Phage-specific metabolic reprogramming of virocells

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.

doi:10.1038/s41396-019-0580-z

Title: Phage-specific metabolic reprogramming of virocells

Journal Article · 02 January 2020 · The ISME Journal

DOI: https://doi.org/10.1038/s41396-019-0580-z · OSTI ID:1624032

Howard-Varona, Cristina ^[1]; Lindback, Morgan M. ^[2]; Bastien, G. Eric ^[3]; Solonenko, Natalie ^[4]; Zayed, Ahmed A. ^[4];

^[4]; Andreopoulos, Bill ^[5];

^[6]; Glavina del Rio, Tijana ^[5]; Adkins, Joshua N. ^[7]; Paul, Subhadeep ^[8];

^[9]; Duhaime, Melissa B. ^[3]

The Ohio State Univ., Columbus, OH (United States). Department of Microbiology; DOE/OSTI
Univ. of Michigan, Ann Arbor, MI (United States). Dept. of Ecology and Evolutionary Biology
Univ. of Michigan, Ann Arbor, MI (United States). Dept. of Ecology and Evolutionary Biology
The Ohio State Univ., Columbus, OH (United States). Department of Microbiology
USDOE Joint Genome Institute (JGI), Walnut Creek, CA (United States)
Battelle Pacific Northwest Labs., Richland, WA (United States). Environmental Molecular Sciences Laboratory
Pacific Northwest National Lab. (PNNL), Richland, WA (United States). Biological Science Division
The Ohio State Univ., Columbus, OH (United States). Department of Statistics
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

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.

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Research Organization:: Lawrence Berkeley National Laboratory (LBNL), Berkeley, CA (United States); Battelle Memorial Institute, Columbus, OH (United States)

Sponsoring Organization:: USDOE Office of Science (SC)

Grant/Contract Number:: AC02-05CH11231; AC05-76RL01830

OSTI ID:: 1624032

Journal Information:: The ISME Journal, Journal Name: The ISME Journal Journal Issue: 4 Vol. 14; ISSN 1751-7362

Publisher:: Nature Publishing GroupCopyright Statement

Country of Publication:: United States

Language:: English

References (154)

Marine DNA Viral Macro- and Microdiversity from Pole to Pole Gregory, Ann C.; Zayed, Ahmed A.; Conceição-Neto, Nádia Cell, Vol. 177, Issue 5 https://doi.org/10.1016/j.cell.2019.03.040	journal	May 2019
Manipulation of cellular syntheses and the nature of viruses: The virocell concept Forterre, Patrick Comptes Rendus Chimie, Vol. 14, Issue 4 https://doi.org/10.1016/j.crci.2010.06.007	journal	April 2011
Viral metabolic reprogramming in marine ecosystems Hurwitz, Bonnie L.; U’Ren, Jana M. Current Opinion in Microbiology, Vol. 31 https://doi.org/10.1016/j.mib.2016.04.002	journal	June 2016
Virocell Metabolism: Metabolic Innovations During Host–Virus Interactions in the Ocean Rosenwasser, Shilo; Ziv, Carmit; Creveld, Shiri Graff van Trends in Microbiology, Vol. 24, Issue 10 https://doi.org/10.1016/j.tim.2016.06.006	journal	October 2016
Metagenomics Sheds Light on the Ecology of Marine Microbes and Their Viruses Coutinho, Felipe Hernandes; Gregoracci, Gustavo Bueno; Walter, Juline Marta Trends in Microbiology, Vol. 26, Issue 11 https://doi.org/10.1016/j.tim.2018.05.015	journal	November 2018
YfaE, a Ferredoxin Involved in Diferric-Tyrosyl Radical Maintenance in Escherichia coli Ribonucleotide Reductase ^† Wu, Chia-Hung; Jiang, Wei; Krebs, Carsten Biochemistry, Vol. 46, Issue 41 https://doi.org/10.1021/bi7012454	journal	October 2007
Iron in north-east Pacific waters Gordon, R. M.; Martin, J. H.; Knauer, G. A. Nature, Vol. 299, Issue 5884 https://doi.org/10.1038/299611a0	journal	October 1982
Ecogenomics and genome landscapes of marine Pseudoalteromonas phage H105/1 Duhaime, Melissa Beth; Wichels, Antje; Waldmann, Jost The ISME Journal, Vol. 5, Issue 1 https://doi.org/10.1038/ismej.2010.94	journal	July 2010
Top-down controls on bacterial community structure: microbial network analysis of bacteria, T4-like viruses and protists Chow, Cheryl-Emiliane T.; Kim, Diane Y.; Sachdeva, Rohan The ISME Journal, Vol. 8, Issue 4 https://doi.org/10.1038/ismej.2013.199	journal	November 2013
Exploring nucleo-cytoplasmic large DNA viruses in Tara Oceans microbial metagenomes Hingamp, Pascal; Grimsley, Nigel; Acinas, Silvia G. The ISME Journal, Vol. 7, Issue 9 https://doi.org/10.1038/ismej.2013.59	journal	April 2013
Filamentous phages prevalent in Pseudoalteromonas spp. confer properties advantageous to host survival in Arctic sea ice Yu, Zi-Chao; Chen, Xiu-Lan; Shen, Qing-Tao The ISME Journal, Vol. 9, Issue 4 https://doi.org/10.1038/ismej.2014.185	journal	October 2014
Transcriptome dynamics of a broad host-range cyanophage and its hosts Doron, Shany; Fedida, Ayalla; Hernández-Prieto, Miguel A. The ISME Journal, Vol. 10, Issue 6 https://doi.org/10.1038/ismej.2015.210	journal	December 2015
High coverage metabolomics analysis reveals phage-specific alterations to Pseudomonas aeruginosa physiology during infection De Smet, Jeroen; Zimmermann, Michael; Kogadeeva, Maria The ISME Journal, Vol. 10, Issue 8 https://doi.org/10.1038/ismej.2016.3	journal	February 2016
Regulation of infection efficiency in a globally abundant marine Bacteriodetes virus Howard-Varona, Cristina; Roux, Simon; Dore, Hugo The ISME Journal, Vol. 11, Issue 1 https://doi.org/10.1038/ismej.2016.81	journal	May 2016
Quantification of mRNA and protein and integration with protein turnover in a bacterium Maier, Tobias; Schmidt, Alexander; Güell, Marc Molecular Systems Biology, Vol. 7, Issue 1 https://doi.org/10.1038/msb.2011.38	journal	January 2011
Genome-wide expression dynamics of a marine virus and host reveal features of co-evolution Lindell, Debbie; Jaffe, Jacob D.; Coleman, Maureen L. Nature, Vol. 449, Issue 7158 https://doi.org/10.1038/nature06130	journal	September 2007
Plankton networks driving carbon export in the oligotrophic ocean Guidi, Lionel; Chaffron, Samuel; Bittner, Lucie Nature, Vol. 532, Issue 7600 https://doi.org/10.1038/nature16942	journal	February 2016
Uncovering Earth’s virome Paez-Espino, David; Eloe-Fadrosh, Emiley A.; Pavlopoulos, Georgios A. Nature, Vol. 536, Issue 7617 https://doi.org/10.1038/nature19094	journal	August 2016
Ecogenomics and potential biogeochemical impacts of globally abundant ocean viruses Roux, Simon; Brum, Jennifer R.; Dutilh, Bas E. Nature, Vol. 537, Issue 7622 https://doi.org/10.1038/nature19366	journal	September 2016
Re-examination of the relationship between marine virus and microbial cell abundances Wigington, Charles H.; Sonderegger, Derek; Brussaard, Corina P. D. Nature Microbiology, Vol. 1, Issue 3 https://doi.org/10.1038/nmicrobiol.2015.24	journal	January 2016
Marine viruses — major players in the global ecosystem Suttle, Curtis A. Nature Reviews Microbiology, Vol. 5, Issue 10 https://doi.org/10.1038/nrmicro1750	journal	October 2007
The elemental composition of virus particles: implications for marine biogeochemical cycles Jover, Luis F.; Effler, T. Chad; Buchan, Alison Nature Reviews Microbiology, Vol. 12, Issue 7 https://doi.org/10.1038/nrmicro3289	journal	June 2014
A new perspective on lysogeny: prophages as active regulatory switches of bacteria Feiner, Ron; Argov, Tal; Rabinovich, Lev Nature Reviews Microbiology, Vol. 13, Issue 10 https://doi.org/10.1038/nrmicro3527	journal	September 2015
A virus or more in (nearly) every cell: ubiquitous networks of virus–host interactions in extreme environments Munson-McGee, Jacob H.; Peng, Shengyun; Dewerff, Samantha The ISME Journal, Vol. 12, Issue 7 https://doi.org/10.1038/s41396-018-0071-7	journal	February 2018
Multiple mechanisms drive phage infection efficiency in nearly identical hosts Howard-Varona, Cristina; Hargreaves, Katherine R.; Solonenko, Natalie E. The ISME Journal, Vol. 12, Issue 6 https://doi.org/10.1038/s41396-018-0099-8	journal	March 2018
CCL5 derived from tumor-associated macrophages promotes prostate cancer stem cells and metastasis via activating β-catenin/STAT3 signaling Huang, Renlun; Wang, Shengqi; Wang, Neng Cell Death & Disease, Vol. 11, Issue 4 https://doi.org/10.1038/s41419-020-2435-y	journal	April 2020
Ecogenomics of virophages and their giant virus hosts assessed through time series metagenomics Roux, Simon; Chan, Leong-Keat; Egan, Rob Nature Communications, Vol. 8, Issue 1 https://doi.org/10.1038/s41467-017-01086-2	journal	October 2017
Phage puppet masters of the marine microbial realm Breitbart, Mya; Bonnain, Chelsea; Malki, Kema Nature Microbiology, Vol. 3, Issue 7 https://doi.org/10.1038/s41564-018-0166-y	journal	June 2018
Targeting redox metabolism: the perfect storm induced by acrylamide poisoning in the brain Raldúa, Demetrio; Casado, Marta; Prats, Eva Scientific Reports, Vol. 10, Issue 1 https://doi.org/10.1038/s41598-019-57142-y	journal	January 2020
Diel cycling and long-term persistence of viruses in the ocean’s euphotic zone Aylward, Frank O.; Boeuf, Dominique; Mende, Daniel R. Proceedings of the National Academy of Sciences, Vol. 114, Issue 43 https://doi.org/10.1073/pnas.1714821114	journal	October 2017
Biological species in the viral world Bobay, Louis-Marie; Ochman, Howard Proceedings of the National Academy of Sciences, Vol. 115, Issue 23 https://doi.org/10.1073/pnas.1717593115	journal	May 2018
Nitrogen sourcing during viral infection of marine cyanobacteria Waldbauer, Jacob R.; Coleman, Maureen L.; Rizzo, Adriana I. Proceedings of the National Academy of Sciences, Vol. 116, Issue 31 https://doi.org/10.1073/pnas.1901856116	journal	July 2019
Evidence of translation efficiency adaptation of the coding regions of the bacteriophage lambda Goz, Eli; Mioduser, Oriah; Diament, Alon DNA Research, Vol. 24, Issue 4 https://doi.org/10.1093/dnares/dsx005	journal	February 2017
Alignment-free $d_2^*$ oligonucleotide frequency dissimilarity measure improves prediction of hosts from metagenomically-derived viral sequences Ahlgren, Nathan A.; Ren, Jie; Lu, Yang Young Nucleic Acids Research, Vol. 45, Issue 1 https://doi.org/10.1093/nar/gkw1002	journal	November 2016
Revisiting the glyoxylate cycle: alternate pathways for microbial acetate assimilation Ensign, Scott A. Molecular Microbiology, Vol. 61, Issue 2 https://doi.org/10.1111/j.1365-2958.2006.05247.x	journal	July 2006
Marine bacteria and biogeochemical cycling of iron in the oceans Tortell, Philippe D.; Maldonado, Maria T.; Granger, Julie FEMS Microbiology Ecology, Vol. 29, Issue 1 https://doi.org/10.1111/j.1574-6941.1999.tb00593.x	journal	May 1999
Just scratching the surface: an expanding view of the Cpx envelope stress response Vogt, Stefanie L.; Raivio, Tracy L. FEMS Microbiology Letters, Vol. 326, Issue 1 https://doi.org/10.1111/j.1574-6968.2011.02406.x	journal	October 2011
The Microbial Engines That Drive Earth's Biogeochemical Cycles Falkowski, P. G.; Fenchel, T.; Delong, E. F. Science, Vol. 320, Issue 5879 https://doi.org/10.1126/science.1153213	journal	May 2008
Quantifying E. coli Proteome and Transcriptome with Single-Molecule Sensitivity in Single Cells Taniguchi, Y.; Choi, P. J.; Li, G. -W. Science, Vol. 329, Issue 5991 https://doi.org/10.1126/science.1188308	journal	July 2010
Patterns and ecological drivers of ocean viral communities Brum, J. R.; Ignacio-Espinoza, J. C.; Roux, S. Science, Vol. 348, Issue 6237 https://doi.org/10.1126/science.1261498	journal	May 2015
Determinants of community structure in the global plankton interactome Lima-Mendez, G.; Faust, K.; Henry, N. Science, Vol. 348, Issue 6237 https://doi.org/10.1126/science.1262073	journal	May 2015
Decoupling function and taxonomy in the global ocean microbiome Louca, S.; Parfrey, L. W.; Doebeli, M. Science, Vol. 353, Issue 6305 https://doi.org/10.1126/science.aaf4507	journal	September 2016
Role of Filamentous Phage SW1 in Regulating the Lateral Flagella of Shewanella piezotolerans Strain WP3 at Low Temperatures Jian, Huahua; Xiao, Xiang; Wang, Fengping Applied and Environmental Microbiology, Vol. 79, Issue 22 https://doi.org/10.1128/aem.01675-13	journal	September 2013
Isolation of Polyvalent Bacteriophages by Sequential Multiple-Host Approaches Yu, Pingfeng; Mathieu, Jacques; Li, Mengyan Applied and Environmental Microbiology, Vol. 82, Issue 3 https://doi.org/10.1128/aem.02382-15	journal	November 2015
Sulfur and Nitrogen Limitation in Escherichia coli K-12: Specific Homeostatic Responses Gyaneshwar, Prasad; Paliy, Oleg; McAuliffe, Jon Journal of Bacteriology, Vol. 187, Issue 3 https://doi.org/10.1128/jb.187.3.1074-1090.2005	journal	February 2005
Morphology, Physiological Characteristics, and Complete Sequence of Marine Bacteriophage RIO-1 Infecting Pseudoalteromonas marina Hardies, S. C.; Hwang, Y. J.; Hwang, C. Y. Journal of Virology, Vol. 87, Issue 16 https://doi.org/10.1128/jvi.01521-13	journal	June 2013
Environmental Viral Genomes Shed New Light on Virus-Host Interactions in the Ocean Nishimura, Yosuke; Watai, Hiroyasu; Honda, Takashi mSphere, Vol. 2, Issue 2 https://doi.org/10.1128/msphere.00359-16	journal	March 2017
Global Transcriptomic Analysis of the Interactions between Phage φAbp1 and Extensively Drug-Resistant Acinetobacter baumannii Yang, Zichen; Yin, Supeng; Li, Gang mSystems, Vol. 4, Issue 2 https://doi.org/10.1128/msystems.00068-19	journal	April 2019
Modeling Diverse Communities of Marine Microbes Follows, Michael J.; Dutkiewicz, Stephanie Annual Review of Marine Science, Vol. 3, Issue 1 https://doi.org/10.1146/annurev-marine-120709-142848	journal	January 2011
The Guild Concept and the Structure of Ecological Communities Simberloff, D.; Dayan, T. Annual Review of Ecology and Systematics, Vol. 22, Issue 1 https://doi.org/10.1146/annurev.es.22.110191.000555	journal	November 1991
Genomic differentiation among wild cyanophages despite widespread horizontal gene transfer Gregory, Ann C.; Solonenko, Sergei A.; Ignacio-Espinoza, J. Cesar BMC Genomics, Vol. 17, Issue 1 https://doi.org/10.1186/s12864-016-3286-x	journal	November 2016
Determining Host Metabolic Limitations on Viral Replication via Integrated Modeling and Experimental Perturbation Birch, Elsa W.; Ruggero, Nicholas A.; Covert, Markus W. PLoS Computational Biology, Vol. 8, Issue 10 https://doi.org/10.1371/journal.pcbi.1002746	journal	October 2012
Next-Generation “-omics” Approaches Reveal a Massive Alteration of Host RNA Metabolism during Bacteriophage Infection of Pseudomonas aeruginosa Chevallereau, Anne; Blasdel, Bob G.; De Smet, Jeroen PLOS Genetics, Vol. 12, Issue 7 https://doi.org/10.1371/journal.pgen.1006134	journal	July 2016
Analysis of the Pseudoalteromonas tunicata Genome Reveals Properties of a Surface-Associated Life Style in the Marine Environment Thomas, Torsten; Evans, Flavia F.; Schleheck, David PLoS ONE, Vol. 3, Issue 9 https://doi.org/10.1371/journal.pone.0003252	journal	September 2008
Life-Style and Genome Structure of Marine Pseudoalteromonas Siphovirus B8b Isolated from the Northwestern Mediterranean Sea Lara, Elena; Holmfeldt, Karin; Solonenko, Natalie PLOS ONE, Vol. 10, Issue 1 https://doi.org/10.1371/journal.pone.0114829	journal	January 2015
Microbial community structure and function on sinking particles in the North Pacific Subtropical Gyre Fontanez, Kristina M.; Eppley, John M.; Samo, Ty J. Frontiers in Microbiology, Vol. 6 https://doi.org/10.3389/fmicb.2015.00469	journal	May 2015
Transcriptomic and Metabolomics Profiling of Phage–Host Interactions between Phage PaP1 and Pseudomonas aeruginosa Zhao, Xia; Shen, Mengyu; Jiang, Xingyu Frontiers in Microbiology, Vol. 8 https://doi.org/10.3389/fmicb.2017.00548	journal	March 2017
Editorial: Phage Therapy: Past, Present and Future Abedon, Stephen T.; García, Pilar; Mullany, Peter Frontiers in Microbiology, Vol. 8 https://doi.org/10.3389/fmicb.2017.00981	journal	June 2017
Comparative Omics and Trait Analyses of Marine Pseudoalteromonas Phages Advance the Phage OTU Concept Duhaime, Melissa B.; Solonenko, Natalie; Roux, Simon Frontiers in Microbiology, Vol. 8 https://doi.org/10.3389/fmicb.2017.01241	journal	July 2017
The Energetic Cost of Building a Virus Mahmoudabadi, Gita; Milo, Ron; Phillips, Rob arXiv https://doi.org/10.48550/arxiv.1701.02565	text	January 2017
Effects of Plants on Metacommunities and Correlation Networks of Soil Microbial Groups in an Ecologically Restored Wetland Jeong, So-Yeon; Kim, Tae Gwan Microbial Ecology, Vol. 81, Issue 3 https://doi.org/10.1007/s00248-020-01625-3	journal	October 2020
Marine DNA Viral Macro- and Microdiversity from Pole to Pole Gregory, Ann C.; Zayed, Ahmed A.; Conceição-Neto, Nádia Cell, Vol. 177, Issue 5 https://doi.org/10.1016/j.cell.2019.03.040	journal	May 2019
(Ph)ighting Phages: How Bacteria Resist Their Parasites Rostøl, Jakob T.; Marraffini, Luciano Cell Host & Microbe, Vol. 25, Issue 2 https://doi.org/10.1016/j.chom.2019.01.009	journal	February 2019
Manipulation of cellular syntheses and the nature of viruses: The virocell concept Forterre, Patrick Comptes Rendus Chimie, Vol. 14, Issue 4 https://doi.org/10.1016/j.crci.2010.06.007	journal	April 2011
Viral metabolic reprogramming in marine ecosystems Hurwitz, Bonnie L.; U’Ren, Jana M. Current Opinion in Microbiology, Vol. 31 https://doi.org/10.1016/j.mib.2016.04.002	journal	June 2016
Virocell Metabolism: Metabolic Innovations During Host–Virus Interactions in the Ocean Rosenwasser, Shilo; Ziv, Carmit; Creveld, Shiri Graff van Trends in Microbiology, Vol. 24, Issue 10 https://doi.org/10.1016/j.tim.2016.06.006	journal	October 2016
Metagenomics Sheds Light on the Ecology of Marine Microbes and Their Viruses Coutinho, Felipe Hernandes; Gregoracci, Gustavo Bueno; Walter, Juline Marta Trends in Microbiology, Vol. 26, Issue 11 https://doi.org/10.1016/j.tim.2018.05.015	journal	November 2018
YfaE, a Ferredoxin Involved in Diferric-Tyrosyl Radical Maintenance in Escherichia coli Ribonucleotide Reductase ^† Wu, Chia-Hung; Jiang, Wei; Krebs, Carsten Biochemistry, Vol. 46, Issue 41 https://doi.org/10.1021/bi7012454	journal	October 2007
Iron in north-east Pacific waters Gordon, R. M.; Martin, J. H.; Knauer, G. A. Nature, Vol. 299, Issue 5884 https://doi.org/10.1038/299611a0	journal	October 1982
The role of heterotrophic bacteria in iron-limited ocean ecosystems Tortell, Philippe D.; Maldonado, Maria T.; Price, Nell M. Nature, Vol. 383, Issue 6598 https://doi.org/10.1038/383330a0	journal	September 1996
Ecogenomics and genome landscapes of marine Pseudoalteromonas phage H105/1 Duhaime, Melissa Beth; Wichels, Antje; Waldmann, Jost The ISME Journal, Vol. 5, Issue 1 https://doi.org/10.1038/ismej.2010.94	journal	July 2010
The virocell concept and environmental microbiology Forterre, Patrick The ISME Journal, Vol. 7, Issue 2 https://doi.org/10.1038/ismej.2012.110	journal	October 2012
Top-down controls on bacterial community structure: microbial network analysis of bacteria, T4-like viruses and protists Chow, Cheryl-Emiliane T.; Kim, Diane Y.; Sachdeva, Rohan The ISME Journal, Vol. 8, Issue 4 https://doi.org/10.1038/ismej.2013.199	journal	November 2013
Phage infection of an environmentally relevant marine bacterium alters host metabolism and lysate composition Ankrah, Nana Yaw D.; May, Amanda L.; Middleton, Jesse L. The ISME Journal, Vol. 8, Issue 5 https://doi.org/10.1038/ismej.2013.216	journal	December 2013
Exploring nucleo-cytoplasmic large DNA viruses in Tara Oceans microbial metagenomes Hingamp, Pascal; Grimsley, Nigel; Acinas, Silvia G. The ISME Journal, Vol. 7, Issue 9 https://doi.org/10.1038/ismej.2013.59	journal	April 2013
Filamentous phages prevalent in Pseudoalteromonas spp. confer properties advantageous to host survival in Arctic sea ice Yu, Zi-Chao; Chen, Xiu-Lan; Shen, Qing-Tao The ISME Journal, Vol. 9, Issue 4 https://doi.org/10.1038/ismej.2014.185	journal	October 2014
Transcriptome dynamics of a broad host-range cyanophage and its hosts Doron, Shany; Fedida, Ayalla; Hernández-Prieto, Miguel A. The ISME Journal, Vol. 10, Issue 6 https://doi.org/10.1038/ismej.2015.210	journal	December 2015
High coverage metabolomics analysis reveals phage-specific alterations to Pseudomonas aeruginosa physiology during infection De Smet, Jeroen; Zimmermann, Michael; Kogadeeva, Maria The ISME Journal, Vol. 10, Issue 8 https://doi.org/10.1038/ismej.2016.3	journal	February 2016
Regulation of infection efficiency in a globally abundant marine Bacteriodetes virus Howard-Varona, Cristina; Roux, Simon; Dore, Hugo The ISME Journal, Vol. 11, Issue 1 https://doi.org/10.1038/ismej.2016.81	journal	May 2016
Lysogeny in nature: mechanisms, impact and ecology of temperate phages Howard-Varona, Cristina; Hargreaves, Katherine R.; Abedon, Stephen T. The ISME Journal, Vol. 11, Issue 7 https://doi.org/10.1038/ismej.2017.16	journal	March 2017
Comparative transcriptomics analyses reveal the conservation of an ancestral infectious strategy in two bacteriophage genera Blasdel, Bob G.; Chevallereau, Anne; Monot, Marc The ISME Journal, Vol. 11, Issue 9 https://doi.org/10.1038/ismej.2017.63	journal	May 2017
Quantification of mRNA and protein and integration with protein turnover in a bacterium Maier, Tobias; Schmidt, Alexander; Güell, Marc Molecular Systems Biology, Vol. 7, Issue 1 https://doi.org/10.1038/msb.2011.38	journal	January 2011
Genome-wide expression dynamics of a marine virus and host reveal features of co-evolution Lindell, Debbie; Jaffe, Jacob D.; Coleman, Maureen L. Nature, Vol. 449, Issue 7158 https://doi.org/10.1038/nature06130	journal	September 2007
Viral tagging reveals discrete populations in Synechococcus viral genome sequence space Deng, Li; Ignacio-Espinoza, J. Cesar; Gregory, Ann C. Nature, Vol. 513, Issue 7517 https://doi.org/10.1038/nature13459	journal	July 2014
Plankton networks driving carbon export in the oligotrophic ocean Guidi, Lionel; Chaffron, Samuel; Bittner, Lucie Nature, Vol. 532, Issue 7600 https://doi.org/10.1038/nature16942	journal	February 2016
Uncovering Earth’s virome Paez-Espino, David; Eloe-Fadrosh, Emiley A.; Pavlopoulos, Georgios A. Nature, Vol. 536, Issue 7617 https://doi.org/10.1038/nature19094	journal	August 2016
Ecogenomics and potential biogeochemical impacts of globally abundant ocean viruses Roux, Simon; Brum, Jennifer R.; Dutilh, Bas E. Nature, Vol. 537, Issue 7622 https://doi.org/10.1038/nature19366	journal	September 2016
Marine viruses discovered via metagenomics shed light on viral strategies throughout the oceans Coutinho, Felipe H.; Silveira, Cynthia B.; Gregoracci, Gustavo B. Nature Communications, Vol. 8, Issue 1 https://doi.org/10.1038/ncomms15955	journal	July 2017
Mapping and quantifying mammalian transcriptomes by RNA-Seq Mortazavi, Ali; Williams, Brian A.; McCue, Kenneth Nature Methods, Vol. 5, Issue 7, p. 621-628 https://doi.org/10.1038/nmeth.1226	journal	May 2008
Re-examination of the relationship between marine virus and microbial cell abundances Wigington, Charles H.; Sonderegger, Derek; Brussaard, Corina P. D. Nature Microbiology, Vol. 1, Issue 3 https://doi.org/10.1038/nmicrobiol.2015.24	journal	January 2016
Marine viruses — major players in the global ecosystem Suttle, Curtis A. Nature Reviews Microbiology, Vol. 5, Issue 10 https://doi.org/10.1038/nrmicro1750	journal	October 2007
The elemental composition of virus particles: implications for marine biogeochemical cycles Jover, Luis F.; Effler, T. Chad; Buchan, Alison Nature Reviews Microbiology, Vol. 12, Issue 7 https://doi.org/10.1038/nrmicro3289	journal	June 2014
A new perspective on lysogeny: prophages as active regulatory switches of bacteria Feiner, Ron; Argov, Tal; Rabinovich, Lev Nature Reviews Microbiology, Vol. 13, Issue 10 https://doi.org/10.1038/nrmicro3527	journal	September 2015
A virus or more in (nearly) every cell: ubiquitous networks of virus–host interactions in extreme environments Munson-McGee, Jacob H.; Peng, Shengyun; Dewerff, Samantha The ISME Journal, Vol. 12, Issue 7 https://doi.org/10.1038/s41396-018-0071-7	journal	February 2018
Multiple mechanisms drive phage infection efficiency in nearly identical hosts Howard-Varona, Cristina; Hargreaves, Katherine R.; Solonenko, Natalie E. The ISME Journal, Vol. 12, Issue 6 https://doi.org/10.1038/s41396-018-0099-8	journal	March 2018
Ecogenomics of virophages and their giant virus hosts assessed through time series metagenomics Roux, Simon; Chan, Leong-Keat; Egan, Rob Nature Communications, Vol. 8, Issue 1 https://doi.org/10.1038/s41467-017-01086-2	journal	October 2017
Phage puppet masters of the marine microbial realm Breitbart, Mya; Bonnain, Chelsea; Malki, Kema Nature Microbiology, Vol. 3, Issue 7 https://doi.org/10.1038/s41564-018-0166-y	journal	June 2018
Metabolic and biogeochemical consequences of viral infection in aquatic ecosystems Zimmerman, Amy E.; Howard-Varona, Cristina; Needham, David M. Nature Reviews Microbiology, Vol. 18, Issue 1 https://doi.org/10.1038/s41579-019-0270-x	journal	November 2019
Energetic cost of building a virus Mahmoudabadi, Gita; Milo, Ron; Phillips, Rob Proceedings of the National Academy of Sciences, Vol. 114, Issue 22 https://doi.org/10.1073/pnas.1701670114	journal	May 2017
Diel cycling and long-term persistence of viruses in the ocean’s euphotic zone Aylward, Frank O.; Boeuf, Dominique; Mende, Daniel R. Proceedings of the National Academy of Sciences, Vol. 114, Issue 43 https://doi.org/10.1073/pnas.1714821114	journal	October 2017
Biological species in the viral world Bobay, Louis-Marie; Ochman, Howard Proceedings of the National Academy of Sciences, Vol. 115, Issue 23 https://doi.org/10.1073/pnas.1717593115	journal	May 2018
Nitrogen sourcing during viral infection of marine cyanobacteria Waldbauer, Jacob R.; Coleman, Maureen L.; Rizzo, Adriana I. Proceedings of the National Academy of Sciences, Vol. 116, Issue 31 https://doi.org/10.1073/pnas.1901856116	journal	July 2019
Iron-Sulfur Cluster Assembly: CHARACTERIZATION OF IscA AND EVIDENCE FOR A SPECIFIC AND FUNCTIONAL COMPLEX WITH FERREDOXIN Ollagnier-de-Choudens, Sandrine; Mattioli, Tony; Takahashi, Yasuhiro Journal of Biological Chemistry, Vol. 276, Issue 25 https://doi.org/10.1074/jbc.M102902200	journal	April 2001
edgeR: a Bioconductor package for differential expression analysis of digital gene expression data Robinson, M. D.; McCarthy, D. J.; Smyth, G. K. Bioinformatics, Vol. 26, Issue 1 https://doi.org/10.1093/bioinformatics/btp616	journal	November 2009
Evidence of translation efficiency adaptation of the coding regions of the bacteriophage lambda Goz, Eli; Mioduser, Oriah; Diament, Alon DNA Research, Vol. 24, Issue 4 https://doi.org/10.1093/dnares/dsx005	journal	February 2017
Specialization versus adaptation: two strategies employed by cyanophages to enhance their translation efficiencies Limor-Waisberg, Keren; Carmi, Asaf; Scherz, Avigdor Nucleic Acids Research, Vol. 39, Issue 14 https://doi.org/10.1093/nar/gkr169	journal	April 2011
Alignment-free $d_2^*$ oligonucleotide frequency dissimilarity measure improves prediction of hosts from metagenomically-derived viral sequences Ahlgren, Nathan A.; Ren, Jie; Lu, Yang Young Nucleic Acids Research, Vol. 45, Issue 1 https://doi.org/10.1093/nar/gkw1002	journal	November 2016
Viral invasion fitness across a continuum from lysis to latency† Weitz, Joshua S.; Li, Guanlin; Gulbudak, Hayriye Virus Evolution, Vol. 5, Issue 1 https://doi.org/10.1093/ve/vez006	journal	January 2019
Contrasting genomic patterns and infection strategies of two co-existing B acteroidetes podovirus genera : Infection strategies of co-existing podoviruse Holmfeldt, Karin; Howard-Varona, Cristina; Solonenko, Natalie Environmental Microbiology, Vol. 16, Issue 8 https://doi.org/10.1111/1462-2920.12391	journal	February 2014
Variably lytic infection dynamics of large B acteroidetes podovirus phi38:1 against two C ellulophaga baltica host strains : Infection dynamics of Dang, Vinh T.; Howard-Varona, Cristina; Schwenck, Sarah Environmental Microbiology, Vol. 17, Issue 11 https://doi.org/10.1111/1462-2920.13009	journal	September 2015
Large-scale maps of variable infection efficiencies in aquatic Bacteroidetes phage-host model systems : Variable phage-host infection interactions Holmfeldt, Karin; Solonenko, Natalie; Howard-Varona, Cristina Environmental Microbiology, Vol. 18, Issue 11 https://doi.org/10.1111/1462-2920.13392	journal	June 2016
Revisiting the glyoxylate cycle: alternate pathways for microbial acetate assimilation Ensign, Scott A. Molecular Microbiology, Vol. 61, Issue 2 https://doi.org/10.1111/j.1365-2958.2006.05247.x	journal	July 2006
Ribonucleotide reductase and the regulation of DNA replication: an old story and an ancient heritage Herrick, John; Sclavi, Bianca Molecular Microbiology, Vol. 63, Issue 1 https://doi.org/10.1111/j.1365-2958.2006.05493.x	journal	January 2007
Marine bacteria and biogeochemical cycling of iron in the oceans Tortell, Philippe D.; Maldonado, Maria T.; Granger, Julie FEMS Microbiology Ecology, Vol. 29, Issue 1 https://doi.org/10.1111/j.1574-6941.1999.tb00593.x	journal	May 1999
Just scratching the surface: an expanding view of the Cpx envelope stress response Vogt, Stefanie L.; Raivio, Tracy L. FEMS Microbiology Letters, Vol. 326, Issue 1 https://doi.org/10.1111/j.1574-6968.2011.02406.x	journal	October 2011
The Microbial Engines That Drive Earth's Biogeochemical Cycles Falkowski, P. G.; Fenchel, T.; Delong, E. F. Science, Vol. 320, Issue 5879 https://doi.org/10.1126/science.1153213	journal	May 2008
Quantifying E. coli Proteome and Transcriptome with Single-Molecule Sensitivity in Single Cells Taniguchi, Y.; Choi, P. J.; Li, G. -W. Science, Vol. 329, Issue 5991 https://doi.org/10.1126/science.1188308	journal	July 2010
Patterns and ecological drivers of ocean viral communities Brum, J. R.; Ignacio-Espinoza, J. C.; Roux, S. Science, Vol. 348, Issue 6237 https://doi.org/10.1126/science.1261498	journal	May 2015
Determinants of community structure in the global plankton interactome Lima-Mendez, G.; Faust, K.; Henry, N. Science, Vol. 348, Issue 6237 https://doi.org/10.1126/science.1262073	journal	May 2015
Decoupling function and taxonomy in the global ocean microbiome Louca, S.; Parfrey, L. W.; Doebeli, M. Science, Vol. 353, Issue 6305 https://doi.org/10.1126/science.aaf4507	journal	September 2016
Emergent simplicity in microbial community assembly Goldford, Joshua E.; Lu, Nanxi; Bajić, Djordje Science, Vol. 361, Issue 6401 https://doi.org/10.1126/science.aat1168	journal	August 2018
Role of Filamentous Phage SW1 in Regulating the Lateral Flagella of Shewanella piezotolerans Strain WP3 at Low Temperatures Jian, Huahua; Xiao, Xiang; Wang, Fengping Applied and Environmental Microbiology, Vol. 79, Issue 22 https://doi.org/10.1128/AEM.01675-13	journal	September 2013
Isolation of Polyvalent Bacteriophages by Sequential Multiple-Host Approaches Yu, Pingfeng; Mathieu, Jacques; Li, Mengyan Applied and Environmental Microbiology, Vol. 82, Issue 3 https://doi.org/10.1128/AEM.02382-15	journal	November 2015
Isolation and characterization of an Escherichia coli K-12 mutant deficient in glutaredoxin. Kren, B.; Parsell, D.; Fuchs, J. A. Journal of Bacteriology, Vol. 170, Issue 1 https://doi.org/10.1128/JB.170.1.308-315.1988	journal	January 1988
Sulfur and Nitrogen Limitation in Escherichia coli K-12: Specific Homeostatic Responses Gyaneshwar, Prasad; Paliy, Oleg; McAuliffe, Jon Journal of Bacteriology, Vol. 187, Issue 3 https://doi.org/10.1128/JB.187.3.1074-1090.2005	journal	February 2005
Development of Giant Bacteriophage KZ Is Independent of the Host Transcription Apparatus Ceyssens, P. -J.; Minakhin, L.; Van den Bossche, A. Journal of Virology, Vol. 88, Issue 18 https://doi.org/10.1128/JVI.01347-14	journal	June 2014
Morphology, Physiological Characteristics, and Complete Sequence of Marine Bacteriophage RIO-1 Infecting Pseudoalteromonas marina Hardies, S. C.; Hwang, Y. J.; Hwang, C. Y. Journal of Virology, Vol. 87, Issue 16 https://doi.org/10.1128/JVI.01521-13	journal	June 2013
Virioplankton: Viruses in Aquatic Ecosystems Wommack, K. E.; Colwell, R. R. Microbiology and Molecular Biology Reviews, Vol. 64, Issue 1 https://doi.org/10.1128/MMBR.64.1.69-114.2000	journal	March 2000
Genomes of Abundant and Widespread Viruses from the Deep Ocean Mizuno, Carolina Megumi; Ghai, Rohit; Saghaï, Aurélien mBio, Vol. 7, Issue 4 https://doi.org/10.1128/mBio.00805-16	journal	July 2016
Environmental Viral Genomes Shed New Light on Virus-Host Interactions in the Ocean Nishimura, Yosuke; Watai, Hiroyasu; Honda, Takashi mSphere, Vol. 2, Issue 2 https://doi.org/10.1128/mSphere.00359-16	journal	March 2017
Global Transcriptomic Analysis of the Interactions between Phage φAbp1 and Extensively Drug-Resistant Acinetobacter baumannii Yang, Zichen; Yin, Supeng; Li, Gang mSystems, Vol. 4, Issue 2 https://doi.org/10.1128/mSystems.00068-19	journal	April 2019
Modeling Diverse Communities of Marine Microbes Follows, Michael J.; Dutkiewicz, Stephanie Annual Review of Marine Science, Vol. 3, Issue 1 https://doi.org/10.1146/annurev-marine-120709-142848	journal	January 2011
The Glyoxylate Shunt, 60 Years On Dolan, Stephen K.; Welch, Martin Annual Review of Microbiology, Vol. 72, Issue 1 https://doi.org/10.1146/annurev-micro-090817-062257	journal	September 2018
The Guild Concept and the Structure of Ecological Communities Simberloff, D.; Dayan, T. Annual Review of Ecology and Systematics, Vol. 22, Issue 1 https://doi.org/10.1146/annurev.es.22.110191.000555	journal	November 1991
A bioinformatic analysis of ribonucleotide reductase genes in phage genomes and metagenomes Dwivedi, Bhakti; Xue, Bingjie; Lundin, Daniel BMC Evolutionary Biology, Vol. 13, Issue 1 https://doi.org/10.1186/1471-2148-13-33	journal	January 2013
Genomic differentiation among wild cyanophages despite widespread horizontal gene transfer Gregory, Ann C.; Solonenko, Sergei A.; Ignacio-Espinoza, J. Cesar BMC Genomics, Vol. 17, Issue 1 https://doi.org/10.1186/s12864-016-3286-x	journal	November 2016
Determining Host Metabolic Limitations on Viral Replication via Integrated Modeling and Experimental Perturbation Birch, Elsa W.; Ruggero, Nicholas A.; Covert, Markus W. PLoS Computational Biology, Vol. 8, Issue 10 https://doi.org/10.1371/journal.pcbi.1002746	journal	October 2012
Expanding the Marine Virosphere Using Metagenomics Mizuno, Carolina Megumi; Rodriguez-Valera, Francisco; Kimes, Nikole E. PLoS Genetics, Vol. 9, Issue 12 https://doi.org/10.1371/journal.pgen.1003987	journal	December 2013
Next-Generation “-omics” Approaches Reveal a Massive Alteration of Host RNA Metabolism during Bacteriophage Infection of Pseudomonas aeruginosa Chevallereau, Anne; Blasdel, Bob G.; De Smet, Jeroen PLOS Genetics, Vol. 12, Issue 7 https://doi.org/10.1371/journal.pgen.1006134	journal	July 2016
Analysis of the Pseudoalteromonas tunicata Genome Reveals Properties of a Surface-Associated Life Style in the Marine Environment Thomas, Torsten; Evans, Flavia F.; Schleheck, David PLoS ONE, Vol. 3, Issue 9 https://doi.org/10.1371/journal.pone.0003252	journal	September 2008
Life-Style and Genome Structure of Marine Pseudoalteromonas Siphovirus B8b Isolated from the Northwestern Mediterranean Sea Lara, Elena; Holmfeldt, Karin; Solonenko, Natalie PLOS ONE, Vol. 10, Issue 1 https://doi.org/10.1371/journal.pone.0114829	journal	January 2015
Contrasting seasonal drivers of virus abundance and production in the North Pacific Ocean Gainer, P. Jackson; Pound, Helena L.; Larkin, Alyse A. PLOS ONE, Vol. 12, Issue 9 https://doi.org/10.1371/journal.pone.0184371	journal	September 2017
Microbial community structure and function on sinking particles in the North Pacific Subtropical Gyre Fontanez, Kristina M.; Eppley, John M.; Samo, Ty J. Frontiers in Microbiology, Vol. 6 https://doi.org/10.3389/fmicb.2015.00469	journal	May 2015
Transcriptomic and Metabolomics Profiling of Phage–Host Interactions between Phage PaP1 and Pseudomonas aeruginosa Zhao, Xia; Shen, Mengyu; Jiang, Xingyu Frontiers in Microbiology, Vol. 8 https://doi.org/10.3389/fmicb.2017.00548	journal	March 2017
Editorial: Phage Therapy: Past, Present and Future Abedon, Stephen T.; García, Pilar; Mullany, Peter Frontiers in Microbiology, Vol. 8 https://doi.org/10.3389/fmicb.2017.00981	journal	June 2017
Comparative Omics and Trait Analyses of Marine Pseudoalteromonas Phages Advance the Phage OTU Concept Duhaime, Melissa B.; Solonenko, Natalie; Roux, Simon Frontiers in Microbiology, Vol. 8 https://doi.org/10.3389/fmicb.2017.01241	journal	July 2017
Reannotation of the Ribonucleotide Reductase in a Cyanophage Reveals Life History Strategies Within the Virioplankton Harrison, Amelia O.; Moore, Ryan M.; Polson, Shawn W. Frontiers in Microbiology, Vol. 10 https://doi.org/10.3389/fmicb.2019.00134	journal	February 2019
Fighting Fire with Fire: Phage Potential for the Treatment of E. coli O157 Infection Howard-Varona, Cristina; Vik, Dean; Solonenko, Natalie Antibiotics, Vol. 7, Issue 4 https://doi.org/10.3390/antibiotics7040101	journal	November 2018
Transcriptomic Analysis of the Campylobacter jejuni Response to T4-Like Phage NCTC 12673 Infection Sacher, Jessica; Flint, Annika; Butcher, James Viruses, Vol. 10, Issue 6 https://doi.org/10.3390/v10060332	journal	June 2018
From Host to Phage Metabolism: Hot Tales of Phage T4’s Takeover of E. coli Kutter, Elizabeth; Bryan, Daniel; Ray, Georgia Viruses, Vol. 10, Issue 7 https://doi.org/10.3390/v10070387	journal	July 2018
Quantification of mRNA and protein and integration with protein turnover in a bacterium Maier, Tobias; Schmidt, Alexander; Güell, Marc ETH Zurich https://doi.org/10.3929/ethz-b-000038553	text	January 2011
Next-Generation “-omics” Approaches Reveal a Massive Alteration of Host RNA Metabolism during Bacteriophage Infection of Pseudomonas aeruginosa Chevallereau, Anne; Blasdel, Bob; De Smet, Jeroen ETH Zurich https://doi.org/10.3929/ethz-b-000119325	text	January 2016
Genomic differentiation among wild cyanophages despite widespread horizontal gene transfer Gregory, Ann; Solonenko, Sergei; Ignacio-Espinoza, J. Figshare, vp https://doi.org/10.6084/m9.figshare.c.3624431	dataset	November 2016
Putative archaeal viruses from the mesopelagic ocean Vik, Dean R.; Roux, Simon; Brum, Jennifer R. PeerJ, Vol. 5 https://doi.org/10.7717/peerj.3428	journal	January 2017

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