The Transcriptome and Proteome of the Diatom Thalassiosira pseudonana Reveal a Diverse Phosphorus Stress Response
Open accessAbstract
Phosphorus (P) is a critical driver of phytoplankton growth and ecosystem function in the ocean. Diatoms are an abundant class of marine phytoplankton that are responsible for significant amounts of primary production. With the control they exert on the oceanic carbon cycle, there have been a number of studies focused on how diatoms respond to limiting macro and micronutrients such as iron and nitrogen. However, diatom physiological responses to P deficiency are poorly understood. Here, we couple deep sequencing of transcript tags and quantitative proteomics to analyze the diatom Thalassiosira pseudonana grown under P-replete and P-deficient conditions. A total of 318 transcripts were differentially regulated with a false discovery rate of <0.05, and a total of 136 proteins were differentially abundant (p<0.05). Significant changes in the abundance of transcripts and proteins were observed and coordinated for multiple biochemical pathways, including glycolysis and translation. Patterns in transcript and protein abundance were also linked to physiological changes in cellular P distributions, and enzyme activities. These data demonstrate that diatom P deficiency results in changes in cellular P allocation through polyphosphate production, increased P transport, a switch to utilization of dissolved organic P through increased production of metalloenzymes, and a remodeling of the cell surface through production of sulfolipids. Together, these findings reveal that T. pseudonana has evolved a sophisticated response to P deficiency involving multiple biochemical strategies that are likely critical to its ability to respond to variations in environmental P availability.
The claims and statistics of this paper haven’t been checked yet.
Run the check — free, no account needed. It reads the open-access text and checks the sources it cites.
Integrity signals
Registry
Cites
Statistics
Claims the paper makes
The claims and statistics of this paper haven’t been checked yet.
Run the check — free, no account needed. It reads the open-access text and checks the sources it cites.
Claims other papers make about this one
Each is checked against this paper’s own text: does it say what the citing paper says it does?
In 2012, Dyhrman et al. identified cell surface-associated APase, suggesting that Pi hydrolysis and Pi uptake may be tightly coupled.
“In 2012, Dyhrman et al. [34] identified cell surface–associated APase, suggesting that Pi hydrolysis and Pi uptake may be “tightly coupled.””
From A Review of Phosphate Mineral Nucleation in Biology and Geobiology (2013) · cites this paper as [34]
Dyhrman et al. identified polyP polymerase regulation, with cellular P condensing to polyP.
“They also identified polyP polymerase regulation, with cellular P condensing to polyP”
From A Review of Phosphate Mineral Nucleation in Biology and Geobiology (2013) · cites this paper as [34]
Alkaline phosphatases are theorized to cleave inorganic phosphate from polyphosphate in diatoms.
“APases cleave Pi from ester phosphates at neutral to basic pH [33] and are theorized to cleave Pi from polyP in diatoms [34].”
From A Review of Phosphate Mineral Nucleation in Biology and Geobiology (2013) · cites this paper as [34]
The Results and Discussion section describes alkaline phosphatases acting on phosphomonoesters and separately discusses polyphosphate accumulation and cycling. Neither that section nor the Conclusions says that alkaline phosphatases are theorized to release inorganic phosphate from polyphosphate; searches for that proposed link found no passage addressing it. (LLM, conf=0.75)
Experimental — accuracy not yet measured
Self-check
Percentages, sums and reported differences re-computed from the paper’s own numbers.
The self-check needs the paper’s full text.
The citation lists haven’t been fetched yet
References 76 · Cited by 337
Research works printed but not linked: 49
- [2]Coleman ML Chisholm SW 2010 Ecosystem-specific selection pressures revealed through comparative population genomics. Proc Nat Acad Sci 107 18634 18639 20937887 PMC2972931
- [7]Paytan A McLaughlin K 2007 The oceanic phosphorus cycle. Chemical Reviews 107 563 576 17256993
- [8]Diaz J Ingall E Benitez-Nelson C Paterson D de Jonge MD 2008 Marine polyphosphate: A key player in geologic phosphorus sequestration. Science 320 652 655 18451299
- [9]Grossman A 2000 Acclimation of Chlamydomonas reinhardtii to its nutrient environment. Protist 151 201 224 11079767
- [11]Riegman R Stolte W Noordeloos AAM Slezak D 2000 Nutrient uptake, and alkaline phosphate (EC 3: 1: 3: 1) activity of Emiliania huxleyi (Prymnesiophyceae) during growth under N and P limitation in continuous cultures. J Phycol 36 87 96 29544012
- [13]Dyhrman ST Palenik BP 1999 Phosphate stress in cultures and field populations of the dinoflagellate Prorocentrum minimum detected using a single cell alkaline phosphatase activity assay. Appl Environ Microbiol 65 3205 3212 10388722 PMC91475
- [16]Li QY Gao XS Sun Y Zhang QQ Song RT 2006 Isolation and characterization of a sodium-dependent phosphate transporter gene in Dunaliella viridis. Biochem Bioph Res Co 340 95 104 16359638
- [18]Allen AE LaRoche J Maheswari U Lommer M Schauer N 2008 Whole-cell response of the pennate diatom Phaeodactylum tricornutum to iron starvation. Proc Nat Acad Sci 105 10438 10443 18653757 PMC2492447
- [19]Mock T Samanta MP Iverson V Berthiaume C Robison M 2008 Whole-genome expression profiling of the marine diatom Thalassiosira pseudonana identifies genes involved in silicon bioprocesses. Proc Nat Acad Sci 105 1579 1584 18212125 PMC2234187
- [20]Thamatrakoln K Korenovska O Niheu AK Bidle KD 2012 Whole-genome expression analysis reveals a role for death-related genes in stress acclimation of the diatom Thalassiosira pseudonana. Enivron Microbiol 14 67 81 21453404
- [21]Morrissy AS Morin RD Delaney A Zeng T McDonald H 2009 Next-generation tag sequencing for cancer gene expression profiling. Genome Res 19 1825 1835 19541910 PMC2765282
- [22]'t Hoen PAC Ariyurek Y Thygesen HH Vreugdenhil E Vossen RHAM 2008 Deep sequencing-based expression analysis shows major advances in robustness, resolution and inter-lab portability over five microarray platforms. Nucleic Acids Res 36 e141 18927111 PMC2588528
- [24]Nowrousian M 2010 Next-generation sequencing techniques for eukaryotic microorganisms: Sequencing-based solutions to biological problems. Eukaryot Cell 9 1300 1310 20601439 PMC2937339
- [25]Wu ZJ Jenkins BD Rynearson TA Dyhrman ST Saito MA 2010 Empirical bayes analysis of sequencing-based transcriptional profiling without replicates. BMC Bioinformatics 11 564 21080965 PMC3098101
- [26]Saito MA Bertrand EM Dutkiewicz S Bulygin VV Moran DM 2011 Iron conservation by reduction of metalloenzyme inventories in the marine diazotroph Crocosphaera watsonii. Proc Nat Acad Sci 108 2184 2189 21248230 PMC3038740
- [27]Thompson DK Beliaev AS Giometti CS Tollaksen SL Khare T 2002 Transcriptional and proteomic analysis of a ferric uptake regulator (fur) mutant of Shewanella oneidensis: Possible involvement of fur in energy metabolism, transcriptional regulation, and oxidative stress. Appl Environ Microbiol 68 881 892 11823232 PMC126683
- [29]Castruita M Casero D Karpowicz SJ Kropat J Vieler A 2011 Systems biology approach in Chlamydomonas reveals connections between copper nutrition and multiple metabolic steps. Plant Cell 23 1273 1292 21498682 PMC3101551
- [30]Armbrust EV Berges JA Bowler C Green BR Martinez D 2004 The genome of the diatom Thalassiosira pseudonana: Ecology, evolution, and metabolism. Science 306 79 86 15459382
- [31]Wiu JQ Du J Rozowsky J Zhang Z Urban AE 2008 Systematic analysis of transcribed loci in ENCODE regions using RACE sequencing reveals extensive transcription in the human genome. Genome Biol 9 R3 doi: 10.1186/gb-2008-1189-1181-r1183 18173853 PMC2395237 · DOI
- [32]Wurch LL Haley ST Orchard ED Gobler CJ Dyhrman ST 2011 Nutrient-regulated transcriptional responses in the brown tide forming alga Aureococcus anophagefferens. Environ Microbiol 13 468 481 20880332 PMC3282463
- [33]Dyhrman ST Haley ST Birkeland SR Wurch LL Cipriano MJ 2006 Long serial analysis of gene expression for gene discovery and transcriptome profiling in the widespread marine coccolithophore Emiliania huxleyi. Appl Environ Microbiol 72 252 260 16391051 PMC1352234
- [34]Moustafa A Evans AN Kulis DM Hackett JD Erdner DL 2010 Transcriptome profiling of a toxic dinoflagellate reveals a gene-rich protist and a potential impact on gene expression due to bacterial presence. PLoS One 5 e9688 doi: 9610.1371/journal.pone.0009688 20300646 PMC2837391 · DOI
- [35]Peng JM Elias JE Thoreen CC Licklider LJ Gygi SP 2003 Evaluation of multidimensional chromatography coupled with tandem mass spectrometry (LC/LC-MS/MS) for large-scale protein analysis: The yeast proteome. J Proteome Res 2 43 50 12643542
- [36]Le Bihan T Martin SF Chirnside ES van Ooijen G Barrios-Llerena ME 2011 Shotgun proteomic analysis of the unicellular alga Ostreococcus tauri. J Prot doi: 10.1016/j.jprot.2011.05.028 21635980 · DOI
- [37]Nunn BL Aker JR Shaffer SA Tsai YH Strzepek RF 2009 Deciphering diatom biochemical pathways via whole-cell proteomics. Aquat Microbial Ecol 55 241 253 PMC2761042 19829762
- [38]Ogawa N DeRisi J Brown PO 2000 New components of a system for phosphate accumulation and polyphosphate metabolism in Saccharomyces cerevisiae revealed by genomic expression analysis. Molec Biol Cell 11 4309 4321 11102525 PMC15074
- [39]Hothorn M Neumann H Lenherr ED Wehner M Rybin V 2009 Catalytic core of a membrane-associated eukaryotic polyphosphate polymerase. Science 324 513 516 19390046
- [40]Kornberg A Rao NN Ault-Riche D 1999 Inorganic polyphosphate: A molecule of many functions. Ann Rev Biochem 68 89 125 10872445
- [41]Karl DM Björkman KM 2002 Dynamics of DOP. Hansell D Carlson C Biogeochemistry of Marine Dissolved Organic Matter Boston Elsevier Science 249 366
- [44]Luo HW Benner R Long RA Hu JJ 2009 Subcellular localization of marine bacterial alkaline phosphatases. Proc Nat Acad Sci 106 21219 21223 19926862 PMC2795515
- [45]Dyhrman ST Palenik B 1999 Phosphate stress in cultures and field populations of the dinoflagellate Prorocentrum minimum detected by a single-cell alkaline phosphatase assay. Appl Environ Microbiol 65 3205 3212 10388722 PMC91475
- [46]Ammerman JW Azam F 1985 Bacterial 5′-Nucleotidase in aquatic ecosystems - a novel mechanism of phosphorus regeneration. Science 227 1338 1340 17793769
- [48]Brzoska P Boos W 1989 The Ugp-encoded glycerophosphoryldiester phosphodiesterase, a transport-related enzyme of Escherichia coli. FEMS Microbiol Rev 63 115 124 2561262
- [50]Martin P Van Mooy BAS Heithoff A Dyhrman ST 2011 Phosphorus supply drives rapid turnover of membrane phospholipids in the diatom Thalassiosira pseudonana. ISME J 5 1057 1060 21160536 PMC3131859
- [51]Van Mooy BAS Fredricks HF Pedler BE Dyhrman ST Karl DM 2009 Phytoplankton in the ocean use non-phosphorus lipids in response to phosphorus scarcity. Nature 458 69 72 19182781
- [52]Guler S Essigmann B Benning C 2000 A cyanobacterial gene, sqdX, required for biosynthesis of the sulfolipid sulfoquinovosyldiacylglyerol. J Bact 182 543 545 10629209 PMC94312
- [53]Benning C 1998 Biosynthesis and function of the sulfolipid sulfoquinovosyl diacylglycerol. Ann Rev Plant Physiol Plant Molec Biol 49 53 75 15012227
- [54]Riekhof WR Andre C Benning C 2005 Two enzymes, BtaA and BtaB, are sufficient for betaine lipid biosynthesis in bacteria. Archives Biochem Biophys 441 96 105 16095555
- [55]Riekhof WR Sears BB Benning C 2005 Annotation of genes involved in glycerolipid biosynthesis in Chlamydomonas reinhardtii: Discovery of the betaine lipid synthase BTA1(Cr). Eukaryot Cell 4 242 252 15701786 PMC549322
- [56]Theodorou ME Elrifi IR Turpin DH Plaxton WC 1991 Effects of phosphorus limitation on respiratory metabolism in the green-alga Selenastrum minutum. Plant Physiol 95 1089 1095 16668095 PMC1077656
- [57]Duff SMG Moorhead GBG Lefebvre DD Plaxton WC 1989 Phosphate starvation inducible bypasses of adenylate and phosphate dependent glycolytic-enzymes in Brassica nigra suspension cells. Plant Physiol 90 1275 1278 16666922 PMC1061882
- [58]Wurch LL Bertrand EM Saito MA Van Mooy BAS Dyhrman ST 2011 Proteome changes driven by phosphorus deficiency and recovery in the brown tide-forming alga Aureococcus anophagefferens. PLoS One 6 e28949 doi: 28910.21371/journal.pone.0028949 22194955 PMC3237563 · DOI
- [59]Tetu SG Brahamsha B Johnson DA Tai V Phillippy K 2009 Microarray analysis of phosphate regulation in the marine cyanobacterium Synechococcus sp WH8102. ISME J 3 835 849 19340084
- [61]Spassov DS Jurecic R 2003 The PUF family of RNA-binding proteins: Does evolutionarily conserved structure equal conserved function? Iubmb Life 55 359 366 14584586
- [62]Wickens M Bernstein DS Kimble J Parker R 2002 A PUF family portrait: 3 ′ UTR regulation as a way of life. Trends Genet 18 150 157 11858839
- [63]Fedoroff NV 2002 RNA-binding proteins in plants: the tip of an iceberg? Cur Opinion Plant Biol 5 452 459 12183185
- [68]Lu XN Zhu HN 2005 Tube-gel digestion - A novel proteomic approach for high throughput analysis of membrane proteins. Molec Cellular Prot 4 1948 1958 PMC1360194 16150870
- [69]Keller A Nesvizhskii AI Kolker E Aebersold R 2002 Empirical statistical model to estimate the accuracy of peptide identifications made by MS/MS and database search. Analytical Chem 74 5383 5392 12403597
- [70]Zhang B VerBerkmoes NC Langston MA Uberbacher E Hettich RL 2006 Detecting differential and correlated protein expression in label-free shotgun proteomics. J Proteome Res 5 2909 2918 17081042
- Authors
- Dyhrman, S. T., Jenkins, B. D., Rynearson, T. A., Saito, M. A., Mercier, M. L., Alexander, H., Whitney, L. P., Drzewianowski, A., Bulygin, V. V., Bertrand, E. M., Wu, Z., Benitez-Nelson, C., & Heithoff, A.
- Affiliations
- Woods Hole Oceanographic Institution (US)
- University of Rhode Island (US)
- Brown University (US)
- Corresponding author
- Dyhrman, Sonya T.
- Jenkins, Bethany D.
- Rynearson, Tatiana A.
- Saito, Mak A.
- Mercier, Melissa L.
- Alexander, Harriet
- Whitney, LeAnn P.
- Drzewianowski, Andrea
- Bulygin, Vladimir V.
- Bertrand, Erin M.
- Wu, Zhijin
- Heithoff, Abigail
- ORCID
- Venue
- PLoS ONE
- Publisher
- Public Library of Science (PLoS)
- Published
- 2012-03-29
- Volume
- 7
- Issue
- 3
- Pages
- e33768
- ISSN
- 1932-6203 (ISSN-L)
- PMC
- PMC3315573
- OpenAlex
- W2075935267
- Cited by
- 337
- References
- 76
- Citations by year
- 2026: 18 · 2025: 17 · 2024: 17 · 2023: 32 · 2022: 26 · 2021: 20 · 2020: 26 · 2019: 33 · 2018: 26 · 2017: 29 · 2016: 28 · 2015: 22 · 2014: 22 · 2013: 12 · 2012: 7
- FWCI
- 14.88
- Type
- journal article
- Language
- en
- Open access
- gold
- doi.org
- Locations
- PLoS ONE (publishedVersion, cc-by)
- Europe PMC (PubMed Central) (publishedVersion, cc-by)
- PubMed Central (publishedVersion, cc-by)
- PubMed (publishedVersion)
- Figshare (submittedVersion, cc-by)
- Journal of Media Literacy Education (submittedVersion, cc-by-nc)
- Scholar Commons (University of South Carolina) (submittedVersion, cc-by)
- Open Access Server of the Woods Hole Scientific Community (Woods Hole Scientific Community) (submittedVersion, cc-by)
- DOAJ (DOAJ: Directory of Open Access Journals) (submittedVersion, cc-by-sa)
- Funders
- National Science Foundation (0752291, 0526800, 0723667, 0549794, 0554548, 1004057)
- U.S. Department of Energy
- Gordon and Betty Moore Foundation
- Joint Genome Institute
- Office of Experimental Program to Stimulate Competitive Research (0554548, 1004057)
- Topics
- Physical Sciences › Earth and Planetary Sciences › Oceanography › Marine and coastal ecosystems
- Physical Sciences › Materials Science › Biomaterials › Diatoms and Algae Research
- Physical Sciences › Environmental Science › Environmental Chemistry › Aquatic Ecosystems and Phytoplankton Dynamics
- Keywords
- Thalassiosira pseudonana, diatoms, phosphorus deficiency, transcriptome, proteome, phosphorus transport, dissolved organic phosphorus, metalloenzymes, sulfolipids, glycolysis, translation (biology), nutrient limitation
- MeSH terms
- Biological Transport, Glycolysis, Phosphorus, Stress, Physiological, Protein Biosynthesis, Diatoms, Proteome, Transcriptome
About these checks
Registry, retraction, Cites and statistics results are computed, not judged, with one exception: a printed reference that no index lists is read once by a model before it counts as a citation error. Claims are extracted by a model and kept only when their quote appears verbatim in the text; each cited source is then checked, with a model’s help, for whether it says what the claim relies on. Those verdicts can be wrong — read the claim’s quote and the cited source before relying on one.
Statistics and arithmetic are recomputed, not judged.
Confidence bands are shown only for fields calibrated on our annotated test set. None is calibrated yet, so no band is shown.
What counts as a claim ›How we measure confidence ›How we check this ›
Are you an author, or do you see a problem with this page? Request a review