TY - JOUR
T1 - Multiple mechanisms drive phage infection efficiency in nearly identical hosts
AU - Howard-Varona, Cristina
AU - Hargreaves, Katherine R.
AU - Solonenko, Natalie E.
AU - Markillie, Lye Meng
AU - White, Richard Allen
AU - Brewer, Heather M.
AU - Ansong, Charles
AU - Orr, Galya
AU - Adkins, Joshua N.
AU - Sullivan, Matthew B.
N1 - Funding Information:
Acknowledgements We give special thanks to the lab for constructive feedback, Dr. Simon Roux (OSU) for bioinformatics support and the University of Arizona (UA) and OSU for computational storage. We thank Lacey Orsini (UA) and OSU’s undergraduates, especially Aubrey Jensen, for experimental support. As well, we thank Ryan Sontag (BSD at PNNL), and Dr. Karin Holmfeldt for isolating the phage–host system. A portion of the research was performed using EMSL, a DOE Office of Science User Facility sponsored by the Office of Biological and Environmental Research (User Award No. 47930 to MBS). This work was also funded by the Gordon and Betty Moore Foundation grants (GBMF No. 2631, 3305, 3790) to MBS.
Publisher Copyright:
© 2018 International Society for Microbial Ecology.
PY - 2018/6/1
Y1 - 2018/6/1
N2 - 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.
AB - 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.
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U2 - 10.1038/s41396-018-0099-8
DO - 10.1038/s41396-018-0099-8
M3 - Article
C2 - 29568113
AN - SCOPUS:85044262346
SN - 1751-7362
VL - 12
SP - 1605
EP - 1618
JO - ISME Journal
JF - ISME Journal
IS - 6
ER -