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Phage endolysins are adapted to specific hosts and are evolutionarily dynamic
Copyright policy )Phage endolysins are adapted to specific hosts and are evolutionarily dynamic
Endolysins are produced by (bacterio)phages to rapidly degrade the bacterial cell wall and release new viral particles. Despite sharing a common function, endolysins present in phages that infect a specific bacterial species can be highly diverse and vary in types, number, and organization of their catalytic and cell wall binding domains. While much is now known about the biochemistry of phage endolysins, far less is known about the implication of their diversity on phage–host adaptation and evolution. Using CRISPR-Cas9 genome editing, we could genetically exchange a subset of different endolysin genes into distinct lactococcal phage genomes. Regardless of the type and biochemical properties of these endolysins, fitness costs associated to their genetic exchange were marginal if both recipient and donor phages were infecting the same bacterial strain, but gradually increased when taking place between phage that infect different strains or bacterial species. From an evolutionary perspective, we observed that endolysins could be naturally exchanged by homologous recombination between phages coinfecting a same bacterial strain. Furthermore, phage endolysins could adapt to their new phage/host environment by acquiring adaptative mutations. These observations highlight the remarkable ability of phage lytic systems to recombine and adapt and, therefore, explain their large diversity and mosaicism. It also indicates that evolution should be considered to act on functional modules rather than on bacteriophages themselves. Furthermore, the extensive degree of evolvability observed for phage endolysins offers new perspectives for their engineering as antimicrobial agents.
Bacteria, General Immunology and Microbiology, Cell Wall, General Neuroscience, Endopeptidases, Bacteriophages, General Agricultural and Biological Sciences, General Biochemistry, Genetics and Molecular Biology
Bacteria, General Immunology and Microbiology, Cell Wall, General Neuroscience, Endopeptidases, Bacteriophages, General Agricultural and Biological Sciences, General Biochemistry, Genetics and Molecular Biology
5716
1. Dion MB, Oechslin F, Moineau S. Phage diversity, genomics and phylogeny. Nat Rev Microbiol. 2020; 18(3):125-38. Epub 2020/02/06. https://doi.org/10.1038/s41579-019-0311-5 PMID: 32015529. [OpenAIRE]
2. Hendrix RW, Smith MC, Burns RN, Ford ME, Hatfull GF. Evolutionary relationships among diverse bacteriophages and prophages: all the world's a phage. Proc Natl Acad Sci U S A. 1999; 96(5):2192-7.
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4. Hendrix RW. Bacteriophages: evolution of the majority. Theor Popul Biol. 2002; 61(4):471-80. Epub 2002/08/09. https://doi.org/10.1006/tpbi.2002.1590 PMID: 12167366.
5. Cahill J, Young R. Phage lysis: multiple genes for multiple barriers. Adv Virus Res. 2019; 103:33-70. Epub 11/28. https://doi.org/10.1016/bs.aivir.2018.09.003 PMID: 30635077.
6. Berry J, Rajaure M, Pang T, Young R. The spanin complex is essential for lambda lysis. J Bacteriol. 2012; 194(20):5667-74. Epub 2012/08/21. https://doi.org/10.1128/JB.01245-12 PMID: 22904283; PubMed Central PMCID: PMC3458670. [OpenAIRE]
7. Xu M, Struck DK, Deaton J, Wang I-N, Young R. A signal-arrest-release sequence mediates export and control of the phage P1 endolysin. Proc Natl Acad Sci U S A. 2004; 101 (17):6415-6420. https://doi.org/ 10.1073/pnas.0400957101 PMID: 15090650
8. Vollmer W, Blanot D, de Pedro MA. Peptidoglycan structure and architecture. FEMS Microbiol Rev. 2008; 32(2):149-67. Epub 2008/01/16. https://doi.org/10.1111/j.1574-6976.2007.00094.x PMID: 18194336. [OpenAIRE]
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10. Schmelcher M, Donovan DM, Loessner MJ. Bacteriophage endolysins as novel antimicrobials. Future Microbiol. 2012; 7(10):1147-71. Epub 2012/10/04. https://doi.org/10.2217/fmb.12.97 PMID: 23030422; PubMed Central PMCID: PMC3563964.
citations This is an alternative to the "Influence" indicator, which also reflects the overall/total impact of an article in the research community at large, based on the underlying citation network (diachronically).16 popularity This indicator reflects the "current" impact/attention (the "hype") of an article in the research community at large, based on the underlying citation network.Top 10% influence This indicator reflects the overall/total impact of an article in the research community at large, based on the underlying citation network (diachronically).Top 10% impulse This indicator reflects the initial momentum of an article directly after its publication, based on the underlying citation network.Top 10% citations This is an alternative to the "Influence" indicator, which also reflects the overall/total impact of an article in the research community at large, based on the underlying citation network (diachronically).16 popularity This indicator reflects the "current" impact/attention (the "hype") of an article in the research community at large, based on the underlying citation network.Top 10% influence This indicator reflects the overall/total impact of an article in the research community at large, based on the underlying citation network (diachronically).Top 10% impulse This indicator reflects the initial momentum of an article directly after its publication, based on the underlying citation network.Top 10%
Citations provided by BIP!Popularity provided by BIP!- Natural Sciences and Engineering Research Council of Canada (NSERC)
- Swiss National Science Foundation (SNSF)
- 181297
- Careers | Fellowships | Early Postdoc.Mobility
- Swiss National Science Foundation (SNSF)
- 191059
- Careers | Fellowships | Postdoc.Mobility
Endolysins are produced by (bacterio)phages to rapidly degrade the bacterial cell wall and release new viral particles. Despite sharing a common function, endolysins present in phages that infect a specific bacterial species can be highly diverse and vary in types, number, and organization of their catalytic and cell wall binding domains. While much is now known about the biochemistry of phage endolysins, far less is known about the implication of their diversity on phage–host adaptation and evolution. Using CRISPR-Cas9 genome editing, we could genetically exchange a subset of different endolysin genes into distinct lactococcal phage genomes. Regardless of the type and biochemical properties of these endolysins, fitness costs associated to their genetic exchange were marginal if both recipient and donor phages were infecting the same bacterial strain, but gradually increased when taking place between phage that infect different strains or bacterial species. From an evolutionary perspective, we observed that endolysins could be naturally exchanged by homologous recombination between phages coinfecting a same bacterial strain. Furthermore, phage endolysins could adapt to their new phage/host environment by acquiring adaptative mutations. These observations highlight the remarkable ability of phage lytic systems to recombine and adapt and, therefore, explain their large diversity and mosaicism. It also indicates that evolution should be considered to act on functional modules rather than on bacteriophages themselves. Furthermore, the extensive degree of evolvability observed for phage endolysins offers new perspectives for their engineering as antimicrobial agents.