Multiple mechanisms drive phage infection efficiency in nearly identical hosts

Cristina Howard-Varona, Katherine R. Hargreaves, Natalie E. Solonenko, Lye Meng Markillie, Richard Allen White, Heather M. Brewer, Charles Ansong, Galya Orr, Joshua N. Adkins, Matthew Sullivan

Research output: Contribution to journalArticle

8 Citations (Scopus)

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.

Original languageEnglish (US)
Pages (from-to)1-14
Number of pages14
JournalISME Journal
DOIs
StateAccepted/In press - Mar 22 2018
Externally publishedYes

Fingerprint

bacteriophages
Bacteriophages
Proteome
proteome
Transcriptome
transcriptome
Infection
infection
translation (genetics)
transcription (genetics)
metabolism
Bacteroidetes
protein
proteomics
gene
biotechnology
Biotechnology
Ecology
transcriptomics
generalist

ASJC Scopus subject areas

  • Microbiology
  • Ecology, Evolution, Behavior and Systematics

Cite this

Howard-Varona, C., Hargreaves, K. R., Solonenko, N. E., Markillie, L. M., White, R. A., Brewer, H. M., ... Sullivan, M. (Accepted/In press). Multiple mechanisms drive phage infection efficiency in nearly identical hosts. ISME Journal, 1-14. https://doi.org/10.1038/s41396-018-0099-8

Multiple mechanisms drive phage infection efficiency in nearly identical hosts. / 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.

In: ISME Journal, 22.03.2018, p. 1-14.

Research output: Contribution to journalArticle

Howard-Varona, C, Hargreaves, KR, Solonenko, NE, Markillie, LM, White, RA, Brewer, HM, Ansong, C, Orr, G, Adkins, JN & Sullivan, M 2018, 'Multiple mechanisms drive phage infection efficiency in nearly identical hosts', ISME Journal, pp. 1-14. https://doi.org/10.1038/s41396-018-0099-8
Howard-Varona C, Hargreaves KR, Solonenko NE, Markillie LM, White RA, Brewer HM et al. Multiple mechanisms drive phage infection efficiency in nearly identical hosts. ISME Journal. 2018 Mar 22;1-14. 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. ; Sullivan, Matthew. / Multiple mechanisms drive phage infection efficiency in nearly identical hosts. In: ISME Journal. 2018 ; pp. 1-14.
@article{4b98334e37884ef5a4c08d32c554d780,
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 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.",
author = "Cristina Howard-Varona and Hargreaves, {Katherine R.} and Solonenko, {Natalie E.} and Markillie, {Lye Meng} and White, {Richard Allen} and Brewer, {Heather M.} and Charles Ansong and Galya Orr and Adkins, {Joshua N.} and Matthew Sullivan",
year = "2018",
month = "3",
day = "22",
doi = "10.1038/s41396-018-0099-8",
language = "English (US)",
pages = "1--14",
journal = "ISME Journal",
issn = "1751-7362",
publisher = "Nature Publishing Group",

}

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

PY - 2018/3/22

Y1 - 2018/3/22

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.

UR - http://www.scopus.com/inward/record.url?scp=85044262346&partnerID=8YFLogxK

UR - http://www.scopus.com/inward/citedby.url?scp=85044262346&partnerID=8YFLogxK

U2 - 10.1038/s41396-018-0099-8

DO - 10.1038/s41396-018-0099-8

M3 - Article

C2 - 29568113

AN - SCOPUS:85044262346

SP - 1

EP - 14

JO - ISME Journal

JF - ISME Journal

SN - 1751-7362

ER -