in

Diminished carbon and nitrate assimilation drive changes in diatom elemental stoichiometry independent of silicification in an iron-limited assemblage

  • Tréguer PJ, Sutton JN, Brzezinski MA, Charette MA, Devries T, Dutkiewicz S, et al. Reviews and syntheses: the biogeochemical cycle of silicon in the modern ocean. Biogeosciences. 2021;18:1269–89.

    Article 
    CAS 

    Google Scholar 

  • Hutchins DA, Bruland KW. Iron-limited diatom growth and Si:N uptake ratios in a coastal upwelling regime. Nature. 1998;393:561–4.

    CAS 
    Article 

    Google Scholar 

  • King AL, Barbeau KA. Evidence for phytoplankton iron limitation in the southern California Current System. Mar Ecol Prog Ser. 2007;342:91–103.

    CAS 
    Article 

    Google Scholar 

  • Pichevin LE, Ganeshram RS, Geibert W, Thunell R, Hinton R. Silica burial enhanced by iron limitation in oceanic upwelling margins. Nat Geosci. 2014;7:541–6.

    CAS 
    Article 

    Google Scholar 

  • Brzezinski MA, Krause JW, Bundy RM, Barbeau M, Franks KA, Goericke RP, et al. Enhanced silica ballasting from iron stress sustains carbon export in a frontal zone within the California Current. J Geophys Res Ocean. 2015;120:4654–69.

    Article 

    Google Scholar 

  • Baines SB, Twining BS, Vogt S, Balch WM, Fisher NS, Nelson DM. Elemental composition of equatorial Pacific diatoms exposed to additions of silicic acid and iron. Deep Res Part II Top Stud Oceanogr. 2011;58:512–23.

    CAS 
    Article 

    Google Scholar 

  • de Baar HJW, van Heuven SMAC, Middag R. Biochemical cycling and trace elements. Encycl Earth Sci Ser. 2017;14:1–21.

  • Assmy P, Smetacek V, Montresor M, Klaas C, Henjes J, Strass VH, et al. Thick-shelled, grazer-protected diatoms decouple ocean carbon and silicon cycles in the iron-limited Antarctic Circumpolar Current. Proc Natl Acad Sci. 2013;110:20633–8.

    CAS 
    PubMed 
    PubMed Central 
    Article 

    Google Scholar 

  • Leynaert A, Bucciarelli E, Claquin P, Dugdale RC, Martin-jézéquel V, Pondaven P, et al. Effect of iron deficiency on diatom cell size and silicic acid uptake kinetics. Limnol Oceanogr. 2004;49:1134–43.

    CAS 
    Article 

    Google Scholar 

  • Marchetti A, Harrison PJ. Coupled changes in the cell morphology and the elemental (C, N, and Si) composition of the pennate diatom Pseudo-nitzschia due to iron deficiency. Limnol Oceanogr. 2007;52:2270–84.

    CAS 
    Article 

    Google Scholar 

  • McNair HM, Brzezinski MA, Krause JW. Diatom populations in an upwelling environment decrease silica content to avoid growth limitation. Environ Microbiol. 2018;20:4184–93.

    CAS 
    PubMed 
    PubMed Central 
    Article 

    Google Scholar 

  • Glibert PM, McCarthy JK. Uptake and assimilation of ammonium and nitrate by phytoplankton: Indices of nutritional status for natural assemblages. J Plankton Res. 1984;6:677–97.

    CAS 
    Article 

    Google Scholar 

  • Takeda S. Influence of iron availability on nutrient consumption ratio of diatoms in oceanic waters. Nature. 1998;393:774–7.

    CAS 
    Article 

    Google Scholar 

  • Timmermans KR, Van Der Wagt B, De Baar HJW. Growth rates, half-saturation constants, and silicate, nitrate, and phosphate depletion in relation to iron availability of four large, open-ocean diatoms from the Southern Ocean. Limnol Oceanogr. 2004;49:2141–51.

    CAS 
    Article 

    Google Scholar 

  • Brzezinski MA, Olson R, Chisholm SW. Silicon availability and cell-cycle progression in marine diatoms. Mar Ecol Prog Ser. 1990;67:83–96.

    CAS 
    Article 

    Google Scholar 

  • Hildebrand M, Volcani BE, Gassmann W, Schroeder JI. A gene family of silicon transporters. Nature. 1997;385:688–9.

    CAS 
    PubMed 
    Article 

    Google Scholar 

  • Durkin CA, Marchetti A, Bender SJ, Truong T, Morales RL, Mock T, et al. Frustule-related gene transcription and the influence of diatom community composition on silica precipitation in an iron-limited environment. Limnol Oceanogr. 2012;57:1619–33.

    CAS 
    Article 

    Google Scholar 

  • Allen AE, LaRoche J, Maheswari U, Lommer M, Schauer N, Lopez PJ, et al. Whole-cell response of the pennate diatom Phaeodactylum tricornutum to iron starvation. Proc Natl Acad Sci. 2008;105:10438–43.

    CAS 
    PubMed 
    PubMed Central 
    Article 

    Google Scholar 

  • Meyerink SW, Ellwood MJ, Maher WA, Dean Price G, Strzepek RF. Effects of iron limitation on silicon uptake kinetics and elemental stoichiometry in two Southern Ocean diatoms, Eucampia antarctica and Proboscia inermis, and the temperate diatom Thalassiosira pseudonana. Limnol Oceanogr. 2017;62:2445–62.

    CAS 
    Article 

    Google Scholar 

  • Marchetti A, Schruth DM, Durkin CA, Parker MS, Kodner RB, Berthiaume CT, et al. Comparative metatranscriptomics identifies molecular bases for the physiological responses of phytoplankton to varying iron availability. Proc Natl Acad Sci USA. 2012;109:E317–25.

    CAS 
    PubMed 
    PubMed Central 
    Article 

    Google Scholar 

  • Boyd PW, Muggli DL, Varela DE, Goldblatt RH, Chretien R, Orians KJ, et al. In vitro iron enrichment experiments in the NE subarctic pacific. Mar Ecol Prog Ser. 1996;136:179–93.

    CAS 
    Article 

    Google Scholar 

  • Marchetti A, Sherry ND, Kiyosawa H, Tsuda A, Harrison PJ. Phytoplankton processes during a mesoscale iron enrichment in the NE subarctic Pacific: Part I-Biomass and assemblage. Deep Res Part II Top Stud Oceanogr. 2006;53:2095–113.

    Article 

    Google Scholar 

  • La Roche J, Geider RJ, Graziano LM, Murray H, Lewis K. Induction of specific proteins in eukaryotic algae grown under iron-, phosphorus-, or nitrogen-deficient conditions. J Phycol. 1993;29:767–77.

    Article 

    Google Scholar 

  • Peers G, Price NM. Copper-containing plastocyanin used for electron transport by an oceanic diatom. Nature. 2006;441:341–4.

    CAS 
    PubMed 
    Article 

    Google Scholar 

  • Boyd PW, Berges JA, Harrison PJ. In vitro iron enrichment experiments at iron-rich and -poor sites in the NE subarctic Pacific. J Exp Mar Bio Ecol. 1998;227:133–51.

    CAS 
    Article 

    Google Scholar 

  • Timmermans KR, Stolte W, de Baar HJW. Iron-mediated effects on nitrate reductase in marine phytoplankton. Mar Biol. 1994;121:389–96.

    CAS 
    Article 

    Google Scholar 

  • Jin X, Gruber N, Dune JP, Sarmiento JL, Armstrong RA. Diagnosing the contributions of phytoplankton functional groups to the production and export of particulate organic carbon, CaCO3, and opal from global nutrient and alkalinity distributions. Global Biogeochem Cycles. 2006;20:1–17.

    Article 
    CAS 

    Google Scholar 

  • McNair HM, Brzezinski MA, Till CP, Krause JW. Taxon-specific contributions to silica production in natural diatom assemblages. Limnol Oceanogr. 2018;63:1056–75.

    CAS 
    PubMed 
    Article 

    Google Scholar 

  • Lampe RH, Cohen NR, Ellis KA, Bruland KW, Maldonado MT, Peterson TD, et al. Divergent gene expression among phytoplankton taxa in response to upwelling. Environ Microbiol. 2018;20:3069–82.

    CAS 
    PubMed 
    Article 

    Google Scholar 

  • Lampe RH, Mann EL, Cohen NR, Till CP, Thamatrakoln K, Brzezinski MA, et al. Different iron storage strategies among bloom-forming diatoms. Proc Natl Acad Sci. 2018;115:E12275–84.

    CAS 
    PubMed 
    PubMed Central 
    Article 

    Google Scholar 

  • Brembu T, Chauton MS, Winge P, Bones AM, Vadstein O. Dynamic responses to silicon in Thalasiossira pseudonana—identification, characterisation and classification of signature genes and their corresponding protein motifs. Sci Rep. 2017;7:4865.

    PubMed 
    PubMed Central 
    Article 
    CAS 

    Google Scholar 

  • Kotzsch A, Gröger P, Pawolski D, Bomans PHH, Sommerdijk NAJM, Schlierf M, et al. Silicanin-1 is a conserved diatom membrane protein involved in silica biomineralization. BMC Biol. 2017;15:9–11.

  • Fawcett SE, Ward BB. Phytoplankton succession and nitrogen utilization during the development of an upwelling bloom. Mar Ecol Prog Ser. 2011;428:13–31.

    CAS 
    Article 

    Google Scholar 

  • Lampe RH, Hernandez G, Lin YY, Marchetti A. Representative diatom and coccolithophore species exhibit divergent responses throughout simulated upwelling cycles. mSystems. 2021;6:e00188–21.

  • Bruland KW, Rue EL, Smith GJ. Iron and macronutrients in California coastal upwelling regimes: Implications for diatom blooms. Limnol Oceanogr. 2001;46:1661–74.

    CAS 
    Article 

    Google Scholar 

  • Redfield AC, Ketchum BH, Richards FA. The influence of organisms on the composition of seawater. The Sea. 1963;2:26–77.

  • White KK, Dugdale RC. Silicate and nitrate uptake in the Monterey Bay upwelling system. Cont Shelf Res. 1997;17:455–72.

    Article 

    Google Scholar 

  • Chappell PD, Whitney LP, Wallace JR, Darer AI, Jean-Charles S, Jenkins BD. Genetic indicators of iron limitation in wild populations of Thalassiosira oceanica from the northeast Pacific Ocean. ISME J. 2015;9:592–602.

    CAS 
    PubMed 
    Article 

    Google Scholar 

  • Marchetti A, Moreno CM, Cohen NR, Oleinikov I, deLong K, Twining BS, et al. Development of a molecular-based index for assessing iron status in bloom-forming pennate diatoms. J Phycol. 2017;53:820–32.

    CAS 
    PubMed 
    Article 

    Google Scholar 

  • Thamatrakoln K, Korenovska O, Niheu AK, Bidle KD. Whole-genome expression analysis reveals a role for death-related genes in stress acclimation of the diatom Thalassiosira pseudonana. Environ Microbiol. 2012;14:67–81.

    CAS 
    PubMed 
    Article 

    Google Scholar 

  • Cohen NR, Ellis KA, Lampe RH, McNair HM, Twining BS, Maldonado MT, et al. Diatom transcriptional and physiological responses to changes in iron bioavailability across ocean provinces. Front Mar Sci. 2017;4:1–20.

    CAS 
    Article 

    Google Scholar 

  • La Roche J, Boyd PW, McKay RML, Geider RJ. Flavodoxin as an in situ marker for iron stress in phytoplankton. Nature. 1996;382:802–5.

    Article 

    Google Scholar 

  • Hervás M, Navarro JAJa, Diaz A, Bottin HH, De la Rosa MA, Díaz A, et al. Laser-flash kinetic analysis of the fast electron transfer from plastocyanin and cytochrome c6 to photosystem I. Experimental evidence on the evolution of the reaction mechanism. Biochemistry. 1995;34:11321–6.

    PubMed 
    Article 

    Google Scholar 

  • Franck VM, Bruland KW, Hutchins DA, Brzezinski MA. Iron and zinc effects on silicic acid and nitrate uptake kinetics in three high-nutrient, low-chlorophyll (HNLC) regions. Mar Ecol Prog Ser. 2003;252:15–33.

    CAS 
    Article 

    Google Scholar 

  • Brown KL, Twing KI, Robertson DL. Unraveling the regulation of nitrogen assimilation in the marine diatom Thalassiosira pseudonana (bacillariophyceae): Diurnal variations in transcript levels for five genes involved in nitrogen assimilation. J Phycol. 2009;45:413–26.

    CAS 
    PubMed 
    Article 

    Google Scholar 

  • Allen AE, Dupont CL, Oborník M, Horák A, Nunes-Nesi A, McCrow JP, et al. Evolution and metabolic significance of the urea cycle in photosynthetic diatoms. Nature. 2011;473:203–7.

    CAS 
    PubMed 
    Article 

    Google Scholar 

  • Görlich S, Pawolski D, Zlotnikov I, Kröger N. Control of biosilica morphology and mechanical performance by the conserved diatom gene Silicanin-1. Commun Biol. 2019;2:245.

  • Durkin CA, Koester JA, Bender SJ, Armbrust VE. The evolution of silicon transporters in diatoms. J Phycol. 2016;52:716–31.

    CAS 
    PubMed 
    PubMed Central 
    Article 

    Google Scholar 

  • King AL, Barbeau KA. Dissolved iron and macronutrient distributions in the southern California Current System. J Geophys Res Ocean. 2011;116:1–18.

    Google Scholar 

  • Hoffmann LJ, Peeken I, Lochte K. Effects of iron on the elemental stoichiometry during EIFEX and in the diatoms Fragilariopsis kerguelensis and Chaetoceros dichaeta. Biogeosciences. 2007;4:569–79.

    CAS 
    Article 

    Google Scholar 

  • Matsumoto K, Sarmiento JL, Brzezinski MA. Silicic acid leakage from the Southern Ocean: a possible explanation for glacial atmospheric pCO2. Global Biogeochem Cycles. 2002;16:1–23.

  • Geider RJ, Greene RM, Kolber ZS, MacIntyre HL, Falkowski PG. Fluorescence assessment of the maximum quantum efficiency of photosynthesis in the western North. Atlantic. Deep Res Part I. 1993;40:1205–24.

    CAS 
    Article 

    Google Scholar 

  • Durkin CA, Bender SJ, Chan KYK, Gaessner K, Grünbaum D, Armbrust VE. Silicic acid supplied to coastal diatom communities influences cellular silicification and the potential export of carbon. Limnol Oceanogr. 2013;58:1707–26.

    CAS 
    Article 

    Google Scholar 

  • Kudo I, Miyamoto M, Noiri Y, Maita Y. Combined effects of temperature and iron on the growth and physiology of the marine diatom Phaeodactylum tricornutum (Bacillariophyceae). J Phycol. 2000;36:1096–102.

    CAS 
    Article 

    Google Scholar 

  • Eldridge ML, Trick CG, Alm MB, DiTullio GR, Rue EL, Bruland KW, et al. Phytoplankton community response to a manipulation of bioavailable iron in HNLC waters of the subtropical Pacific Ocean. Aquat Microb Ecol. 2004;35:79–91.

    Article 

    Google Scholar 

  • Sunda WG, Huntsman SA. Iron uptake and growth limitation in oceanic and coastal phytoplankton. Mar Chem. 1995;50:189–206.

    CAS 
    Article 

    Google Scholar 

  • Morel FMM, Rueter JG, Price NM. Iron nutrition of phytoplankton and its possible importance in the ecology of ocean regions with high nutrient and low biomass. Oceanography. 1991;4:56–61.

    Article 

    Google Scholar 

  • Coale TH, Moosburner M, Horák A, Oborník M, Barbeau KA, Allen AE. Reduction-dependent siderophore assimilation in a model pennate diatom. Proc Natl Acad Sci USA. 2019;116:23609–17.

    CAS 
    PubMed 
    PubMed Central 
    Article 

    Google Scholar 

  • De La Rocha CL, Hutchins DA, Brzezinski MA, Zhang Y. Effects of iron and zinc deficiency on elemental composition and silica production by diatoms. Mar Ecol Prog Ser. 2000;195:71–9.

    Article 

    Google Scholar 

  • Claquin P, Martin-Jézéquel V, Kromkamp JC, Veldhuis MJW, Kraay GW. Uncoupling of silicon compared with carbon and nitrogen metabolisms and the role of the cell cycle in continuous cultures of Thalassiosira pseudonana (Bacillariophyceae) under light, nitrogen, and phosphorus control. J Phycol. 2002;38:922–30.

    CAS 
    Article 

    Google Scholar 

  • Wang WX, Dei RCH. Biological uptake and assimilation of iron by marine plankton: influences of macronutrients. Mar Chem. 2001;74:213–26.

    CAS 
    Article 

    Google Scholar 

  • Sapriel G, Quinet M, Heijde M, Jourdren L, Tanty V, Luo G, et al. Genome-wide transcriptome analyses of silicon metabolism in Phaeodactylum tricornutum reveal the multilevel regulation of silicic acid transporters. PLoS ONE. 2009;4:e7458–14.

  • Kröger N, Deutzmann R, Sumper M. Polycationic peptides from diatom biosilica that direct silica nanosphere formation. Science. 1999;286:1129–32.

    PubMed 
    Article 

    Google Scholar 

  • Scheffel A, Poulsen N, Shian S, Kröger N. Nanopatterned protein microrings from a diatom that direct silica morphogenesis. Proc Natl Acad Sci USA. 2011;108:3175–80.

    CAS 
    PubMed 
    PubMed Central 
    Article 

    Google Scholar 

  • Knight MJ, Senior L, Nancolas B, Ratcliffe S, Curnow P. Direct evidence of the molecular basis for biological silicon transport. Nat Commun. 2016;7:1–11.

    Article 
    CAS 

    Google Scholar 

  • Shrestha RP, Hildebrand M. Evidence for a regulatory role of diatom silicon transporters in cellular silicon responses. Eukaryot Cell. 2015;14:29.

    PubMed 
    Article 
    CAS 

    Google Scholar 

  • Thamatrakoln K, Hildebrand M. Silicon uptake in diatoms revisited: A model for saturable and nonsaturable uptake kinetics and the role of silicon transporters. Plant Physiol. 2008;146:1397–407.

    CAS 
    PubMed 
    PubMed Central 
    Article 

    Google Scholar 

  • Conway HL, Harrison PJ. Marine diatoms grown in chemostats under silicate or ammonium limitation. IV. Transient response of Chaetoceros debilis, Skeletonema costatum, and Thalassiosira gravida to a single addition of the limiting nutrient. Mar Biol. 1977;43:33–43.

    CAS 
    Article 

    Google Scholar 

  • Thamatrakoln K, Hildebrand M. Analysis of Thalassiosira pseudonana silicon transporters indicates distinct regulatory levels and transport activity through the cell cycle. Eukaryot Cell. 2007;6:271–9.

    CAS 
    PubMed 
    Article 

    Google Scholar 

  • Ashworth J, Coesel SN, Lee A, Armbrust VE, Orellana MV, Baliga NS. Genome-wide diel growth state transitions in the diatom Thalassiosira pseudonana. Proc Natl Acad Sci USA. 2013;110:7518–23.

    CAS 
    PubMed 
    PubMed Central 
    Article 

    Google Scholar 

  • Chauton MS, Winge P, Brembu T, Vadstein O, Bones AM. Gene regulation of carbon fixation, storage, and utilization in the diatom Phaeodactylum tricornutum acclimated to light/dark cycles. Plant Physiol. 2013;161:1034–48.

    CAS 
    PubMed 
    Article 

    Google Scholar 

  • Chisholm SW, Costello JC. Influence of environmental factors and population composition on the timing of cell division in Thalassiosira fluviatilis (Bacillariophyceae) grown on light/dark cycles. J Phycol. 1980;16:375–83.

    Article 

    Google Scholar 

  • Smith SR, Glé C, Abbriano RM, Traller JC, Davis AK, Trentacoste E, et al. Transcript level coordination of carbon pathways during silicon starvation-induced lipid accumulation in the diatom Thalassiosira pseudonana. New Phytol. 2016;210:890–904.

    CAS 
    PubMed 
    PubMed Central 
    Article 

    Google Scholar 

  • Vaulot D, Olson RJ, Chisholm SW. Light and dark control of the cell cycle in two marine phytoplankton species. Exp Cell Res. 1986;167:38–52.

    CAS 
    PubMed 
    Article 

    Google Scholar 

  • Marchetti A, Parker MS, Moccia LP, Lin EO, Arrieta AL, Ribalet FF, et al. Ferritin is used for iron storage in bloom-forming marine pennate diatoms. Nature. 2009;457:467–70.

    CAS 
    PubMed 
    Article 

    Google Scholar 

  • Goldman JAL, Schatz MJ, Berthiaume CT, Coesel SN, Orellana MV, Armbrust VE. Fe limitation decreases transcriptional regulation over the diel cycle in the model diatom Thalassiosira pseudonana. PLoS ONE. 2019;14:1–25.

    Article 
    CAS 

    Google Scholar 

  • Assmy P, Smetacek V, Montresor M, Klaas C, Henjes J, Strass VH, et al. Thick-shelled, grazer-protected diatoms decouple ocean carbon and silicon cycles in the iron-limited Antarctic Circumpolar Current. Proc Natl Acad Sci USA. 2013;110:20633–8.

    CAS 
    PubMed 
    PubMed Central 
    Article 

    Google Scholar 

  • Kranzler CF, Brzezinski MA, Cohen NR, Lampe RH, Maniscalco M, Till CP, et al. Impaired viral infection and reduced mortality of diatoms in iron-limited oceanic regions. Nat Geosci. 2021;14:231–7.

    CAS 
    Article 

    Google Scholar 

  • Hutchins DA, Franck VM, Brzezinski MA, Bruland KW. Inducing phytoplankton iron limitation in iron-replete coastal waters with a strong chelating ligand. Limnol Oceanogr. 1999;44:1009–18.

    CAS 
    Article 

    Google Scholar 

  • Robertson G, Schein J, Chiu R, Corbett R, Field M, Jackman SD, et al. De novo assembly and analysis of RNA-seq data. Nat Methods. 2010;7:909–12.

    CAS 
    PubMed 
    Article 

    Google Scholar 

  • Kanehisa M, Furumichi M, Tanabe M, Sato Y, Morishima K. KEGG: new perspectives on genomes, pathways, diseases and drugs. Nucleic Acids Res. 2017;45:D353–61.

    CAS 
    PubMed 
    Article 

    Google Scholar 

  • Smith SR, Dupont CL, McCarthy JK, Broddrick JT, Oborník M, Horák A, et al. Evolution and regulation of nitrogen flux through compartmentalized metabolic networks in a marine diatom. Nat Commun. 2019;10:4552.

    PubMed 
    PubMed Central 
    Article 
    CAS 

    Google Scholar 

  • Morrissey J, Sutak R, Paz-Yepes J, Tanaka A, Moustafa A, Veluchamy A, et al. A novel protein, ubiquitous in marine phytoplankton, concentrates iron at the cell surface and facilitates uptake. Curr Biol. 2015;25:364–71.

    CAS 
    PubMed 
    Article 

    Google Scholar 

  • Matsen FA, Kodner RB, Armbrust VE. pplacer: linear time maximum-likelihood and Bayesian phylogenetic placement of sequences onto a fixed reference tree. BMC Bioinform. 2010;11:538.

    Article 

    Google Scholar 

  • Robinson MD, McCarthy DJ, Smyth GK. edgeR: a Bioconductor package for differential expression analysis of digital gene expression data. Bioinformatics. 2010;26:139–40.

    CAS 
    PubMed 
    Article 

    Google Scholar 

  • Benjamini Y, Hochberg Y. Controlling the false discovery rate: a practical and powerful approach to multiple testing. J R Stat Soc Ser B Methodol. 1995;57:289–300.


  • Source: Ecology - nature.com

    Insights into amino acid fractionation and incorporation by compound-specific carbon isotope analysis of three-spined sticklebacks

    Periodically taken photographs reveal the effect of pollinator insects on seed set in lotus flowers