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Title: 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 1 infection efficiency, which remains poorly understood, particularly in nature. Here we apply 2 genome-wide transcriptomics and proteomics to investigate infection efficiency in nature’s own 3 experiment: two nearly-identical (genetically and physiologically) Bacteroidetes bacterial strains 4 (host18 and host38) that are genetically intractable, but environmentally important, where phage 5 infection efficiency varies. On host18, specialist phage phi18:3 infects efficiently whereas 6 generalist phi38:1 infects inefficiently. On host38, only phi38:1 infects, and efficiently. Overall, 7 phi18:3 globally repressed host18’s transcriptome and proteome, expressed genes that likely 8 evaded host restriction/modification (R/M) defenses and controlled its metabolism, and 9 synchronized phage transcription with translation. In contrast, phi38:1 failed to repress host18’s 10 transcriptome and proteome, did not evade host R/M defenses or express genes for metabolism 11 control, did not synchronize transcripts with proteins and its protein abundances were likely 12 targeted by host proteases. However, on host38, phi38:1 globally repressed host transcriptome and 13 proteome, synchronized phage transcription with translation, and infected host38 efficiently. 14 Together these findings reveal multiple infection inefficiencies. While this contrasts the single 15 mechanisms often revealed in laboratory mutant studies, it likely bettermore » reflects the phage-host 16 interaction dynamics that occur in nature.« less

Authors:
 [1];  [1];  [1];  [2];  [2]; ORCiD logo [2];  [2];  [2];  [2]; ORCiD logo [1]
  1. The Ohio State Univ., Columbus, OH (United States)
  2. Pacific Northwest National Lab. (PNNL), Richland, WA (United States)
Publication Date:
Research Org.:
Pacific Northwest National Lab. (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:
Journal Article: 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. 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., and Sullivan, Matthew B.. Thu . "Multiple mechanisms drive phage infection efficiency in nearly identical hosts". United States. doi: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 1 infection efficiency, which remains poorly understood, particularly in nature. Here we apply 2 genome-wide transcriptomics and proteomics to investigate infection efficiency in nature’s own 3 experiment: two nearly-identical (genetically and physiologically) Bacteroidetes bacterial strains 4 (host18 and host38) that are genetically intractable, but environmentally important, where phage 5 infection efficiency varies. On host18, specialist phage phi18:3 infects efficiently whereas 6 generalist phi38:1 infects inefficiently. On host38, only phi38:1 infects, and efficiently. Overall, 7 phi18:3 globally repressed host18’s transcriptome and proteome, expressed genes that likely 8 evaded host restriction/modification (R/M) defenses and controlled its metabolism, and 9 synchronized phage transcription with translation. In contrast, phi38:1 failed to repress host18’s 10 transcriptome and proteome, did not evade host R/M defenses or express genes for metabolism 11 control, did not synchronize transcripts with proteins and its protein abundances were likely 12 targeted by host proteases. However, on host38, phi38:1 globally repressed host transcriptome and 13 proteome, synchronized phage transcription with translation, and infected host38 efficiently. 14 Together these findings reveal multiple infection inefficiencies. While this contrasts the single 15 mechanisms often revealed in laboratory mutant studies, it likely better reflects the phage-host 16 interaction dynamics that occur in nature.},
doi = {10.1038/s41396-018-0099-8},
journal = {The ISME Journal},
issn = {1751-7362},
number = 6,
volume = 12,
place = {United States},
year = {2018},
month = {3}
}

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