Multiple mechanisms drive phage infection efficiency in nearly identical hosts
Abstract
Phage-host interactions are critical to ecology, evolution, and biotechnology. Central to those is infection efficiency, which remains poorly understood, particularly in nature. Here we apply genome-wide transcriptomics and proteomics to investigate infection efficiency in nature’s own experiment: two nearly-identical (genetically and physiologically) Bacteroidetes bacterial strains (host18 and host38) that are genetically intractable, but environmentally important, where phage infection efficiency varies. On host18, specialist phage phi18:3 infects efficiently whereas generalist phi38:1 infects inefficiently. On host38, only phi38:1 infects, and efficiently. Overall, phi18:3 globally repressed host18’s transcriptome and proteome, expressed genes that likely evaded host restriction/modification (R/M) defenses and controlled its metabolism, and synchronized phage transcription with translation. In contrast, phi38:1 failed to repress host18’s transcriptome and proteome, did not evade host R/M defenses or express genes for metabolism control, did not synchronize transcripts with proteins and its protein abundances were likely targeted by host proteases. However, on host38, phi38:1 globally repressed host transcriptome and proteome, synchronized phage transcription with translation, and infected host38 efficiently. Together these findings reveal multiple infection inefficiencies. While this contrasts the single mechanisms often revealed in laboratory mutant studies, it likely better reflects the phage-host interaction dynamics that occur in nature.
- Authors:
-
[2];
[1]
- The Ohio State Univ., Columbus, OH (United States)
- Pacific Northwest National Lab. (PNNL), Richland, WA (United States)
- Publication Date:
- Research Org.:
- Pacific Northwest National Laboratory (PNNL), Richland, WA (United States)
- Sponsoring Org.:
- USDOE
- OSTI Identifier:
- 1491755
- Report Number(s):
- PNNL-SA-132683
Journal ID: ISSN 1751-7362
- Grant/Contract Number:
- AC05-76RL01830
- Resource Type:
- Accepted Manuscript
- Journal Name:
- The ISME Journal
- Additional Journal Information:
- Journal Volume: 12; Journal Issue: 6; Journal ID: ISSN 1751-7362
- Publisher:
- Nature Publishing Group
- Country of Publication:
- United States
- Language:
- English
- Subject:
- 59 BASIC BIOLOGICAL SCIENCES
Citation Formats
Howard-Varona, Cristina, Hargreaves, Katherine R., Solonenko, Natalie E., Markillie, Lye Meng, White, Richard Allen, Brewer, Heather M., Ansong, Charles, Orr, Galya, Adkins, Joshua N., and Sullivan, Matthew B. Multiple mechanisms drive phage infection efficiency in nearly identical hosts. United States: N. p., 2018.
Web. doi:10.1038/s41396-018-0099-8.
Howard-Varona, Cristina, Hargreaves, Katherine R., Solonenko, Natalie E., Markillie, Lye Meng, White, Richard Allen, Brewer, Heather M., Ansong, Charles, Orr, Galya, Adkins, Joshua N., & Sullivan, Matthew B. Multiple mechanisms drive phage infection efficiency in nearly identical hosts. United States. https://doi.org/10.1038/s41396-018-0099-8
Howard-Varona, Cristina, Hargreaves, Katherine R., Solonenko, Natalie E., Markillie, Lye Meng, White, Richard Allen, Brewer, Heather M., Ansong, Charles, Orr, Galya, Adkins, Joshua N., and Sullivan, Matthew B. Thu .
"Multiple mechanisms drive phage infection efficiency in nearly identical hosts". United States. https://doi.org/10.1038/s41396-018-0099-8. https://www.osti.gov/servlets/purl/1491755.
@article{osti_1491755,
title = {Multiple mechanisms drive phage infection efficiency in nearly identical hosts},
author = {Howard-Varona, Cristina and Hargreaves, Katherine R. and Solonenko, Natalie E. and Markillie, Lye Meng and White, Richard Allen and Brewer, Heather M. and Ansong, Charles and Orr, Galya and Adkins, Joshua N. and Sullivan, Matthew B.},
abstractNote = {Phage-host interactions are critical to ecology, evolution, and biotechnology. Central to those is infection efficiency, which remains poorly understood, particularly in nature. Here we apply genome-wide transcriptomics and proteomics to investigate infection efficiency in nature’s own experiment: two nearly-identical (genetically and physiologically) Bacteroidetes bacterial strains (host18 and host38) that are genetically intractable, but environmentally important, where phage infection efficiency varies. On host18, specialist phage phi18:3 infects efficiently whereas generalist phi38:1 infects inefficiently. On host38, only phi38:1 infects, and efficiently. Overall, phi18:3 globally repressed host18’s transcriptome and proteome, expressed genes that likely evaded host restriction/modification (R/M) defenses and controlled its metabolism, and synchronized phage transcription with translation. In contrast, phi38:1 failed to repress host18’s transcriptome and proteome, did not evade host R/M defenses or express genes for metabolism control, did not synchronize transcripts with proteins and its protein abundances were likely targeted by host proteases. However, on host38, phi38:1 globally repressed host transcriptome and proteome, synchronized phage transcription with translation, and infected host38 efficiently. Together these findings reveal multiple infection inefficiencies. While this contrasts the single mechanisms often revealed in laboratory mutant studies, it likely better reflects the phage-host interaction dynamics that occur in nature.},
doi = {10.1038/s41396-018-0099-8},
journal = {The ISME Journal},
number = 6,
volume = 12,
place = {United States},
year = {Thu Mar 22 00:00:00 EDT 2018},
month = {Thu Mar 22 00:00:00 EDT 2018}
}
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