DOE PAGES title logo U.S. Department of Energy
Office of Scientific and Technical Information

Title: Genetic manipulation of competition for nitrate between heterotrophic bacteria and diatoms

Abstract

Diatoms are a dominant group of eukaryotic phytoplankton that contribute substantially to global primary production and the cycling of important elements such as carbon and nitrogen. Heterotrophic bacteria, including members of the gammaproteobacteria, are commonly associated with diatom populations and may rely on them for organic carbon while potentially competing with them for other essential nutrients. Considering that bacterioplankton drive oceanic release of CO2 (i.e., bacterial respiration) while diatoms drive ocean carbon sequestration vial the biological pump, the outcome of such competition could influence the direction and magnitude of carbon flux in the upper ocean. Nitrate availability is commonly a determining factor for the growth of diatom populations, particularly in coastal and upwelling regions. Diatoms as well as many bacterial species can utilize nitrate, however the ability of bacteria to compete for nitrate may be hindered by carbon limitation. Here we have developed a genetically tractable model system using the pennate diatom Phaeodactylurn tricomuturn and the widespread heterotrophic bacteria Alterornonas macleodii to examine carbon-nitrogen dynamics. While subsisting solely on P tricomutum derived carbon. A. macleodii does not appear to be an effective competitor for nitrate, and may in fact benefit the diatom; particularly in stationary phase. However, allochthonous dissolved organicmore » carbon addition in the form of pyruvate triggers A. macleodir proliferation and nitrate uptake, leading to reduced P tricornutum growth. Nitrate reductase deficient mutants of A, macleodii (AnasA) do not exhibit such explosive growth and associated competitive ability in response to allochthonous carbon when nitrate is the sole nitrogen source, but could survive by utilizing solely P tricomutum-derived nitrogen. Furthermore, allocthonous carbon addition enables wild-type A. macleodil to rescue nitrate reductase deficient P tricomutum populations from nitrogen starvation, and RNA-seq transcriptomic evidence supports nitrogen-based interactions between diatoms and bacteria at the molecular level. This study provides key insights into the roles of carbon and nitrogen in phytoplankton-bacteria dynamics and lays the foundation for developing a mechanistic understanding of these interactions using co-culturing and genetic manipulation.« less

Authors:
 [1];  [1];  [2];  [2];  [1]
  1. Univ. of California San Diego, La Jolla, CA (United States). Integrative Oceanography Division, Scripps Institution of Oceanography; J. Craig Venter Inst., La Jolla, CA (United States). Microbial and Environmental Genomics Group
  2. J. Craig Venter Inst., La Jolla, CA (United States). Microbial and Environmental Genomics Group
Publication Date:
Research Org.:
Univ. of California, San Diego, CA (United States)
Sponsoring Org.:
USDOE Office of Science (SC); Gordon and Betty Moore Foundation; National Science Foundation (NSF)
OSTI Identifier:
1287173
Alternate Identifier(s):
OSTI ID: 1438053
Grant/Contract Number:  
SC0008593; GBMF3828; GBMF5006; OCE-1136477
Resource Type:
Accepted Manuscript
Journal Name:
Frontiers in Microbiology
Additional Journal Information:
Journal Volume: 7; Journal ID: ISSN 1664-302X
Publisher:
Frontiers Research Foundation
Country of Publication:
United States
Language:
English
Subject:
59 BASIC BIOLOGICAL SCIENCES; diatoms; bacteria; nitrate; competition; genetic manipulation; transcriptomics; Phaeodactylum; Alteromonas; dissolved organic nitrogen; whole-cell response; phaeodactylum-tricornutum; alteromonas-macleodii; marine-bacteria; phytoplankton cultures; assimilation genes; iron starvation; growth; sea

Citation Formats

Diner, Rachel E., Schwenck, Sarah M., McCrow, John P., Zheng, Hong, and Allen, Andrew E. Genetic manipulation of competition for nitrate between heterotrophic bacteria and diatoms. United States: N. p., 2016. Web. doi:10.3389/fmicb.2016.00880.
Diner, Rachel E., Schwenck, Sarah M., McCrow, John P., Zheng, Hong, & Allen, Andrew E. Genetic manipulation of competition for nitrate between heterotrophic bacteria and diatoms. United States. https://doi.org/10.3389/fmicb.2016.00880
Diner, Rachel E., Schwenck, Sarah M., McCrow, John P., Zheng, Hong, and Allen, Andrew E. Thu . "Genetic manipulation of competition for nitrate between heterotrophic bacteria and diatoms". United States. https://doi.org/10.3389/fmicb.2016.00880. https://www.osti.gov/servlets/purl/1287173.
@article{osti_1287173,
title = {Genetic manipulation of competition for nitrate between heterotrophic bacteria and diatoms},
author = {Diner, Rachel E. and Schwenck, Sarah M. and McCrow, John P. and Zheng, Hong and Allen, Andrew E.},
abstractNote = {Diatoms are a dominant group of eukaryotic phytoplankton that contribute substantially to global primary production and the cycling of important elements such as carbon and nitrogen. Heterotrophic bacteria, including members of the gammaproteobacteria, are commonly associated with diatom populations and may rely on them for organic carbon while potentially competing with them for other essential nutrients. Considering that bacterioplankton drive oceanic release of CO2 (i.e., bacterial respiration) while diatoms drive ocean carbon sequestration vial the biological pump, the outcome of such competition could influence the direction and magnitude of carbon flux in the upper ocean. Nitrate availability is commonly a determining factor for the growth of diatom populations, particularly in coastal and upwelling regions. Diatoms as well as many bacterial species can utilize nitrate, however the ability of bacteria to compete for nitrate may be hindered by carbon limitation. Here we have developed a genetically tractable model system using the pennate diatom Phaeodactylurn tricomuturn and the widespread heterotrophic bacteria Alterornonas macleodii to examine carbon-nitrogen dynamics. While subsisting solely on P tricomutum derived carbon. A. macleodii does not appear to be an effective competitor for nitrate, and may in fact benefit the diatom; particularly in stationary phase. However, allochthonous dissolved organic carbon addition in the form of pyruvate triggers A. macleodir proliferation and nitrate uptake, leading to reduced P tricornutum growth. Nitrate reductase deficient mutants of A, macleodii (AnasA) do not exhibit such explosive growth and associated competitive ability in response to allochthonous carbon when nitrate is the sole nitrogen source, but could survive by utilizing solely P tricomutum-derived nitrogen. Furthermore, allocthonous carbon addition enables wild-type A. macleodil to rescue nitrate reductase deficient P tricomutum populations from nitrogen starvation, and RNA-seq transcriptomic evidence supports nitrogen-based interactions between diatoms and bacteria at the molecular level. This study provides key insights into the roles of carbon and nitrogen in phytoplankton-bacteria dynamics and lays the foundation for developing a mechanistic understanding of these interactions using co-culturing and genetic manipulation.},
doi = {10.3389/fmicb.2016.00880},
journal = {Frontiers in Microbiology},
number = ,
volume = 7,
place = {United States},
year = {Thu Jun 09 00:00:00 EDT 2016},
month = {Thu Jun 09 00:00:00 EDT 2016}
}

Works referenced in this record:

Dominance of bacterial biomass in the Sargasso Sea and its ecological implications
journal, January 1989

  • Fuhrman, Ja; Sleeter, Td; Carlson, Ca
  • Marine Ecology Progress Series, Vol. 57
  • DOI: 10.3354/meps057207

Profiling of the Early Nitrogen Stress Response in the Diatom Phaeodactylum tricornutum Reveals a Novel Family of RING-Domain Transcription Factors
journal, November 2015

  • Matthijs, Michiel; Fabris, Michele; Broos, Stefan
  • Plant Physiology, Vol. 170, Issue 1
  • DOI: 10.1104/pp.15.01300

The Ocean's Food Web, A Changing Paradigm
journal, September 1974


Prokaryotes: The unseen majority
journal, June 1998

  • Whitman, W. B.; Coleman, D. C.; Wiebe, W. J.
  • Proceedings of the National Academy of Sciences, Vol. 95, Issue 12
  • DOI: 10.1073/pnas.95.12.6578

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

Genomes of surface isolates of Alteromonas macleodii: the life of a widespread marine opportunistic copiotroph
journal, September 2012

  • López-Pérez, Mario; Gonzaga, Aitor; Martin-Cuadrado, Ana-Belen
  • Scientific Reports, Vol. 2, Issue 1
  • DOI: 10.1038/srep00696

Biogeography of the ubiquitous marine bacterium Alteromonas macleodii determined by multilocus sequence analysis
journal, September 2008


In situ ultraviolet spectrophotometry for high resolution and long-term monitoring of nitrate, bromide and bisulfide in the ocean
journal, July 2002

  • Johnson, Kenneth S.; Coletti, Luke J.
  • Deep Sea Research Part I: Oceanographic Research Papers, Vol. 49, Issue 7
  • DOI: 10.1016/S0967-0637(02)00020-1

Metabolic characterization of a model heterotrophic bacterium capable of significant chemical alteration of marine dissolved organic matter
journal, December 2015


The interaction between ammonium and nitrate uptake in phytoplankton
journal, January 1990


The microbial carbon pump and the oceanic recalcitrant dissolved organic matter pool
journal, May 2011

  • Jiao, Nianzhi; Herndl, Gerhard J.; Hansell, Dennis A.
  • Nature Reviews Microbiology, Vol. 9, Issue 7
  • DOI: 10.1038/nrmicro2386-c5

Four new derivatives of the broad-host-range cloning vector pBBR1MCS, carrying different antibiotic-resistance cassettes
journal, December 1995


A dual-species co-cultivation system to study the interactions between Roseobacters and dinoflagellates
journal, June 2014


Comparisons of Nitrate Uptake, Storage, and Reduction in Marine Diatoms and Flagellates
journal, October 2000


Excretion of dissolved organic nitrogen by phytoplankton assessed by wet oxidation and 15N tracer procedures
journal, January 1997

  • Pujo-Pay, M.; Conan, P.; Raimbault, P.
  • Marine Ecology Progress Series, Vol. 153
  • DOI: 10.3354/meps153099

Heat shock factor and the heat shock response
journal, May 1991


An ecological and evolutionary context for integrated nitrogen metabolism and related signaling pathways in marine diatoms
journal, June 2006

  • Allen, Andrew E.; Vardi, Assaf; Bowler, Chris
  • Current Opinion in Plant Biology, Vol. 9, Issue 3
  • DOI: 10.1016/j.pbi.2006.03.013

Whole-cell response to nitrogen deprivation in the diatom Phaeodactylum tricornutum
journal, July 2015

  • Alipanah, Leila; Rohloff, Jens; Winge, Per
  • Journal of Experimental Botany, Vol. 66, Issue 20
  • DOI: 10.1093/jxb/erv340

A Unique Short-Chain Dehydrogenase/Reductase in Arabidopsis Glucose Signaling and Abscisic Acid Biosynthesis and Functions
journal, October 2002

  • Cheng, Wan-Hsing; Endo, Akira; Zhou, Li
  • The Plant Cell, Vol. 14, Issue 11
  • DOI: 10.1105/tpc.006494

The Phaeodactylum genome reveals the evolutionary history of diatom genomes
journal, October 2008

  • Bowler, Chris; Allen, Andrew E.; Badger, Jonathan H.
  • Nature, Vol. 456, Issue 7219
  • DOI: 10.1038/nature07410

Rapid formation and sedimentation of large aggregates is predictable from coagulation rates (half-lives) of transparent exopolymer particles (TEP)
journal, January 1995

  • Logan, Bruce E.; Passow, Uta; Alldredge, Alice L.
  • Deep Sea Research Part II: Topical Studies in Oceanography, Vol. 42, Issue 1
  • DOI: 10.1016/0967-0645(95)00012-F

Mix and match: how climate selects phytoplankton
journal, October 2007

  • Falkowski, Paul G.; Oliver, Matthew J.
  • Nature Reviews Microbiology, Vol. 5, Issue 10
  • DOI: 10.1038/nrmicro1751

Dependence of the Cyanobacterium Prochlorococcus on Hydrogen Peroxide Scavenging Microbes for Growth at the Ocean's Surface
journal, February 2011


Interactions between Diatoms and Bacteria
journal, August 2012

  • Amin, S. A.; Parker, M. S.; Armbrust, E. V.
  • Microbiology and Molecular Biology Reviews, Vol. 76, Issue 3
  • DOI: 10.1128/MMBR.00007-12

Uptake of new and Regenerated Forms of Nitrogen in Primary Productivity1: Uptake of Nitrogen in Primary Productivity
journal, April 1967


featureCounts: an efficient general purpose program for assigning sequence reads to genomic features
journal, November 2013


Dissolved organic nitrogen: a dynamic participant in aquatic ecosystems
journal, January 2003


Interactions of planktonic algae and bacteria: effects on algal growth and organic matter dynamics
journal, May 2007


Assimilatory nitrate utilization by bacteria on the West Florida Shelf as determined by stable isotope probing and functional microarray analysis
journal, November 2011


Response of the Photosynthetic Apparatus of Phaeodactylum Tricornutum (Bacillariophyceae) to Nitrate, Phosphate, or iron Starvation1
journal, December 1993


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

Evolution and metabolic significance of the urea cycle in photosynthetic diatoms
journal, May 2011

  • Allen, Andrew E.; Dupont, Christopher L.; Oborník, Miroslav
  • Nature, Vol. 473, Issue 7346
  • DOI: 10.1038/nature10074

A Novel Protein, Ubiquitous in Marine Phytoplankton, Concentrates Iron at the Cell Surface and Facilitates Uptake
journal, February 2015


Nitrogen Uptake, Dissolved Organic Nitrogen Release, and New Production
journal, September 1994


Enzymatic assembly of DNA molecules up to several hundred kilobases
journal, April 2009

  • Gibson, Daniel G.; Young, Lei; Chuang, Ray-Yuan
  • Nature Methods, Vol. 6, Issue 5, p. 343-345
  • DOI: 10.1038/nmeth.1318

Contribution of dissolved free amino acids and ammonium to the nitrogen requirements of heterotrophic bacterioplankton
journal, January 1991


Nitrate Utilization by the Diatom Skeletonema costatum : II. Regulation of Nitrate Uptake
journal, December 1978

  • Serra, Juan L.; Llama, Maria J.; Cadenas, Eduardo
  • Plant Physiology, Vol. 62, Issue 6
  • DOI: 10.1104/pp.62.6.991

Response of Prochlorococcus ecotypes to co-culture with diverse marine bacteria
journal, February 2011

  • Sher, Daniel; Thompson, Jessie W.; Kashtan, Nadav
  • The ISME Journal, Vol. 5, Issue 7
  • DOI: 10.1038/ismej.2011.1

Microbial structuring of marine ecosystems
journal, October 2007

  • Azam, Farooq; Malfatti, Francesca
  • Nature Reviews Microbiology, Vol. 5, Issue 10
  • DOI: 10.1038/nrmicro1747

Ubiquity and Diversity of Heterotrophic Bacterial nasA Genes in Diverse Marine Environments
journal, February 2015


Genetic analysis of the Alteromonas macleodii [NiFe]-hydrogenase: Genetic Analysis of A. macleodii
journal, July 2011


Inactivation of Phaeodactylum tricornutum urease gene using transcription activator-like effector nuclease-based targeted mutagenesis
journal, October 2014

  • Weyman, Philip D.; Beeri, Karen; Lefebvre, Stephane C.
  • Plant Biotechnology Journal, Vol. 13, Issue 4
  • DOI: 10.1111/pbi.12254

Nitrogen Cycling in the Ocean: New Perspectives on Processes and Paradigms
journal, March 2002


Prevalence and microdiversity of Alteromonas macleodii-like microorganisms in different oceanic regions
journal, January 2002


Use of Flow Cytometry to Measure Biogeochemical Rates and Processes in the Ocean
journal, January 2011


edgeR: a Bioconductor package for differential expression analysis of digital gene expression data
journal, November 2009


Marine Microbes See a Sea of Gradients
journal, November 2012


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

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

Inorganic and organic nitrogen uptake by phytoplankton and heterotrophic bacteria in the stratified Mid-Atlantic Bight
journal, August 2010

  • Bradley, Paul B.; Sanderson, Marta P.; Frischer, Marc E.
  • Estuarine, Coastal and Shelf Science, Vol. 88, Issue 4
  • DOI: 10.1016/j.ecss.2010.02.001

Cryptic carbon and sulfur cycling between surface ocean plankton
journal, December 2014

  • Durham, Bryndan P.; Sharma, Shalabh; Luo, Haiwei
  • Proceedings of the National Academy of Sciences, Vol. 112, Issue 2
  • DOI: 10.1073/pnas.1413137112

Remodeling of intermediate metabolism in the diatom Phaeodactylum tricornutum under nitrogen stress
journal, December 2014

  • Levitan, Orly; Dinamarca, Jorge; Zelzion, Ehud
  • Proceedings of the National Academy of Sciences, Vol. 112, Issue 2
  • DOI: 10.1073/pnas.1419818112

DON as a source of bioavailable nitrogen for phytoplankton
journal, January 2006


A CRISPR/Cas9 system adapted for gene editing in marine algae
journal, April 2016

  • Nymark, Marianne; Sharma, Amit Kumar; Sparstad, Torfinn
  • Scientific Reports, Vol. 6, Issue 1
  • DOI: 10.1038/srep24951

Phytoplankton-bacteria interactions: an apparant paradox? Analysis of a model system with both competition and commensalism
journal, January 1985

  • Bratbak, G.; Thingstad, Tf
  • Marine Ecology Progress Series, Vol. 25
  • DOI: 10.3354/meps025023

Competitive dynamics in two species of marine phytoplankton under non-equilibrium conditions
journal, May 2011

  • Cermeño, P.; Lee, Jb; Wyman, K.
  • Marine Ecology Progress Series, Vol. 429
  • DOI: 10.3354/meps09088

Algicidal Bacteria in the Sea and their Impact on Algal Blooms1
journal, March 2004


Single bacterial strain capable of significant contribution to carbon cycling in the surface ocean
journal, April 2014

  • Pedler, B. E.; Aluwihare, L. I.; Azam, F.
  • Proceedings of the National Academy of Sciences, Vol. 111, Issue 20
  • DOI: 10.1073/pnas.1401887111

Chemotactic and Growth Responses of Marine Bacteria to Algal Extracellular Products
journal, October 1972

  • Bell, Wayne; Mitchell, Ralph
  • The Biological Bulletin, Vol. 143, Issue 2
  • DOI: 10.2307/1540052

Interaction and signalling between a cosmopolitan phytoplankton and associated bacteria
journal, May 2015

  • Amin, S. A.; Hmelo, L. R.; van Tol, H. M.
  • Nature, Vol. 522, Issue 7554
  • DOI: 10.1038/nature14488

Designer diatom episomes delivered by bacterial conjugation
journal, April 2015

  • Karas, Bogumil J.; Diner, Rachel E.; Lefebvre, Stephane C.
  • Nature Communications, Vol. 6, Issue 1
  • DOI: 10.1038/ncomms7925

CHL1 Is a Dual-Affinity Nitrate Transporter of Arabidopsis Involved in Multiple Phases of Nitrate Uptake
journal, May 1999

  • Liu, Kun-Hsiang; Huang, Chi-Ying; Tsay, Yi-Fang
  • The Plant Cell, Vol. 11, Issue 5
  • DOI: 10.1105/tpc.11.5.865

Rethinking the marine carbon cycle: Factoring in the multifarious lifestyles of microbes
journal, February 2015


CHL1 encodes a component of the low-affinity nitrate uptake system in Arabidopsis and shows cell type-specific expression in roots.
journal, December 1996

  • Huang, N. C.; Chiang, C. S.; Crawford, N. M.
  • The Plant Cell, Vol. 8, Issue 12
  • DOI: 10.1105/tpc.8.12.2183

Nitrogen uptake by phytoplankton and bacteria during an induced Phaeocystis pouchetii bloom, measured using size fractionation and flow cytometric sorting
journal, August 2010

  • Bradley, Pb; Sanderson, Mp; Nejstgaard, Jc
  • Aquatic Microbial Ecology, Vol. 61, Issue 1
  • DOI: 10.3354/ame01414

Phosphorus cycling and algal-bacterial competition in Sandsfjord, western Norway
journal, January 1993

  • Thingstad, Tr; Skjoldal, Er; Bohne, Ra
  • Marine Ecology Progress Series, Vol. 99
  • DOI: 10.3354/meps099239

Molecular toolbox for studying diatom biology in Phaeodactylum tricornutum
journal, December 2007


Utilization of inorganic and organic nitrogen by bacteria in marine systems1: Nitrogen uptake by bacteria
journal, September 1986


Inorganic and Organic Nitrogen Use by Phytoplankton Along Chesapeake Bay, Measured Using a Flow Cytometric Sorting Approach
journal, April 2010

  • Bradley, Paul B.; Lomas, Michael W.; Bronk, Deborah A.
  • Estuaries and Coasts, Vol. 33, Issue 4
  • DOI: 10.1007/s12237-009-9252-y

Chemotaxis toward phytoplankton drives organic matter partitioning among marine bacteria
journal, January 2016

  • Smriga, Steven; Fernandez, Vicente I.; Mitchell, James G.
  • Proceedings of the National Academy of Sciences, Vol. 113, Issue 6
  • DOI: 10.1073/pnas.1512307113

CHL1 Is a Dual-Affinity Nitrate Transporter of Arabidopsis Involved in Multiple Phases of Nitrate Uptake
journal, May 1999

  • Liu, Kun-Hsiang; Huang, Chi-Ying; Tsay, Yi-Fang
  • The Plant Cell, Vol. 11, Issue 5
  • DOI: 10.2307/3870820

DON as a source of bioavailable nitrogen for phytoplankton
journal, January 2007


CHL1 Encodes a Component of the Low-Affinity Nitrate Uptake System in Arabidopsis and Shows Cell Type-Specific Expression in Roots
journal, December 1996

  • Huang, Nien-Chen; Chiang, Chien-Sung; Crawford, Nigel M.
  • The Plant Cell, Vol. 8, Issue 12
  • DOI: 10.2307/3870460

Nitrate Utilization by the Diatom Skeletonema costatum: I. Kinetics of Nitrate Uptake
journal, December 1978

  • Serra, Juan L.; Llama, Maria J.; Cadenas, Eduardo
  • Plant Physiology, Vol. 62, Issue 6
  • DOI: 10.1104/pp.62.6.987

First principles of terrestrial life: exemplars for potential extra-terrestrial biology
journal, July 2022


Inorganic and Organic Nitrogen Use by Phytoplankton Along Chesapeake Bay, Measured Using a Flow Cytometric Sorting Approach
journal, April 2010

  • Bradley, Paul B.; Lomas, Michael W.; Bronk, Deborah A.
  • Estuaries and Coasts, Vol. 33, Issue 4
  • DOI: 10.1007/s12237-009-9252-y

Heat shock factor and the heat shock response
journal, May 1991


Four new derivatives of the broad-host-range cloning vector pBBR1MCS, carrying different antibiotic-resistance cassettes
journal, December 1995


A Novel Protein, Ubiquitous in Marine Phytoplankton, Concentrates Iron at the Cell Surface and Facilitates Uptake
journal, February 2015


Inorganic and organic nitrogen uptake by phytoplankton and heterotrophic bacteria in the stratified Mid-Atlantic Bight
journal, August 2010

  • Bradley, Paul B.; Sanderson, Marta P.; Frischer, Marc E.
  • Estuarine, Coastal and Shelf Science, Vol. 88, Issue 4
  • DOI: 10.1016/j.ecss.2010.02.001

Molecular toolbox for studying diatom biology in Phaeodactylum tricornutum
journal, December 2007


Metabolic characterization of a model heterotrophic bacterium capable of significant chemical alteration of marine dissolved organic matter
journal, December 2015


An ecological and evolutionary context for integrated nitrogen metabolism and related signaling pathways in marine diatoms
journal, June 2006

  • Allen, Andrew E.; Vardi, Assaf; Bowler, Chris
  • Current Opinion in Plant Biology, Vol. 9, Issue 3
  • DOI: 10.1016/j.pbi.2006.03.013

Bacterial uptake of DOM released from P-limited phytoplankton
journal, December 2003


Response of Prochlorococcus ecotypes to co-culture with diverse marine bacteria
journal, February 2011

  • Sher, Daniel; Thompson, Jessie W.; Kashtan, Nadav
  • The ISME Journal, Vol. 5, Issue 7
  • DOI: 10.1038/ismej.2011.1

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

The Phaeodactylum genome reveals the evolutionary history of diatom genomes
journal, October 2008

  • Bowler, Chris; Allen, Andrew E.; Badger, Jonathan H.
  • Nature, Vol. 456, Issue 7219
  • DOI: 10.1038/nature07410

Evolution and metabolic significance of the urea cycle in photosynthetic diatoms
journal, May 2011

  • Allen, Andrew E.; Dupont, Christopher L.; Oborník, Miroslav
  • Nature, Vol. 473, Issue 7346
  • DOI: 10.1038/nature10074

Interaction and signalling between a cosmopolitan phytoplankton and associated bacteria
journal, May 2015

  • Amin, S. A.; Hmelo, L. R.; van Tol, H. M.
  • Nature, Vol. 522, Issue 7554
  • DOI: 10.1038/nature14488

Designer diatom episomes delivered by bacterial conjugation
journal, April 2015

  • Karas, Bogumil J.; Diner, Rachel E.; Lefebvre, Stephane C.
  • Nature Communications, Vol. 6, Issue 1
  • DOI: 10.1038/ncomms7925

Microbial structuring of marine ecosystems
journal, October 2007

  • Azam, Farooq; Malfatti, Francesca
  • Nature Reviews Microbiology, Vol. 5, Issue 10
  • DOI: 10.1038/nrmicro1747

Mix and match: how climate selects phytoplankton
journal, October 2007

  • Falkowski, Paul G.; Oliver, Matthew J.
  • Nature Reviews Microbiology, Vol. 5, Issue 10
  • DOI: 10.1038/nrmicro1751

The microbial carbon pump and the oceanic recalcitrant dissolved organic matter pool
journal, May 2011

  • Jiao, Nianzhi; Herndl, Gerhard J.; Hansell, Dennis A.
  • Nature Reviews Microbiology, Vol. 9, Issue 7
  • DOI: 10.1038/nrmicro2386-c5

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

Host–virus–predator coexistence in a grey-box model with dynamic optimization of host fitness
journal, September 2019


Machine learning discovery of missing links that mediate alternative branches to plant alkaloids
journal, March 2022

  • Vavricka, Christopher J.; Takahashi, Shunsuke; Watanabe, Naoki
  • Nature Communications, Vol. 13, Issue 1
  • DOI: 10.1038/s41467-022-28883-8

Targeting redox metabolism: the perfect storm induced by acrylamide poisoning in the brain
journal, January 2020


IL-1-dependent enteric gliosis guides intestinal inflammation and dysmotility and modulates macrophage function
journal, August 2022


A CRISPR/Cas9 system adapted for gene editing in marine algae
journal, April 2016

  • Nymark, Marianne; Sharma, Amit Kumar; Sparstad, Torfinn
  • Scientific Reports, Vol. 6, Issue 1
  • DOI: 10.1038/srep24951

Prevalence and microdiversity of Alteromonas macleodii-like microorganisms in different oceanic regions
journal, January 2002


Comparisons of Nitrate Uptake, Storage, and Reduction in Marine Diatoms and Flagellates
journal, October 2000


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

Single bacterial strain capable of significant contribution to carbon cycling in the surface ocean
journal, April 2014

  • Pedler, B. E.; Aluwihare, L. I.; Azam, F.
  • Proceedings of the National Academy of Sciences, Vol. 111, Issue 20
  • DOI: 10.1073/pnas.1401887111

Cryptic carbon and sulfur cycling between surface ocean plankton
journal, December 2014

  • Durham, Bryndan P.; Sharma, Shalabh; Luo, Haiwei
  • Proceedings of the National Academy of Sciences, Vol. 112, Issue 2
  • DOI: 10.1073/pnas.1413137112

Remodeling of intermediate metabolism in the diatom Phaeodactylum tricornutum under nitrogen stress
journal, December 2014

  • Levitan, Orly; Dinamarca, Jorge; Zelzion, Ehud
  • Proceedings of the National Academy of Sciences, Vol. 112, Issue 2
  • DOI: 10.1073/pnas.1419818112

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

Chemotaxis toward phytoplankton drives organic matter partitioning among marine bacteria
journal, January 2016

  • Smriga, Steven; Fernandez, Vicente I.; Mitchell, James G.
  • Proceedings of the National Academy of Sciences, Vol. 113, Issue 6
  • DOI: 10.1073/pnas.1512307113

Whole-cell response to nitrogen deprivation in the diatom Phaeodactylum tricornutum
journal, July 2015

  • Alipanah, Leila; Rohloff, Jens; Winge, Per
  • Journal of Experimental Botany, Vol. 66, Issue 20
  • DOI: 10.1093/jxb/erv340

Profiling of the Early Nitrogen Stress Response in the Diatom Phaeodactylum tricornutum Reveals a Novel Family of RING-Domain Transcription Factors
journal, November 2015

  • Matthijs, Michiel; Fabris, Michele; Broos, Stefan
  • Plant Physiology, Vol. 170, Issue 1
  • DOI: 10.1104/pp.15.01300

A Unique Short-Chain Dehydrogenase/Reductase in Arabidopsis Glucose Signaling and Abscisic Acid Biosynthesis and Functions
journal, October 2002

  • Cheng, Wan-Hsing; Endo, Akira; Zhou, Li
  • The Plant Cell, Vol. 14, Issue 11
  • DOI: 10.1105/tpc.006494

CHL1 Is a Dual-Affinity Nitrate Transporter of Arabidopsis Involved in Multiple Phases of Nitrate Uptake
journal, May 1999

  • Liu, Kun-Hsiang; Huang, Chi-Ying; Tsay, Yi-Fang
  • The Plant Cell, Vol. 11, Issue 5
  • DOI: 10.1105/tpc.11.5.865

Response of the Photosynthetic Apparatus of Phaeodactylum Tricornutum (Bacillariophyceae) to Nitrate, Phosphate, or iron Starvation1
journal, December 1993


Algicidal Bacteria in the Sea and their Impact on Algal Blooms1
journal, March 2004


Assimilatory nitrate utilization by bacteria on the West Florida Shelf as determined by stable isotope probing and functional microarray analysis
journal, November 2011


Genetic analysis of the Alteromonas macleodii [NiFe]-hydrogenase: Genetic Analysis of A. macleodii
journal, July 2011


Inactivation of Phaeodactylum tricornutum urease gene using transcription activator-like effector nuclease-based targeted mutagenesis
journal, October 2014

  • Weyman, Philip D.; Beeri, Karen; Lefebvre, Stephane C.
  • Plant Biotechnology Journal, Vol. 13, Issue 4
  • DOI: 10.1111/pbi.12254

Rethinking the marine carbon cycle: Factoring in the multifarious lifestyles of microbes
journal, February 2015


Nitrogen Uptake, Dissolved Organic Nitrogen Release, and New Production
journal, September 1994


Facilitation of Robust Growth of Prochlorococcus Colonies and Dilute Liquid Cultures by "Helper" Heterotrophic Bacteria
journal, May 2008

  • Morris, J. J.; Kirkegaard, R.; Szul, M. J.
  • Applied and Environmental Microbiology, Vol. 74, Issue 14
  • DOI: 10.1128/aem.02479-07

Effects of temperature and salinity on Vibrio cholerae growth.
journal, January 1982


Growth of and omega-3 fatty acid production by Phaeodactylum tricornutum under different culture conditions.
journal, January 1991


Development of a Genetic Transformation System for an Alga-Lysing Bacterium
journal, June 1998


Diversity and Detection of Nitrate Assimilation Genes in Marine Bacteria
journal, November 2001


Growth of Vibrio cholerae O1 in Red Tide Waters off California
journal, November 2003


Use of Flow Cytometry to Measure Biogeochemical Rates and Processes in the Ocean
journal, January 2011


Dependence of the Cyanobacterium Prochlorococcus on Hydrogen Peroxide Scavenging Microbes for Growth at the Ocean's Surface
journal, February 2011


Ubiquity and Diversity of Heterotrophic Bacterial nasA Genes in Diverse Marine Environments
journal, February 2015


The Ocean's Food Web, A Changing Paradigm
journal, September 1974


Chemotactic and Growth Responses of Marine Bacteria to Algal Extracellular Products
journal, October 1972

  • Bell, Wayne; Mitchell, Ralph
  • The Biological Bulletin, Vol. 143, Issue 2
  • DOI: 10.2307/1540052

CHL1 Encodes a Component of the Low-Affinity Nitrate Uptake System in Arabidopsis and Shows Cell Type-Specific Expression in Roots
journal, December 1996

  • Huang, Nien-Chen; Chiang, Chien-Sung; Crawford, Nigel M.
  • The Plant Cell, Vol. 8, Issue 12
  • DOI: 10.2307/3870460

Dissolved organic nitrogen: a dynamic participant in aquatic ecosystems
journal, January 2003


Interactions of planktonic algae and bacteria: effects on algal growth and organic matter dynamics
journal, May 2007


Dominance of bacterial biomass in the Sargasso Sea and its ecological implications
journal, January 1989

  • Fuhrman, Ja; Sleeter, Td; Carlson, Ca
  • Marine Ecology Progress Series, Vol. 57
  • DOI: 10.3354/meps057207

The interaction between ammonium and nitrate uptake in phytoplankton
journal, January 1990


Contribution of dissolved free amino acids and ammonium to the nitrogen requirements of heterotrophic bacterioplankton
journal, January 1991


Competitive dynamics in two species of marine phytoplankton under non-equilibrium conditions
journal, May 2011

  • Cermeño, P.; Lee, Jb; Wyman, K.
  • Marine Ecology Progress Series, Vol. 429
  • DOI: 10.3354/meps09088

Phosphorus cycling and algal-bacterial competition in Sandsfjord, western Norway
journal, January 1993

  • Thingstad, Tr; Skjoldal, Er; Bohne, Ra
  • Marine Ecology Progress Series, Vol. 99
  • DOI: 10.3354/meps099239

Excretion of dissolved organic nitrogen by phytoplankton assessed by wet oxidation and 15N tracer procedures
journal, January 1997

  • Pujo-Pay, M.; Conan, P.; Raimbault, P.
  • Marine Ecology Progress Series, Vol. 153
  • DOI: 10.3354/meps153099

A dual-species co-cultivation system to study the interactions between Roseobacters and dinoflagellates
journal, June 2014


Utilization of inorganic and organic nitrogen by bacteria in marine systems1: Nitrogen uptake by bacteria
journal, September 1986


DON as a source of bioavailable nitrogen for phytoplankton
journal, January 2006


Works referencing / citing this record:

Transformation techniques for metabolic engineering of diatoms and haptophytes: current state and prospects
journal, March 2018

  • Velmurugan, Natarajan; Deka, Deepi
  • Applied Microbiology and Biotechnology, Vol. 102, Issue 10
  • DOI: 10.1007/s00253-018-8925-5

Advanced genetic tools enable synthetic biology in the oleaginous microalgae Nannochloropsis sp.
journal, March 2018


Genome editing in diatoms: achievements and goals
journal, August 2018


Benefit from decline: the primary transcriptome of Alteromonas macleodii str. Te101 during Trichodesmium demise
journal, January 2018


Biphasic cellular adaptations and ecological implications of Alteromonas macleodii degrading a mixture of algal polysaccharides
journal, August 2018


Genomic, metabolic and phenotypic variability shapes ecological differentiation and intraspecies interactions of Alteromonas macleodii
journal, January 2020


A synthetic microbial loop for modelling heterotroph-phototroph metabolic interactions
journal, July 2018

  • Fondi, Marco; Di Patti, Francesca
  • Ecological Modelling
  • DOI: 10.1101/379131

Benefit from decline: the primary transcriptome of Alteromonas macleodii str. Te101 during Trichodesmium demise
text, January 2018