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

Title: 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 » 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.« less

Authors:
 [1];  [1]
  1. 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. doi: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. doi: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 = {2016},
month = {5}
}

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

Citation Metrics:
Cited by: 1 work
Citation information provided by
Web of Science

Save / Share:

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
  • DOI: 10.1016/S0967-0645(00)00166-1

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
  • DOI: 10.1038/ismej.2010.36

Evidence for aggregation and export of cyanobacteria and nano-eukaryotes from the Sargasso Sea euphotic zone
journal, January 2011


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
  • DOI: 10.1038/ngeo1265

The biogeochemical cycling of phosphorus in marine systems
journal, August 2000


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
  • DOI: 10.1029/2003EO180001

Microbes and the Marine Phosphorus Cycle
journal, June 2007


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
  • DOI: 10.1038/ngeo232

Sargasso Sea phosphorus biogeochemistry: an important role for dissolved organic phosphorus (DOP)
journal, January 2010


Phosphate Depletion in the Western North Atlantic Ocean
journal, August 2000


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
  • DOI: 10.1016/S0967-0637(01)00027-9

Cell-specific detection of phosphorus stress in Trichodesmium from the Western North Atlantic
journal, November 2002


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
  • DOI: 10.4319/lo.2004.49.6.2303

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
  • DOI: 10.3354/ame01348

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
  • DOI: 10.1029/2005GB002510

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
  • DOI: 10.1029/2008GB003389

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
  • DOI: 10.1002/2013GB004801

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
  • DOI: 10.1038/ismej.2011.117

Distribution, Phylogeny, and Growth of Cold-Adapted Picoprasinophytes in Arctic seas
journal, February 2007


Green Evolution and Dynamic Adaptations Revealed by Genomes of the Marine Picoeukaryotes Micromonas
journal, April 2009


Elevated CO 2 and Phosphate Limitation Favor Micromonas pusilla through Stimulated Growth and Reduced Viral Impact
journal, March 2014

  • Maat, Douwe S.; Crawfurd, Katherine J.; Timmermans, Klaas R.
  • Applied and Environmental Microbiology, Vol. 80, Issue 10
  • DOI: 10.1128/AEM.03639-13

Increasing P-stress and viral infection impact lipid remodeling of the picophytoplankter Micromonas pusilla
journal, January 2015


Stichochrysis immobilis is a diatom, not a chrysophyte
journal, May 1993


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
  • DOI: 10.4319/lo.2012.57.2.0554

Physiological responses of three species of marine pico-phytoplankton to ammonium, phosphate, iron and light limitation
journal, January 2005


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
  • DOI: 10.1016/0967-0645(93)90014-E

Measurement of the Apparent Dissociation Constants of Carbonic acid in Seawater at Atmospheric Pressure1
journal, November 1973


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
  • DOI: 10.1016/0198-0149(87)90021-5

TopHat2: accurate alignment of transcriptomes in the presence of insertions, deletions and gene fusions
journal, January 2013


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


Moderated estimation of fold change and dispersion for RNA-seq data with DESeq2
journal, December 2014


Java Treeview--extensible visualization of microarray data
journal, June 2004


Characterizing aquatic bacteria according to population, cell size, and apparent DNA content by flow cytometry
journal, January 1989


Molecular Mechanisms by Which Marine Phytoplankton Respond to Their Dynamic Chemical Environment
journal, January 2015


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
  • DOI: 10.1093/molbev/msq113

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

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
  • DOI: 10.1007/s10750-010-0341-5

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
  • DOI: 10.1029/2007GL031745

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

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
  • DOI: 10.1038/nature07659

The Transcriptome and Proteome of the Diatom Thalassiosira pseudonana Reveal a Diverse Phosphorus Stress Response
journal, March 2012


Proteome Changes Driven by Phosphorus Deficiency and Recovery in the Brown Tide-Forming Alga Aureococcus anophagefferens
journal, December 2011


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
  • DOI: 10.3389/fmicb.2014.00375

The Organization and Regulation of Plant Glycolysis
journal, June 1996


Induction of both acid and alkaline phosphatase activity in two green-algae (chlorophyceae) in low N and P concentrations
journal, February 2004


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
  • DOI: 10.1016/S1389-1723(99)80189-3

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
  • DOI: 10.4319/lo.2010.55.5.2161

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
  • DOI: 10.1038/ismej.2010.192

Long Serial Analysis of Gene Expression for Gene Discovery and Transcriptome Profiling in the Widespread Marine Coccolithophore Emiliania huxleyi
journal, January 2006


Characterization of ectoenzyme activity and phosphate-regulated proteins in the coccolithophorid Emiliania huxleyi
journal, October 2003


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
  • DOI: 10.1093/plankt/fbt091

Ecological Genomics of Marine Picocyanobacteria
journal, June 2009

  • Scanlan, D. J.; Ostrowski, M.; Mazard, S.
  • Microbiology and Molecular Biology Reviews, Vol. 73, Issue 2
  • DOI: 10.1128/MMBR.00035-08

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
  • DOI: 10.1029/2008GL036866

Identification of a High-Affinity Phosphate Transporter Gene in a Prasinophyte Alga, Tetraselmis chui, and Its Expression under Nutrient Limitation
journal, February 2003


Arsenic cycling in marine systems
journal, September 1980


How Saccharomyces cerevisiae copes with toxic metals and metalloids
journal, November 2010


Role of Glutathione S-Transferases and Glutathione in Arsenic and Peroxide Resistance in Saccharomyces Cerevisiae: A Reverse Genetic Analysis Approach
journal, January 2007


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

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
  • DOI: 10.1104/pp.95.4.1089

Detecting anthropogenic carbon dioxide uptake and ocean acidification in the North Atlantic Ocean
journal, January 2012


Rapid shifts in picoeukaryote community structure in response to ocean acidification
journal, March 2011


    Works referencing / citing this record:

    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
    • DOI: 10.3389/fmars.2018.00273

    Phosphonate utilization by eukaryotic phytoplankton: Phosphonate utilization
    journal, December 2018

    • Whitney, LeAnn P.; Lomas, Michael W.
    • Limnology and Oceanography Letters, Vol. 4, Issue 1
    • DOI: 10.1002/lol2.10100

    Phosphonate utilization by eukaryotic phytoplankton: Phosphonate utilization
    journal, December 2018

    • Whitney, LeAnn P.; Lomas, Michael W.
    • Limnology and Oceanography Letters, Vol. 4, Issue 1
    • DOI: 10.1002/lol2.10100

    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
    • DOI: 10.3389/fmars.2018.00273