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Title: Phage-specific metabolic reprogramming of virocells

Abstract

Ocean viruses are abundant and infect 20–40% of surface microbes. Infected cells, termed virocells, are thus a predominant microbial state. Yet, virocells and their ecosystem impacts are understudied, thus precluding their incorporation into ecosystem models. Here we investigated how unrelated bacterial viruses (phages) reprogram one host into contrasting virocells with different potential ecosystem footprints. We independently infected the marine Pseudoalteromonasbacterium with siphovirus PSA-HS2 and podovirus PSA-HP1. Time-resolved multi-omics unveiled drastically different metabolic reprogramming and resource requirements by each virocell, which were related to phage–host genomic complementarity and viral fitness. Namely, HS2 was more complementary to the host in nucleotides and amino acids, and fitter during infection than HP1. Functionally, HS2 virocells hardly differed from uninfected cells, with minimal host metabolism impacts. HS2 virocells repressed energy-consuming metabolisms, including motility and translation. Contrastingly, HP1 virocells substantially differed from uninfected cells. They repressed host transcription, responded to infection continuously, and drastically reprogrammed resource acquisition, central carbon and energy metabolisms. Ecologically, this work suggests that one cell, infected versus uninfected, can have immensely different metabolisms that affect the ecosystem differently. Finally, we relate phage–host genome complementarity, virocell metabolic reprogramming, and viral fitness in a conceptual model to guide incorporating viruses into ecosystem models.

Authors:
 [1];  [2];  [3];  [4];  [4]; ORCiD logo [4];  [5]; ORCiD logo [6];  [5];  [7];  [8]; ORCiD logo [9];  [3]
  1. The Ohio State Univ., Columbus, OH (United States). Department of Microbiology
  2. Univ. of Michigan, Ann Arbor, MI (United States). Dept. of Ecology and Evolutionary Biology
  3. Univ. of Michigan, Ann Arbor, MI (United States). Dept. of Ecology and Evolutionary Biology
  4. The Ohio State Univ., Columbus, OH (United States). Department of Microbiology
  5. USDOE Joint Genome Institute (JGI), Walnut Creek, CA (United States)
  6. Battelle Pacific Northwest Labs., Richland, WA (United States). Environmental Molecular Sciences Laboratory
  7. Pacific Northwest National Lab. (PNNL), Richland, WA (United States). Biological Science Division
  8. The Ohio State Univ., Columbus, OH (United States). Department of Statistics
  9. The Ohio State Univ., Columbus, OH (United States). Department of Microbiology; The Ohio State Univ., Columbus, OH (United States). Dept. of Civil, Environmental and Geodetic Engineering; The Ohio State Univ., Columbus, OH (United States). Center for RNA Biology
Publication Date:
Research Org.:
Lawrence Berkeley National Lab. (LBNL), Berkeley, CA (United States); Battelle Memorial Institute, Columbus, OH (United States)
Sponsoring Org.:
USDOE Office of Science (SC)
OSTI Identifier:
1624032
Grant/Contract Number:  
AC02-05CH11231; AC05-76RL01830
Resource Type:
Accepted Manuscript
Journal Name:
The ISME Journal
Additional Journal Information:
Journal Volume: 14; Journal Issue: 4; Journal ID: ISSN 1751-7362
Publisher:
Nature Publishing Group
Country of Publication:
United States
Language:
English
Subject:
Environmental Sciences & Ecology; Microbiology

Citation Formats

Howard-Varona, Cristina, Lindback, Morgan M., Bastien, G. Eric, Solonenko, Natalie, Zayed, Ahmed A., Jang, HoBin, Andreopoulos, Bill, Brewer, Heather M., Glavina del Rio, Tijana, Adkins, Joshua N., Paul, Subhadeep, Sullivan, Matthew B., and Duhaime, Melissa B. Phage-specific metabolic reprogramming of virocells. United States: N. p., 2020. Web. doi:10.1038/s41396-019-0580-z.
Howard-Varona, Cristina, Lindback, Morgan M., Bastien, G. Eric, Solonenko, Natalie, Zayed, Ahmed A., Jang, HoBin, Andreopoulos, Bill, Brewer, Heather M., Glavina del Rio, Tijana, Adkins, Joshua N., Paul, Subhadeep, Sullivan, Matthew B., & Duhaime, Melissa B. Phage-specific metabolic reprogramming of virocells. United States. doi:10.1038/s41396-019-0580-z.
Howard-Varona, Cristina, Lindback, Morgan M., Bastien, G. Eric, Solonenko, Natalie, Zayed, Ahmed A., Jang, HoBin, Andreopoulos, Bill, Brewer, Heather M., Glavina del Rio, Tijana, Adkins, Joshua N., Paul, Subhadeep, Sullivan, Matthew B., and Duhaime, Melissa B. Thu . "Phage-specific metabolic reprogramming of virocells". United States. doi:10.1038/s41396-019-0580-z. https://www.osti.gov/servlets/purl/1624032.
@article{osti_1624032,
title = {Phage-specific metabolic reprogramming of virocells},
author = {Howard-Varona, Cristina and Lindback, Morgan M. and Bastien, G. Eric and Solonenko, Natalie and Zayed, Ahmed A. and Jang, HoBin and Andreopoulos, Bill and Brewer, Heather M. and Glavina del Rio, Tijana and Adkins, Joshua N. and Paul, Subhadeep and Sullivan, Matthew B. and Duhaime, Melissa B.},
abstractNote = {Ocean viruses are abundant and infect 20–40% of surface microbes. Infected cells, termed virocells, are thus a predominant microbial state. Yet, virocells and their ecosystem impacts are understudied, thus precluding their incorporation into ecosystem models. Here we investigated how unrelated bacterial viruses (phages) reprogram one host into contrasting virocells with different potential ecosystem footprints. We independently infected the marine Pseudoalteromonasbacterium with siphovirus PSA-HS2 and podovirus PSA-HP1. Time-resolved multi-omics unveiled drastically different metabolic reprogramming and resource requirements by each virocell, which were related to phage–host genomic complementarity and viral fitness. Namely, HS2 was more complementary to the host in nucleotides and amino acids, and fitter during infection than HP1. Functionally, HS2 virocells hardly differed from uninfected cells, with minimal host metabolism impacts. HS2 virocells repressed energy-consuming metabolisms, including motility and translation. Contrastingly, HP1 virocells substantially differed from uninfected cells. They repressed host transcription, responded to infection continuously, and drastically reprogrammed resource acquisition, central carbon and energy metabolisms. Ecologically, this work suggests that one cell, infected versus uninfected, can have immensely different metabolisms that affect the ecosystem differently. Finally, we relate phage–host genome complementarity, virocell metabolic reprogramming, and viral fitness in a conceptual model to guide incorporating viruses into ecosystem models.},
doi = {10.1038/s41396-019-0580-z},
journal = {The ISME Journal},
number = 4,
volume = 14,
place = {United States},
year = {2020},
month = {1}
}

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