skip to main content
DOE PAGES title logo U.S. Department of Energy
Office of Scientific and Technical Information

Title: Diel transcriptional response of a California Current plankton microbiome to light, low iron, and enduring viral infection

Abstract

Phytoplankton and associated microbial communities provide organic carbon to oceanic food webs and drive ecosystem dynamics. However, capturing those dynamics is challenging. Here, an in situ, semi-Lagrangian, robotic sampler profiled pelagic microbes at 4 h intervals over ~2.6 days in North Pacific high-nutrient, low-chlorophyll waters. We report on the community structure and transcriptional dynamics of microbes in an operationally large size class (>5 μm) predominantly populated by dinoflagellates, ciliates, haptophytes, pelagophytes, diatoms, cyanobacteria (chiefly Synechococcus), prasinophytes (chiefly Ostreococcus), fungi, archaea, and proteobacteria. Apart from fungi and archaea, all groups exhibited 24-h periodicity in some transcripts, but larger portions of the transcriptome oscillated in phototrophs. Periodic photosynthesis-related transcripts exhibited a temporal cascade across the morning hours, conserved across diverse phototrophic lineages. Pronounced silica:nitrate drawdown, a high flavodoxin to ferredoxin transcript ratio, and elevated expression of other Fe-stress markers indicated Fe-limitation. Fe-stress markers peaked during a photoperiodically adaptive time window that could modulate phytoplankton response to seasonal Fe-limitation. Remarkably, we observed viruses that infect the majority of abundant taxa, often with total transcriptional activity synchronized with putative hosts. Taken together, these data reveal a microbial plankton community that is shaped by recycled production and tightly controlled by Fe-limitation and viral activity

Authors:
 [1];  [2];  [3];  [4];  [5]; ORCiD logo [6];  [7];  [8];  [8]; ORCiD logo [9]; ORCiD logo [10];  [11]; ORCiD logo [3]
  1. University of California, San Diego, CA (United States). Scripps Institution of Oceanography; J. Craig Venter Institute, La Jolla, CA (United States). Microbial and Environmental Genomics Group
  2. J. Craig Venter Institute, La Jolla, CA (United States). Microbial and Environmental Genomics Group
  3. University of California, San Diego, CA (United States). Scripps Institution of Oceanography; J. Craig Venter Institute, La Jolla, CA (United States). Microbial and Environmental Genomics Group
  4. Virginia Polytechnic Inst. and State Univ. (Virginia Tech), Blacksburg, VA (United States). Dept. of Biological Sciences
  5. Massachusetts Inst. of Technology (MIT), Cambridge, MA (United States). Dept. of Civil and Environmental Engineering
  6. American University in Cairo, New Cairo (Egypt). Dept. of Biology and Biotechnology Graduate Program
  7. Virginia Polytechnic Inst. and State Univ. (Virginia Tech), Blacksburg, VA (United States). Dept. of Biological Sciences; Monterey Bay Aquarium Research Institute, Moss Landing, CA (United States)
  8. Monterey Bay Aquarium Research Institute, Moss Landing, CA (United States)
  9. University of California, San Diego, CA (United States). Scripps Institution of Oceanography
  10. GEOMAR Helmholtz Centre for Ocean Research, Kiel (Germany). Ocean EcoSystems Biology Unit
  11. Massachusetts Inst. of Technology (MIT), Cambridge, MA (United States). Dept. of Civil and Environmental Engineering; University of Hawaii, Honolulu, HI (United States). Daniel K. Inouye Center for Microbial Oceanography: Research and Education (C-MORE)
Publication Date:
Research Org.:
J. Craig Venter Inst., Inc., Rockville, MD (United States)
Sponsoring Org.:
USDOE Office of Science (SC)
OSTI Identifier:
1624026
Grant/Contract Number:  
SC0008593; SC0018344
Resource Type:
Accepted Manuscript
Journal Name:
The ISME Journal
Additional Journal Information:
Journal Volume: 13; Journal Issue: 11; Journal ID: ISSN 1751-7362
Publisher:
Nature Publishing Group
Country of Publication:
United States
Language:
English
Subject:
Environmental Sciences & Ecology; Microbiology

Citation Formats

Kolody, B. C., McCrow, J. P., Allen, L. Zeigler, Aylward, F. O., Fontanez, K. M., Moustafa, A., Moniruzzaman, M., Chavez, F. P., Scholin, C. A., Allen, E. E., Worden, A. Z., Delong, E. F., and Allen, A. E.. Diel transcriptional response of a California Current plankton microbiome to light, low iron, and enduring viral infection. United States: N. p., 2019. Web. https://doi.org/10.1038/s41396-019-0472-2.
Kolody, B. C., McCrow, J. P., Allen, L. Zeigler, Aylward, F. O., Fontanez, K. M., Moustafa, A., Moniruzzaman, M., Chavez, F. P., Scholin, C. A., Allen, E. E., Worden, A. Z., Delong, E. F., & Allen, A. E.. Diel transcriptional response of a California Current plankton microbiome to light, low iron, and enduring viral infection. United States. https://doi.org/10.1038/s41396-019-0472-2
Kolody, B. C., McCrow, J. P., Allen, L. Zeigler, Aylward, F. O., Fontanez, K. M., Moustafa, A., Moniruzzaman, M., Chavez, F. P., Scholin, C. A., Allen, E. E., Worden, A. Z., Delong, E. F., and Allen, A. E.. Thu . "Diel transcriptional response of a California Current plankton microbiome to light, low iron, and enduring viral infection". United States. https://doi.org/10.1038/s41396-019-0472-2. https://www.osti.gov/servlets/purl/1624026.
@article{osti_1624026,
title = {Diel transcriptional response of a California Current plankton microbiome to light, low iron, and enduring viral infection},
author = {Kolody, B. C. and McCrow, J. P. and Allen, L. Zeigler and Aylward, F. O. and Fontanez, K. M. and Moustafa, A. and Moniruzzaman, M. and Chavez, F. P. and Scholin, C. A. and Allen, E. E. and Worden, A. Z. and Delong, E. F. and Allen, A. E.},
abstractNote = {Phytoplankton and associated microbial communities provide organic carbon to oceanic food webs and drive ecosystem dynamics. However, capturing those dynamics is challenging. Here, an in situ, semi-Lagrangian, robotic sampler profiled pelagic microbes at 4 h intervals over ~2.6 days in North Pacific high-nutrient, low-chlorophyll waters. We report on the community structure and transcriptional dynamics of microbes in an operationally large size class (>5 μm) predominantly populated by dinoflagellates, ciliates, haptophytes, pelagophytes, diatoms, cyanobacteria (chiefly Synechococcus), prasinophytes (chiefly Ostreococcus), fungi, archaea, and proteobacteria. Apart from fungi and archaea, all groups exhibited 24-h periodicity in some transcripts, but larger portions of the transcriptome oscillated in phototrophs. Periodic photosynthesis-related transcripts exhibited a temporal cascade across the morning hours, conserved across diverse phototrophic lineages. Pronounced silica:nitrate drawdown, a high flavodoxin to ferredoxin transcript ratio, and elevated expression of other Fe-stress markers indicated Fe-limitation. Fe-stress markers peaked during a photoperiodically adaptive time window that could modulate phytoplankton response to seasonal Fe-limitation. Remarkably, we observed viruses that infect the majority of abundant taxa, often with total transcriptional activity synchronized with putative hosts. Taken together, these data reveal a microbial plankton community that is shaped by recycled production and tightly controlled by Fe-limitation and viral activity},
doi = {10.1038/s41396-019-0472-2},
journal = {The ISME Journal},
number = 11,
volume = 13,
place = {United States},
year = {2019},
month = {7}
}

Journal Article:
Free Publicly Available Full Text
Publisher's Version of Record

Figures / Tables:

Fig. 1 Fig. 1: Major taxa found in the eastern North Pacific drift track. a Taxonomically annotated total community expression over time across size classes. Expression includes only non-organellar ORFs and is normalized by library (time point) within each fraction. Taxa grouping of each ab initio ORF is determined by best LPImore » hit. Asterisks and tildes denote taxa groups significantly enriched in the large and small size classes, respectively (edgeR, FDR <0.05). b Phylogenetic reconstruction of 16S rRNA gene reference sequences and distributions of active plastids represented in terms of cDNA-based amplicon relative abundances summed across all time points (circles; Supplementary Dataset 5). Circles representing relative amplicon abundance are superimposed over a reference phylogeny which is colored by taxonomy. Proximity of circles to the tips of the branches represents closeness of observed sequences to the references and circle sizes are proportional to normalized read abundance. Note that dinoflagellates known to have tertiary plastids are placed in this method according to the plastid origins (e.g., Gymnodinium myriopyrenoides and several Dinophysis species clading with cryptophytes)« less

Save / Share:

Works referenced in this record:

Climate-driven trends in contemporary ocean productivity
journal, December 2006

  • Behrenfeld, Michael J.; O’Malley, Robert T.; Siegel, David A.
  • Nature, Vol. 444, Issue 7120
  • DOI: 10.1038/nature05317

Master recyclers: features and functions of bacteria associated with phytoplankton blooms
journal, August 2014

  • Buchan, Alison; LeCleir, Gary R.; Gulvik, Christopher A.
  • Nature Reviews Microbiology, Vol. 12, Issue 10
  • DOI: 10.1038/nrmicro3326

Viruses in the sea
journal, September 2005


Growth physiology and fate of diatoms in the ocean: a review
journal, January 2005


Transcriptional Orchestration of the Global Cellular Response of a Model Pennate Diatom to Diel Light Cycling under Iron Limitation
journal, December 2016


Specialized proteomic responses and an ancient photoprotection mechanism sustain marine green algal growth during phosphate limitation
journal, June 2018


Whole-cell response of the pennate diatom Phaeodactylum tricornutum to iron starvation
journal, July 2008

  • Allen, A. E.; LaRoche, J.; Maheswari, U.
  • Proceedings of the National Academy of Sciences, Vol. 105, Issue 30
  • DOI: 10.1073/pnas.0711370105

The Quest to Develop Ecogenomic Sensors: A 25-Year History of the Environmental Sample Processor (ESP) as a Case Study
journal, December 2017


Pattern and synchrony of gene expression among sympatric marine microbial populations
journal, January 2013

  • Ottesen, E. A.; Young, C. R.; Eppley, J. M.
  • Proceedings of the National Academy of Sciences, Vol. 110, Issue 6
  • DOI: 10.1073/pnas.1222099110

Multispecies diel transcriptional oscillations in open ocean heterotrophic bacterial assemblages
journal, July 2014


Diel cycling and long-term persistence of viruses in the ocean’s euphotic zone
journal, October 2017

  • Aylward, Frank O.; Boeuf, Dominique; Mende, Daniel R.
  • Proceedings of the National Academy of Sciences, Vol. 114, Issue 43
  • DOI: 10.1073/pnas.1714821114

Microbial community transcriptional networks are conserved in three domains at ocean basin scales
journal, March 2015

  • Aylward, Frank O.; Eppley, John M.; Smith, Jason M.
  • Proceedings of the National Academy of Sciences, Vol. 112, Issue 17
  • DOI: 10.1073/pnas.1502883112

Phytoplankton–bacterial interactions mediate micronutrient colimitation at the coastal Antarctic sea ice edge
journal, July 2015

  • Bertrand, Erin M.; McCrow, John P.; Moustafa, Ahmed
  • Proceedings of the National Academy of Sciences, Vol. 112, Issue 32
  • DOI: 10.1073/pnas.1501615112

Colony formation in Phaeocystis antarctica: connecting molecular mechanisms with iron biogeochemistry
journal, January 2018

  • Bender, Sara J.; Moran, Dawn M.; McIlvin, Matthew R.
  • Biogeosciences, Vol. 15, Issue 16
  • DOI: 10.5194/bg-15-4923-2018

WGCNA: an R package for weighted correlation network analysis
journal, December 2008


Iron and macronutrients in California coastal upwelling regimes: Implications for diatom blooms
journal, November 2001

  • Bruland, Kenneth W.; Rue, Eden L.; Smith, Geoffrey J.
  • Limnology and Oceanography, Vol. 46, Issue 7
  • DOI: 10.4319/lo.2001.46.7.1661

Iron-limited diatom growth and Si:N uptake ratios in a coastal upwelling regime
journal, June 1998

  • Hutchins, David A.; Bruland, Kenneth W.
  • Nature, Vol. 393, Issue 6685
  • DOI: 10.1038/31203

The central California Current transition zone: A broad region exhibiting evidence for iron limitation
journal, January 2014


Enhanced silica ballasting from iron stress sustains carbon export in a frontal zone within the California Current: SILICA BALLASTING AND IRON STRESS
journal, July 2015

  • Brzezinski, Mark A.; Krause, Jeffrey W.; Bundy, Randelle M.
  • Journal of Geophysical Research: Oceans, Vol. 120, Issue 7
  • DOI: 10.1002/2015JC010829

PCR-Based Diversity Estimates of Artificial and Environmental 18S rRNA Gene Libraries
journal, March 2009


Cyanobacterial distributions along a physico-chemical gradient in the Northeastern Pacific Ocean: Cyanobacterial distributions in the Pacific Ocean
journal, March 2015

  • Sudek, Sebastian; Everroad, R. Craig; Gehman, Alyssa-Lois M.
  • Environmental Microbiology, Vol. 17, Issue 10
  • DOI: 10.1111/1462-2920.12742

Global distribution patterns of distinct clades of the photosynthetic picoeukaryote Ostreococcus
journal, February 2011

  • Demir-Hilton, Elif; Sudek, Sebastian; Cuvelier, Marie L.
  • The ISME Journal, Vol. 5, Issue 7
  • DOI: 10.1038/ismej.2010.209

Quantitative biogeography of picoprasinophytes establishes ecotype distributions and significant contributions to marine phytoplankton
journal, July 2017

  • Limardo, Alexander J.; Sudek, Sebastian; Choi, Chang Jae
  • Environmental Microbiology, Vol. 19, Issue 8
  • DOI: 10.1111/1462-2920.13812

Abundance and Biogeography of Picoprasinophyte Ecotypes and Other Phytoplankton in the Eastern North Pacific Ocean
journal, January 2016

  • Simmons, Melinda P.; Sudek, Sebastian; Monier, Adam
  • Applied and Environmental Microbiology, Vol. 82, Issue 6
  • DOI: 10.1128/AEM.02730-15

Metabolic activity of size-fractionated microbial plankton in estuarine, near-shore, and continental shelf waters of Georgia
journal, January 1990

  • Griffith, Pc; Douglas, Dj; Wainright, Sc
  • Marine Ecology Progress Series, Vol. 59
  • DOI: 10.3354/meps059263

Influence of nutrients and currents on the genomic composition of microbes across an upwelling mosaic
journal, January 2012

  • Allen, Lisa Zeigler; Allen, Eric E.; Badger, Jonathan H.
  • The ISME Journal, Vol. 6, Issue 7
  • DOI: 10.1038/ismej.2011.201

Metagenomic analysis of size-fractionated picoplankton in a marine oxygen minimum zone
journal, September 2013

  • Ganesh, Sangita; Parris, Darren J.; DeLong, Edward F.
  • The ISME Journal, Vol. 8, Issue 1
  • DOI: 10.1038/ismej.2013.144

Eukaryotic microbes, principally fungi and labyrinthulomycetes, dominate biomass on bathypelagic marine snow
journal, September 2016

  • Bochdansky, Alexander B.; Clouse, Melissa A.; Herndl, Gerhard J.
  • The ISME Journal, Vol. 11, Issue 2
  • DOI: 10.1038/ismej.2016.113

The history, biology, and taxonomy of the Cytophaga group
journal, December 1977

  • Christensen, Penelope J.
  • Canadian Journal of Microbiology, Vol. 23, Issue 12
  • DOI: 10.1139/m77-236

Chitin Induces Natural Competence in Vibrio cholerae
journal, December 2005


Major transitions in dinoflagellate evolution unveiled by phylotranscriptomics
journal, December 2016

  • Janouškovec, Jan; Gavelis, Gregory S.; Burki, Fabien
  • Proceedings of the National Academy of Sciences, Vol. 114, Issue 2
  • DOI: 10.1073/pnas.1614842114

Orchestrated Transcription of Key Pathways in Arabidopsis by the Circadian Clock
journal, December 2000


Circadian orchestration of gene expression in cyanobacteria.
journal, June 1995

  • Liu, Y.; Tsinoremas, N. F.; Johnson, C. H.
  • Genes & Development, Vol. 9, Issue 12
  • DOI: 10.1101/gad.9.12.1469

Clocks in the Green Lineage: Comparative Functional Analysis of the Circadian Architecture of the Picoeukaryote Ostreococcus
journal, November 2009

  • Corellou, Florence; Schwartz, Christian; Motta, Jean-Paul
  • The Plant Cell, Vol. 21, Issue 11
  • DOI: 10.1105/tpc.109.068825

A eukaryotic LOV-histidine kinase with circadian clock function in the picoalga Ostreococcus: LOV-histidine kinase in the circadian clock
journal, January 2011


Light sensing and responses in marine microalgae
journal, June 2017

  • Jaubert, Marianne; Bouly, Jean-Pierre; Ribera d’Alcalà, Maurizio
  • Current Opinion in Plant Biology, Vol. 37
  • DOI: 10.1016/j.pbi.2017.03.005

A Hard Day's Night: Diel Shifts in Microbial Eukaryotic Activity in the North Pacific Subtropical Gyre
journal, October 2018


Daily and Circadian Variation in Survival From Ultraviolet Radiation in Chlamydomonas reinhardtii
journal, January 2000


Temporal Organization: Reflections of a Darwinian Clock-Watcher
journal, October 1993


Evolution of Daily Gene Co-expression Patterns from Algae to Plants
journal, July 2017

  • de los Reyes, Pedro; Romero-Campero, Francisco J.; Ruiz, M. Teresa
  • Frontiers in Plant Science, Vol. 8
  • DOI: 10.3389/fpls.2017.01217

Orchestrated transcription of biological processes in the marine picoeukaryote Ostreococcus exposed to light/dark cycles
journal, January 2010


Global transcriptome analysis reveals circadian regulation of key pathways in plant growth and development
journal, January 2008


Two Types of FtsH Protease Subunits Are Required for Chloroplast Biogenesis and Photosystem II Repair in Arabidopsis
journal, August 2005


A Circadian Rhythm in cell Division in a Prokaryote, the Cyanobacterium Synechococcus Wh78031: note
journal, March 1989


Influence of cell cycle phase on calcification in the coccolithophore Emiliania huxleyi
journal, March 2008

  • MÜller, Marius N.; Antia, Avan N.; LaRoche, Julie
  • Limnology and Oceanography, Vol. 53, Issue 2
  • DOI: 10.4319/lo.2008.53.2.0506

Diel Patterns of Growth and Division in Marine Picoplankton in Culture
journal, June 2001


Photoperiodic control of the Arabidopsis proteome reveals a translational coincidence mechanism
journal, March 2018

  • Seaton, Daniel D.; Graf, Alexander; Baerenfaller, Katja
  • Molecular Systems Biology, Vol. 14, Issue 3
  • DOI: 10.15252/msb.20177962

Daily Rhythms in the Cyanobacterium Synechococcus elongatus Probed by High-resolution Mass Spectrometry–based Proteomics Reveals a Small Defined Set of Cyclic Proteins
journal, March 2014

  • Guerreiro, Ana C. L.; Benevento, Marco; Lehmann, Robert
  • Molecular & Cellular Proteomics, Vol. 13, Issue 8
  • DOI: 10.1074/mcp.M113.035840

Algae know the time of day: Circadian and Photoperiodic Programs
journal, December 2001


The Chloroplast Calcium Sensor CAS Is Required for Photoacclimation in Chlamydomonas reinhardtii
journal, August 2011

  • Petroutsos, Dimitris; Busch, Andreas; Janßen, Ingrid
  • The Plant Cell, Vol. 23, Issue 8
  • DOI: 10.1105/tpc.111.087973

Perception of Environmental Signals by a Marine Diatom
journal, June 2000


Strategies to maintain redox homeostasis during photosynthesis under changing conditions
journal, April 2005

  • Scheibe, Renate; Backhausen, Jan E.; Emmerlich, Vera
  • Journal of Experimental Botany, Vol. 56, Issue 416
  • DOI: 10.1093/jxb/eri181

Carbonate-sensitive phytotransferrin controls high-affinity iron uptake in diatoms
journal, March 2018

  • McQuaid, Jeffrey B.; Kustka, Adam B.; Oborník, Miroslav
  • Nature, Vol. 555, Issue 7697
  • DOI: 10.1038/nature25982

Different iron storage strategies among bloom-forming diatoms
journal, December 2018

  • Lampe, Robert H.; Mann, Elizabeth L.; Cohen, Natalie R.
  • Proceedings of the National Academy of Sciences, Vol. 115, Issue 52
  • DOI: 10.1073/pnas.1805243115

FtsH Is Involved in the Early Stages of Repair of Photosystem II in Synechocystis sp PCC 6803
journal, August 2003

  • Silva, Paulo; Thompson, Elinor; Bailey, Shaun
  • The Plant Cell, Vol. 15, Issue 9
  • DOI: 10.1105/tpc.012609

Marine algae and land plants share conserved phytochrome signaling systems
journal, September 2014

  • Duanmu, D.; Bachy, C.; Sudek, S.
  • Proceedings of the National Academy of Sciences, Vol. 111, Issue 44
  • DOI: 10.1073/pnas.1416751111

Choreography of the Transcriptome, Photophysiology, and Cell Cycle of a Minimal Photoautotroph, Prochlorococcus
journal, April 2009


Transcriptome response of high- and low-light-adapted Prochlorococcus strains to changing iron availability
journal, May 2011

  • Thompson, Anne W.; Huang, Katherine; Saito, Mak A.
  • The ISME Journal, Vol. 5, Issue 10
  • DOI: 10.1038/ismej.2011.49

A Nucleus-Encoded Chloroplast Phosphoprotein Governs Expression of the Photosystem I Subunit PsaC in Chlamydomonas reinhardtii
journal, April 2016

  • Douchi, Damien; Qu, Yujiao; Longoni, Paolo
  • The Plant Cell, Vol. 28, Issue 5
  • DOI: 10.1105/tpc.15.00725

Photosynthetic architecture differs in coastal and oceanic diatoms
journal, October 2004


Novel Dinoflagellate Clock-Related Genes Identified Through Microarray Analysis1
journal, June 2003


Post-transcriptional Regulation of S-Phase Genes in the Dinoflagellate, Karenia brevis: DINOFLAGELLATE S-PHASE REGULATION
journal, May 2011


RNA silencing and genome regulation
journal, May 2005


Different Regulatory Mechanisms Modulate the Expression of a Dinoflagellate Iron-Superoxide Dismutase
journal, March 2001

  • Okamoto, O. Keith; Robertson, Deborah L.; Fagan, Thomas F.
  • Journal of Biological Chemistry, Vol. 276, Issue 23
  • DOI: 10.1074/jbc.M101169200

Functional group-specific traits drive phytoplankton dynamics in the oligotrophic ocean
journal, October 2015

  • Alexander, Harriet; Rouco, Mónica; Haley, Sheean T.
  • Proceedings of the National Academy of Sciences, Vol. 112, Issue 44
  • DOI: 10.1073/pnas.1518165112

Dinoflagellates: a remarkable evolutionary experiment
journal, October 2004

  • Hackett, Jeremiah D.; Anderson, Donald M.; Erdner, Deana L.
  • American Journal of Botany, Vol. 91, Issue 10
  • DOI: 10.3732/ajb.91.10.1523

A global ocean atlas of eukaryotic genes
journal, January 2018


Two circadian oscillators in one cell
journal, March 1993

  • Roenneberg, Till; Morse, David
  • Nature, Vol. 362, Issue 6418
  • DOI: 10.1038/362362a0

Characterization of a Dinoflagellate Cryptochrome Blue-Light Receptor with a Possible role in Circadian Control of the cell Cycle
journal, June 2007


Diversity and regulation of ATP sulfurylase in photosynthetic organisms
journal, November 2014

  • Prioretti, Laura; Gontero, Brigitte; Hell, Ruediger
  • Frontiers in Plant Science, Vol. 5
  • DOI: 10.3389/fpls.2014.00597

Dinoflagellates, diatoms, and their viruses
journal, June 2008


Viral activation of cellular metabolism
journal, May 2015


Phage auxiliary metabolic genes and the redirection of cyanobacterial host carbon metabolism
journal, August 2011

  • Thompson, L. R.; Zeng, Q.; Kelly, L.
  • Proceedings of the National Academy of Sciences, Vol. 108, Issue 39
  • DOI: 10.1073/pnas.1102164108

Viral mortality of marine bacteria and cyanobacteria
journal, January 1990

  • Proctor, Lita M.; Fuhrman, Jed A.
  • Nature, Vol. 343, Issue 6253
  • DOI: 10.1038/343060a0

Energy limitation of cyanophage development: implications for marine carbon cycling
journal, January 2018


Genome-wide diel growth state transitions in the diatom Thalassiosira pseudonana
journal, April 2013

  • Ashworth, J.; Coesel, S.; Lee, A.
  • Proceedings of the National Academy of Sciences, Vol. 110, Issue 18
  • DOI: 10.1073/pnas.1300962110

Circadian Rhythms in Cyanobacteria
journal, September 2015

  • Cohen, Susan E.; Golden, Susan S.
  • Microbiology and Molecular Biology Reviews, Vol. 79, Issue 4
  • DOI: 10.1128/MMBR.00036-15

Guidelines for Genome-Scale Analysis of Biological Rhythms
journal, October 2017

  • Hughes, Michael E.; Abruzzi, Katherine C.; Allada, Ravi
  • Journal of Biological Rhythms, Vol. 32, Issue 5
  • DOI: 10.1177/0748730417728663

Genome Sequence of Ostreococcus tauri Virus OtV-2 Throws Light on the Role of Picoeukaryote Niche Separation in the Ocean
journal, February 2011

  • Weynberg, K. D.; Allen, M. J.; Gilg, I. C.
  • Journal of Virology, Vol. 85, Issue 9
  • DOI: 10.1128/JVI.02131-10

Discovery of a dsRNA virus infecting the marine photosynthetic protist Micromonas pusilla
journal, February 2004


Guidelines for Genome-Scale Analysis of Biological Rhythms
text, January 2017

  • S. C., Rund, Samuel; Erquan, Zhang, Eric; Aziz, Sancar,
  • The University of North Carolina at Chapel Hill University Libraries
  • DOI: 10.17615/ktp3-6d25

Information Theory, Inference, and Learning Algorithms
journal, December 2005

  • Yang, Yuhong
  • Journal of the American Statistical Association, Vol. 100, Issue 472
  • DOI: 10.1198/jasa.2005.s54

Photoperiodic control of the Arabidopsis proteome reveals a translational coincidence mechanism
text, January 2018


    Works referencing / citing this record:

    Metabolic and biogeochemical consequences of viral infection in aquatic ecosystems
    journal, November 2019

    • Zimmerman, Amy E.; Howard-Varona, Cristina; Needham, David M.
    • Nature Reviews Microbiology, Vol. 18, Issue 1
    • DOI: 10.1038/s41579-019-0270-x

    Transcriptional patterns of Emiliania huxleyi in the North Pacific Subtropical Gyre reveal the daily rhythms of its metabolic potential
    journal, November 2019

    • Hernández Limón, María D.; Hennon, Gwenn M. M.; Harke, Matthew J.
    • Environmental Microbiology, Vol. 22, Issue 1
    • DOI: 10.1111/1462-2920.14855

    Resource conservation manifests in the genetic code
    text, January 2020


      Figures/Tables have been extracted from DOE-funded journal article accepted manuscripts.