020, 524, 484–489. [Google Scholar] [CrossRef]
- Jorgensen, L.V.G. Zebrafish as a Model for Fish Diseases in Aquaculture. Pathogens 2020, 9, 609. [Google Scholar] [CrossRef]
- Dudeja, S.S.; Suneja-Madan, P.; Paul, M.; Maheswari, R.; Kothe, E. Bacterial endophytes: Molecular interactions with their hosts. J. Basic Microbiol. 2021, 61, 475–505. [Google Scholar] [CrossRef]
- Riahi Rad, Z.; Riahi Rad, Z.; Goudarzi, H.; Goudarzi, M.; Mahmoudi, M.; Yasbolaghi Sharahi, J.; Hashemi, A. MicroRNAs in the interaction between host-bacterial pathogens: A new perspective. J. Cell Physiol. 2021, 236, 6249–6270. [Google Scholar] [CrossRef]
- Nejman-Falenczyk, B.; Bloch, S.; Licznerska, K.; Dydecka, A.; Felczykowska, A.; Topka, G.; Wegrzyn, A.; Wegrzyn, G. A small, microRNA-size, ribonucleic acid regulating gene expression and development of Shiga toxin-converting bacteriophage Phi24Beta. Sci. Rep. 2015, 5, 10080. [Google Scholar] [CrossRef]
- Nejman-Falenczyk, B.; Bloch, S.; Licznerska, K.; Felczykowska, A.; Dydecka, A.; Wegrzyn, A.; Wegrzyn, G. Small regulatory RNAs in lambdoid bacteriophages and phage-derived plasmids: Not only antisense. Plasmid 2015, 78, 71–78. [Google Scholar] [CrossRef]
- Alikina, O.V.; Glazunova, O.A.; Bykov, A.A.; Kiselev, S.S.; Tutukina, M.N.; Shavkunov, K.S.; Ozoline, O.N. A cohabiting bacterium alters the spectrum of short RNAs secreted by Escherichia coli. FEMS Microbiol. Lett. 2018, 365, fny262. [Google Scholar] [CrossRef]
- Markelova, N.; Glazunova, O.; Alikina, O.; Panyukov, V.; Shavkunov, K.; Ozoline, O. Suppression of Escherichia coli Growth Dynamics via RNAs Secreted by Competing Bacteria. Front. Mol. Biosci. 2021, 8, 609979. [Google Scholar] [CrossRef] [PubMed]
- Kornienko, M.; Fisunov, G.; Bespiatykh, D.; Kuptsov, N.; Gorodnichev, R.; Klimina, K.; Kulikov, E.; Ilina, E.; Letarov, A.; Shitikov, E. Transcriptional Landscape of Staphylococcus aureus Kayvirus Bacteriophage vB_SauM-515A1. Viruses 2020, 12, 1320. [Google Scholar] [CrossRef] [PubMed]
- McMillan, H.M.; Kuehn, M.J. The extracellular vesicle generation paradox: A bacterial point of view. EMBO J. 2021, 40, e108174. [Google Scholar] [CrossRef] [PubMed]
- Han, E.C.; Choi, S.Y.; Lee, Y.; Park, J.W.; Hong, S.H.; Lee, H.J. Extracellular RNAs in periodontopathogenic outer membrane vesicles promote TNF-alpha production in human macrophages and cross the blood–brain barrier in mice. FASEB J. 2019, 33, 13412–13422. [Google Scholar] [CrossRef] [PubMed]
- Choi, J.W.; Kwon, T.Y.; Hong, S.H.; Lee, H.J. Isolation and Characterization of a microRNA-size Secretable Small RNA in Streptococcus sanguinis. Cell Biochem. Biophys. 2018, 76, 293–301. [Google Scholar] [CrossRef] [PubMed]
- Choi, J.W.; Um, J.H.; Cho, J.H.; Lee, H.J. Tiny RNAs and their voyage via extracellular vesicles: Secretion of bacterial small RNA and eukaryotic microRNA. Exp. Biol. Med. 2017, 242, 1475–1481. [Google Scholar] [CrossRef] [PubMed]
- Tzipilevich, E.; Habusha, M.; Ben-Yehuda, S. Acquisition of Phage Sensitivity by Bacteria through Exchange of Phage Receptors. Cell 2017, 168, 186–199.e12. [Google Scholar] [CrossRef]
- Endres, J.L.; Chaudhari, S.S.; Zhang, X.; Prahlad, J.; Wang, S.Q.; Foley, L.A.; Luca, S.; Bose, J.L.; Thomas, V.C.; Bayles, K.W. The Staphylococcus aureus CidA and LrgA Proteins Are Functional Holins Involved in the Transport of By-Products of Carbohydrate Metabolism. mBio 2022, 13, e0282721. [Google Scholar] [CrossRef]
- Yasuda, M.; Yamamoto, T.; Nagakubo, T.; Morinaga, K.; Obana, N.; Nomura, N.; Toyofuku, M. Phage Genes Induce Quorum Sensing Signal Release through Membrane Vesicle Formation. Microbes Environ. 2022, 37, ME21067. [Google Scholar] [CrossRef]
- Pasqua, M.; Zennaro, A.; Trirocco, R.; Fanelli, G.; Micheli, G.; Grossi, M.; Colonna, B.; Prosseda, G. Modulation of OMV Production by the Lysis Module of the DLP12 Defective Prophage of Escherichia coli K12. Microorganisms 2021, 9, 369. [Google Scholar] [CrossRef] [PubMed]
- Cahill, J.; Young, R. Phage Lysis: Multiple Genes for Multiple Barriers. Adv. Virus Res. 2019, 103, 33–70. [Google Scholar] [CrossRef] [PubMed]
- Toyofuku, M.; Nomura, N.; Eberl, L. Types and origins of bacterial membrane vesicles. Nat. Rev. Microbiol. 2019, 17, 13–24. [Google Scholar] [CrossRef] [PubMed]
- Naradasu, D.; Miran, W.; Sharma, S.; Takenawa, S.; Soma, T.; Nomura, N.; Toyofuku, M.; Okamoto, A. Biogenesis of Outer Membrane Vesicles Concentrates the Unsaturated Fatty Acid of Phosphatidylinositol in Capnocytophaga ochracea. Front. Microbiol. 2021, 12, 682685. [Google Scholar] [CrossRef] [PubMed]
- Toyofuku, M. Bacterial communication through membrane vesicles. Biosci. Biotechnol. Biochem. 2019, 83, 1599–1605. [Google Scholar] [CrossRef] [PubMed]
- Luria, S.E.; Delbruck, M. Mutations of bacteria from virus sensitivity to virus resistance. Genetics 1943, 28, 491–511. [Google Scholar] [CrossRef]
- Pal, C.; Macia, M.D.; Oliver, A.; Schachar, I.; Buckling, A. Coevolution with viruses drives the evolution of bacterial mutation rates. Nature 2007, 450, 1079–1081. [Google Scholar] [CrossRef]
- Morgan, A.D.; Bonsall, M.B.; Buckling, A. Impact of bacterial mutation rate on coevolutionary dynamics between bacteria and phages. Evolution 2010, 64, 2980–2987. [Google Scholar] [CrossRef]
- Gomez, P.; Buckling, A. Coevolution with phages does not influence the evolution of bacterial mutation rates in soil. ISME J. 2013, 7, 2242–2244. [Google Scholar] [CrossRef]
- Scott, J.; Van Nguyen, S.; King, C.J.; Hendrickson, C.G.; Mcshan, W.M. Phage-Like Streptococcus pyogenes Chromosomal Islands (SpyCI) and Mutator Phenotypes: Control by Growth State and Rescue by a SpyCI-Encoded Promoter. Front. Microbiol. 2012, 3, 317. [Google Scholar] [CrossRef]
- Wang, D.; Ning, Q.; Deng, Z.; Zhang, M.; You, J. Role of environmental stresses in elevating resistance mutations in bacteria: Phenomena and mechanisms. Environ. Pollut. 2022, 307. [Google Scholar] [CrossRef] [PubMed]
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Letarov, A.V.; Letarova, M.A. The Burden of Survivors: How Can Phage Infection Impact Non-Infected Bacteria? Int. J. Mol. Sci. 2023, 24, 2733. https://doi.org/10.3390/ijms24032733
Letarov AV, Letarova MA. The Burden of Survivors: How Can Phage Infection Impact Non-Infected Bacteria? International Journal of Molecular Sciences. 2023; 24(3):2733. https://doi.org/10.3390/ijms24032733
Chicago/Turabian StyleLetarov, Andrey V., and Maria A. Letarova. 2023. "The Burden of Survivors: How Can Phage Infection Impact Non-Infected Bacteria?" International Journal of Molecular Sciences 24, no. 3: 2733. https://doi.org/10.3390/ijms24032733
APA StyleLetarov, A. V., & Letarova, M. A. (2023). The Burden of Survivors: How Can Phage Infection Impact Non-Infected Bacteria? International Journal of Molecular Sciences, 24(3), 2733. https://doi.org/10.3390/ijms24032733