Growth on ATP elicits a P-stress response in the picoeukaryote Micromonas pusilla
Abstract
The surface waters of oligotrophic oceans have chronically low phosphate (Pi) concentrations, which renders dissolved organic phosphorus (DOP) an important nutrient source. In the subtropical North Atlantic, cyanobacteria are often numerically dominant, but picoeukaryotes can dominate autotrophic biomass and productivity making them important contributors to the ocean carbon cycle. Despite their importance, little is known regarding the metabolic response of picoeukaryotes to changes in phosphorus (P) source and availability. To understand the molecular mechanisms that regulate P utilization in oligotrophic environments, we evaluated transcriptomes of the picoeukaryote Micromonas pusilla grown under Pi-replete and -deficient conditions, with an additional investigation of growth on DOP in replete conditions. Genes that function in sulfolipid substitution and Pi uptake increased in expression with Pi-deficiency, suggesting cells were reallocating cellular P and increasing P acquisition capabilities. Pi-deficient M. pusilla cells also increased alkaline phosphatase activity and reduced their cellular P content. Cells grown with DOP were able to maintain relatively high growth rates, however the transcriptomic response was more similar to the Pi-deficient response than that seen in cells grown under Pi-replete conditions. The results demonstrate that not all P sources are the same for growth; while M. pusilla, a model picoeukaryote, may grow wellmore »
- Authors:
-
- Bigelow Laboratory for Ocean Sciences, East Boothbay, ME (United States)
- Publication Date:
- Research Org.:
- Bigelow Laboratory for Ocean Sciences, East Boothbay, ME (United States)
- Sponsoring Org.:
- USDOE Office of Science (SC)
- OSTI Identifier:
- 1283057
- Grant/Contract Number:
- AC02-05CH11231
- Resource Type:
- Accepted Manuscript
- Journal Name:
- PLoS ONE
- Additional Journal Information:
- Journal Volume: 11; Journal Issue: 5; Journal ID: ISSN 1932-6203
- Publisher:
- Public Library of Science
- Country of Publication:
- United States
- Language:
- English
- Subject:
- 59 BASIC BIOLOGICAL SCIENCES; western north-atlantic; dissolved organic phosphorus; sargasso sea; saccharomyces-cerevisiae; phosphatase-activity; community structure; emiliania-huxleyi; marine systems; flow-cytometry; carbonic-acid
Citation Formats
Whitney, LeAnn P., and Lomas, Michael W. Growth on ATP elicits a P-stress response in the picoeukaryote Micromonas pusilla. United States: N. p., 2016.
Web. doi:10.1371/journal.pone.0155158.
Whitney, LeAnn P., & Lomas, Michael W. Growth on ATP elicits a P-stress response in the picoeukaryote Micromonas pusilla. United States. https://doi.org/10.1371/journal.pone.0155158
Whitney, LeAnn P., and Lomas, Michael W. Wed .
"Growth on ATP elicits a P-stress response in the picoeukaryote Micromonas pusilla". United States. https://doi.org/10.1371/journal.pone.0155158. https://www.osti.gov/servlets/purl/1283057.
@article{osti_1283057,
title = {Growth on ATP elicits a P-stress response in the picoeukaryote Micromonas pusilla},
author = {Whitney, LeAnn P. and Lomas, Michael W.},
abstractNote = {The surface waters of oligotrophic oceans have chronically low phosphate (Pi) concentrations, which renders dissolved organic phosphorus (DOP) an important nutrient source. In the subtropical North Atlantic, cyanobacteria are often numerically dominant, but picoeukaryotes can dominate autotrophic biomass and productivity making them important contributors to the ocean carbon cycle. Despite their importance, little is known regarding the metabolic response of picoeukaryotes to changes in phosphorus (P) source and availability. To understand the molecular mechanisms that regulate P utilization in oligotrophic environments, we evaluated transcriptomes of the picoeukaryote Micromonas pusilla grown under Pi-replete and -deficient conditions, with an additional investigation of growth on DOP in replete conditions. Genes that function in sulfolipid substitution and Pi uptake increased in expression with Pi-deficiency, suggesting cells were reallocating cellular P and increasing P acquisition capabilities. Pi-deficient M. pusilla cells also increased alkaline phosphatase activity and reduced their cellular P content. Cells grown with DOP were able to maintain relatively high growth rates, however the transcriptomic response was more similar to the Pi-deficient response than that seen in cells grown under Pi-replete conditions. The results demonstrate that not all P sources are the same for growth; while M. pusilla, a model picoeukaryote, may grow well on DOP, the metabolic demand is greater than growth on Pi. Lastly, these findings provide insight into the cellular strategies which may be used to support growth in a stratified future ocean predicted to favor picoeukaryotes.},
doi = {10.1371/journal.pone.0155158},
journal = {PLoS ONE},
number = 5,
volume = 11,
place = {United States},
year = {Wed May 11 00:00:00 EDT 2016},
month = {Wed May 11 00:00:00 EDT 2016}
}
Web of Science
Works referenced in this record:
Phytoplankton population dynamics at the Bermuda Atlantic Time-series station in the Sargasso Sea
journal, January 2001
- DuRand, Michele D.; Olson, Robert J.; Chisholm, Sallie W.
- Deep Sea Research Part II: Topical Studies in Oceanography, Vol. 48, Issue 8-9
Significant CO2 fixation by small prymnesiophytes in the subtropical and tropical northeast Atlantic Ocean
journal, April 2010
- Jardillier, Ludwig; Zubkov, Mikhail V.; Pearman, John
- The ISME Journal, Vol. 4, Issue 9
Primary production of prochlorophytes, cyanobacteria, and eucaryotic ultraphytoplankton: Measurements from flow cytometric sorting
journal, January 1994
- Li, William K. W.
- Limnology and Oceanography, Vol. 39, Issue 1
Evidence for aggregation and export of cyanobacteria and nano-eukaryotes from the Sargasso Sea euphotic zone
journal, January 2011
- Lomas, M. W.; Moran, S. B.
- Biogeosciences, Vol. 8, Issue 1
Assimilation of upwelled nitrate by small eukaryotes in the Sargasso Sea
journal, September 2011
- Fawcett, Sarah E.; Lomas, Michael W.; Casey, John R.
- Nature Geoscience, Vol. 4, Issue 10
The biogeochemical cycling of phosphorus in marine systems
journal, August 2000
- Benitez-Nelson, Claudia R.
- Earth-Science Reviews, Vol. 51, Issue 1-4
Phosphorus deficiency in the Atlantic: An emerging paradigm in oceanography
journal, January 2003
- Ammerman, James W.; Hood, Raleigh R.; Case, Darin A.
- Eos, Transactions American Geophysical Union, Vol. 84, Issue 18
Microbes and the Marine Phosphorus Cycle
journal, June 2007
- Dyhrman, Sonya; Ammerman, James; Van Mooy, Benjamin
- Oceanography, Vol. 20, Issue 2
Phosphorus cycling in the North and South Atlantic Ocean subtropical gyres
journal, June 2008
- Mather, Rhiannon L.; Reynolds, Sarah E.; Wolff, George A.
- Nature Geoscience, Vol. 1, Issue 7
Sargasso Sea phosphorus biogeochemistry: an important role for dissolved organic phosphorus (DOP)
journal, January 2010
- Lomas, M. W.; Burke, A. L.; Lomas, D. A.
- Biogeosciences, Vol. 7, Issue 2
Phosphate Depletion in the Western North Atlantic Ocean
journal, August 2000
- Wu, J.
- Science, Vol. 289, Issue 5480
Nutrient gradients in the western North Atlantic Ocean: Relationship to microbial community structure and comparison to patterns in the Pacific Ocean
journal, November 2001
- Cavender-Bares, Kent K.; Karl, David M.; Chisholm, Sallie W.
- Deep Sea Research Part I: Oceanographic Research Papers, Vol. 48, Issue 11
Cell-specific detection of phosphorus stress in Trichodesmium from the Western North Atlantic
journal, November 2002
- Ståhl-Delbanco, Annika; Hansson, Lars-Anders
- Limnology and Oceanography, Vol. 47, Issue 6
Taxonomic variability of phosphorus stress in Sargasso Sea phytoplankton
journal, November 2004
- Lomas, Michael W.; Swain, Ashley; Shelton, Ryan
- Limnology and Oceanography, Vol. 49, Issue 6
Phytoplankton taxon-specific orthophosphate (Pi) and ATP utilization in the western subtropical North Atlantic
journal, December 2009
- Casey, Jr; Lomas, Mw; Michelou, Vk
- Aquatic Microbial Ecology, Vol. 58
Does the transport of dissolved organic nutrients affect export production in the Atlantic Ocean?: TRANSPORT OF DISSOLVED ORGANIC NUTRIENTS
journal, July 2006
- Roussenov, Vassil; Williams, Richard G.; Mahaffey, Claire
- Global Biogeochemical Cycles, Vol. 20, Issue 3
Distribution of dissolved organic nutrients and their effect on export production over the Atlantic Ocean: DON AND DOP IN THE ATLANTIC OCEAN
journal, November 2009
- Torres-Valdés, S.; Roussenov, V. M.; Sanders, R.
- Global Biogeochemical Cycles, Vol. 23, Issue 4
Evidence for production and lateral transport of dissolved organic phosphorus in the eastern subtropical North Atlantic
journal, August 2014
- Reynolds, Sarah; Mahaffey, Claire; Roussenov, Vassil
- Global Biogeochemical Cycles, Vol. 28, Issue 8
Phytoplankton distribution patterns in the northwestern Sargasso Sea revealed by small subunit rRNA genes from plastids
journal, September 2011
- Treusch, Alexander H.; Demir-Hilton, Elif; Vergin, Kevin L.
- The ISME Journal, Vol. 6, Issue 3
Distribution, Phylogeny, and Growth of Cold-Adapted Picoprasinophytes in Arctic seas
journal, February 2007
- Lovejoy, Connie; Vincent, Warwick F.; Bonilla, Sylvia
- Journal of Phycology, Vol. 43, Issue 1
Green Evolution and Dynamic Adaptations Revealed by Genomes of the Marine Picoeukaryotes Micromonas
journal, April 2009
- Worden, A. Z.; Lee, J. -H.; Mock, T.
- Science, Vol. 324, Issue 5924
Increasing P-stress and viral infection impact lipid remodeling of the picophytoplankter Micromonas pusilla
journal, January 2015
- Maat, D. S.; Bale, N. J.; Hopmans, E. C.
- Biogeosciences Discussions, Vol. 12, Issue 18
Using flow cytometry for counting natural planktonic bacteria and understanding the structure of planktonic bacterial communities [Using flow cytometry for counting natural planktonic bacteria and understanding the structure of planktonic bacterial communities]
journal, June 2000
- Gasol, Josep M.; Del Giorgio, Paul A.
- Scientia Marina, Vol. 64, Issue 2
Stichochrysis immobilis is a diatom, not a chrysophyte
journal, May 1993
- Guillard, R. R. L.; Hargraves, P. E.
- Phycologia, Vol. 32, Issue 3
Allometric scaling and taxonomic variation in nutrient utilization traits and maximum growth rate of phytoplankton
journal, March 2012
- Edwards, Kyle F.; Thomas, Mridul K.; Klausmeier, Christopher A.
- Limnology and Oceanography, Vol. 57, Issue 2
Physiological responses of three species of marine pico-phytoplankton to ammonium, phosphate, iron and light limitation
journal, January 2005
- Timmermans, K. R.; van der Wagt, B.; Veldhuis, M. J. W.
- Journal of Sea Research, Vol. 53, Issue 1-2
Measurement of the Apparent Dissociation Constants of Carbonic acid in Seawater at Atmospheric Pressure1
journal, November 1973
- Mehrbach, C.; Culberson, C. H.; Hawley, J. E.
- Limnology and Oceanography, Vol. 18, Issue 6
A comparison of the equilibrium constants for the dissociation of carbonic acid in seawater media
journal, October 1987
- Dickson, A. G.; Millero, F. J.
- Deep Sea Research Part A. Oceanographic Research Papers, Vol. 34, Issue 10
TopHat2: accurate alignment of transcriptomes in the presence of insertions, deletions and gene fusions
journal, January 2013
- Kim, Daehwan; Pertea, Geo; Trapnell, Cole
- Genome Biology, Vol. 14, Issue 4
featureCounts: an efficient general purpose program for assigning sequence reads to genomic features
journal, November 2013
- Liao, Y.; Smyth, G. K.; Shi, W.
- Bioinformatics, Vol. 30, Issue 7
Moderated estimation of fold change and dispersion for RNA-seq data with DESeq2
journal, December 2014
- Love, Michael I.; Huber, Wolfgang; Anders, Simon
- Genome Biology, Vol. 15, Issue 12
Java Treeview--extensible visualization of microarray data
journal, June 2004
- Saldanha, A. J.
- Bioinformatics, Vol. 20, Issue 17
Characterizing aquatic bacteria according to population, cell size, and apparent DNA content by flow cytometry
journal, January 1989
- Robertson, B. R.; Button, D. K.
- Cytometry, Vol. 10, Issue 1
Molecular Mechanisms by Which Marine Phytoplankton Respond to Their Dynamic Chemical Environment
journal, January 2015
- Palenik, Brian
- Annual Review of Marine Science, Vol. 7, Issue 1
The Mixed Lineage Nature of Nitrogen Transport and Assimilation in Marine Eukaryotic Phytoplankton: A Case Study of Micromonas
journal, May 2010
- McDonald, Sarah M.; Plant, Joshua N.; Worden, Alexandra Z.
- Molecular Biology and Evolution, Vol. 27, Issue 10
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
Linking traits to species diversity and community structure in phytoplankton
journal, July 2010
- Litchman, Elena; de Tezanos Pinto, Paula; Klausmeier, Christopher A.
- Hydrobiologia, Vol. 653, Issue 1
Ocean's least productive waters are expanding
journal, January 2008
- Polovina, Jeffrey J.; Howell, Evan A.; Abecassis, Melanie
- Geophysical Research Letters, Vol. 35, Issue 3
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
Phytoplankton in the ocean use non-phosphorus lipids in response to phosphorus scarcity
journal, March 2009
- Van Mooy, Benjamin A. S.; Fredricks, Helen F.; Pedler, Byron E.
- Nature, Vol. 458, Issue 7234
Phosphate utilization by an oceanic diatom in phosphorus-limited chemostat culture and in the oligotrophic waters of the central North Pacific1: Phosphate utilization
journal, January 1976
- Perry, M. J.
- Limnology and Oceanography, Vol. 21, Issue 1
The Transcriptome and Proteome of the Diatom Thalassiosira pseudonana Reveal a Diverse Phosphorus Stress Response
journal, March 2012
- Dyhrman, Sonya T.; Jenkins, Bethany D.; Rynearson, Tatiana A.
- PLoS ONE, Vol. 7, Issue 3
Proteome Changes Driven by Phosphorus Deficiency and Recovery in the Brown Tide-Forming Alga Aureococcus anophagefferens
journal, December 2011
- Wurch, Louie L.; Bertrand, Erin M.; Saito, Mak A.
- PLoS ONE, Vol. 6, Issue 12
De novo assembly of Aureococcus anophagefferens transcriptomes reveals diverse responses to the low nutrient and low light conditions present during blooms
journal, July 2014
- Frischkorn, Kyle R.; Harke, Matthew J.; Gobler, Christopher J.
- Frontiers in Microbiology, Vol. 5
The Organization and Regulation of Plant Glycolysis
journal, June 1996
- Plaxton, William C.
- Annual Review of Plant Physiology and Plant Molecular Biology, Vol. 47, Issue 1
Polyphosphate in Trichodesmium from the low-phosphorus Sargasso Sea
journal, September 2010
- Orchard, Elizabeth D.; Benitez-Nelson, Claudia R.; Pellechia, Perry J.
- Limnology and Oceanography, Vol. 55, Issue 5
Phosphorus supply drives rapid turnover of membrane phospholipids in the diatom Thalassiosira pseudonana
journal, December 2010
- Martin, Patrick; Van Mooy, Benjamin AS; Heithoff, Abigail
- The ISME Journal, Vol. 5, Issue 6
Long Serial Analysis of Gene Expression for Gene Discovery and Transcriptome Profiling in the Widespread Marine Coccolithophore Emiliania huxleyi
journal, January 2006
- Dyhrman, S. T.; Haley, S. T.; Birkeland, S. R.
- Applied and Environmental Microbiology, Vol. 72, Issue 1
Characterization of ectoenzyme activity and phosphate-regulated proteins in the coccolithophorid Emiliania huxleyi
journal, October 2003
- Dyhrman, S. T.
- Journal of Plankton Research, Vol. 25, Issue 10
Utilization of phosphate diesters by phosphodiesterase-producing marine diatoms
journal, September 2013
- Yamaguchi, Haruo; Arisaka, Hiroshi; Otsuka, Naoki
- Journal of Plankton Research, Vol. 36, Issue 1
Macro-scale exhaustion of surface phosphate by dinitrogen fixation in the western North Pacific: MACRO-SCALE EXHAUSTION OF PHOSPHATE
journal, February 2009
- Hashihama, Fuminori; Furuya, Ken; Kitajima, Satoshi
- Geophysical Research Letters, Vol. 36, Issue 3
Identification of a High-Affinity Phosphate Transporter Gene in a Prasinophyte Alga, Tetraselmis chui, and Its Expression under Nutrient Limitation
journal, February 2003
- Chung, C. -C.; Hwang, S. -P. L.; Chang, J.
- Applied and Environmental Microbiology, Vol. 69, Issue 2
Arsenic cycling in marine systems
journal, September 1980
- Sanders, James G.
- Marine Environmental Research, Vol. 3, Issue 4
How Saccharomyces cerevisiae copes with toxic metals and metalloids
journal, November 2010
- Wysocki, Robert; Tamás, Markus J.
- FEMS Microbiology Reviews, Vol. 34, Issue 6
Role of Glutathione S-Transferases and Glutathione in Arsenic and Peroxide Resistance in Saccharomyces Cerevisiae: A Reverse Genetic Analysis Approach
journal, January 2007
- Todorova, T.; Vuilleumier, S.; Kujumdzieva, A.
- Biotechnology & Biotechnological Equipment, Vol. 21, Issue 3
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
Effects of Phosphorus Limitation on Respiratory Metabolism in the Green Alga Selenastrum minutum
journal, April 1991
- Theodorou, Maria E.; Elrifi, Ivor R.; Turpin, David H.
- Plant Physiology, Vol. 95, Issue 4
Detecting anthropogenic carbon dioxide uptake and ocean acidification in the North Atlantic Ocean
journal, January 2012
- Bates, N. R.; Best, M. H. P.; Neely, K.
- Biogeosciences, Vol. 9, Issue 7
Rapid shifts in picoeukaryote community structure in response to ocean acidification
journal, March 2011
- Meakin, Nicholas G.; Wyman, Michael
- The ISME Journal, Vol. 5, Issue 9
EFFECTS OF INCREASED TEMPERATURE AND CO 2 ON PHOTOSYNTHESIS, GROWTH, AND ELEMENTAL RATIOS IN MARINE SYNECHOCOCCUS AND PROCHLOROCOCCUS (CYANOBACTERIA)
journal, June 2007
- Fu, Fei-Xue; Warner, Mark E.; Zhang, Yaohong
- Journal of Phycology, Vol. 43, Issue 3
MS Excel Program Developed for CO2 System Calculations
dataset, January 2006
- Environmental Sciences Division, Oak Ridge National Laboratory
- Carbon Dioxide Information Analysis Center (CDIAC)
A comparison of the equilibrium constants for the dissociation of carbonic acid in seawater media
journal, October 1987
- Dickson, A. G.; Millero, F. J.
- Deep Sea Research Part A. Oceanographic Research Papers, Vol. 34, Issue 10
Plankton community response to sequential silicate and nitrate depletion during the 1989 North Atlantic spring bloom
journal, January 1993
- Sieracki, Michael E.; Verity, Peter G.; Stoecker, Diane K.
- Deep Sea Research Part II: Topical Studies in Oceanography, Vol. 40, Issue 1-2
New aspects of inorganic polyphosphate metabolism and function
journal, January 1999
- Kulaev, Igor; Vagabov, Vladimir; Kulakovskaya, Tatiana
- Journal of Bioscience and Bioengineering, Vol. 88, Issue 2
Induction of both acid and alkaline phosphatase activity in two green-algae (chlorophyceae) in low N and P concentrations
journal, February 2004
- Kruskopf, Mikaela Maria; Du Plessis, Sandra
- Hydrobiologia, Vol. 513, Issue 1
Phosphorus supply drives rapid turnover of membrane phospholipids in the diatom Thalassiosira pseudonana
journal, December 2010
- Martin, Patrick; Van Mooy, Benjamin AS; Heithoff, Abigail
- The ISME Journal, Vol. 5, Issue 6
Erratum: Significant CO2 fixation by small prymnesiophytes in the subtropical and tropical northeast Atlantic Ocean
journal, November 2013
- Jardillier, Ludwig; Zubkov, Mikhail V.; Pearman, John
- The ISME Journal, Vol. 7, Issue 12
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
Phytoplankton in the ocean use non-phosphorus lipids in response to phosphorus scarcity
journal, March 2009
- Van Mooy, Benjamin A. S.; Fredricks, Helen F.; Pedler, Byron E.
- Nature, Vol. 458, Issue 7234
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
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
The Mixed Lineage Nature of Nitrogen Transport and Assimilation in Marine Eukaryotic Phytoplankton: A Case Study of Micromonas
journal, May 2010
- McDonald, Sarah M.; Plant, Joshua N.; Worden, Alexandra Z.
- Molecular Biology and Evolution, Vol. 27, Issue 10
How Saccharomyces cerevisiae copes with toxic metals and metalloids
journal, November 2010
- Wysocki, Robert; Tamás, Markus J.
- FEMS Microbiology Reviews, Vol. 34, Issue 6
Green Evolution and Dynamic Adaptations Revealed by Genomes of the Marine Picoeukaryotes Micromonas
journal, April 2009
- Worden, A. Z.; Lee, J. -H.; Mock, T.
- Science, Vol. 324, Issue 5924
Phosphate Depletion in the Western North Atlantic Ocean
journal, August 2000
- Wu, J.
- Science, Vol. 289, Issue 5480
Ecological Genomics of Marine Picocyanobacteria
journal, June 2009
- Scanlan, D. J.; Ostrowski, M.; Mazard, S.
- Microbiology and Molecular Biology Reviews, Vol. 73, Issue 2
Molecular Mechanisms by Which Marine Phytoplankton Respond to Their Dynamic Chemical Environment
journal, January 2015
- Palenik, Brian
- Annual Review of Marine Science, Vol. 7, Issue 1
The Organization and Regulation of Plant Glycolysis
journal, June 1996
- Plaxton, William C.
- Annual Review of Plant Physiology and Plant Molecular Biology, Vol. 47, Issue 1
TopHat2: accurate alignment of transcriptomes in the presence of insertions, deletions and gene fusions
journal, January 2013
- Kim, Daehwan; Pertea, Geo; Trapnell, Cole
- Genome Biology, Vol. 14, Issue 4
Moderated estimation of fold change and dispersion for RNA-seq data with DESeq2
journal, December 2014
- Love, Michael I.; Huber, Wolfgang; Anders, Simon
- Genome Biology, Vol. 15, Issue 12
Proteome Changes Driven by Phosphorus Deficiency and Recovery in the Brown Tide-Forming Alga Aureococcus anophagefferens
journal, December 2011
- Wurch, Louie L.; Bertrand, Erin M.; Saito, Mak A.
- PLoS ONE, Vol. 6, Issue 12
The Transcriptome and Proteome of the Diatom Thalassiosira pseudonana Reveal a Diverse Phosphorus Stress Response
journal, March 2012
- Dyhrman, Sonya T.; Jenkins, Bethany D.; Rynearson, Tatiana A.
- PLoS ONE, Vol. 7, Issue 3
De novo assembly of Aureococcus anophagefferens transcriptomes reveals diverse responses to the low nutrient and low light conditions present during blooms
journal, July 2014
- Frischkorn, Kyle R.; Harke, Matthew J.; Gobler, Christopher J.
- Frontiers in Microbiology, Vol. 5
Measurement of the Apparent Dissociation Constants of Carbonic acid in Seawater at Atmospheric Pressure1
journal, November 1973
- Mehrbach, C.; Culberson, C. H.; Hawley, J. E.
- Limnology and Oceanography, Vol. 18, Issue 6
Works referencing / citing this record:
Genomic adaptation of marine phytoplankton populations regulates phosphate uptake
journal, January 2020
- Martiny, Adam C.; Ustick, Lucas; A. Garcia, Catherine
- Limnology and Oceanography, Vol. 65, Issue S1
Phosphonate utilization by eukaryotic phytoplankton: Phosphonate utilization
journal, December 2018
- Whitney, LeAnn P.; Lomas, Michael W.
- Limnology and Oceanography Letters, Vol. 4, Issue 1
Cell abundance, growth rate, cellular P quotas, and alkaline phosphatase activity from a laboratory experiment examining the response of three species of marine phytoplankton grown under different phosphorus (P) conditions
dataset, January 2020
- Whitney, LeAnn; Lomas, Michael
- Biological and Chemical Oceanography Data Management Office (BCO-DMO)
Evaluation of Mixotrophy-Associated Gene Expression in Two Species of Polar Marine Algae
journal, August 2018
- McKie-Krisberg, Zaid M.; Sanders, Robert W.; Gast, Rebecca J.
- Frontiers in Marine Science, Vol. 5