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Nutrients and Their Acquisition: Phosphorus Physiology in Microalgae

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The Physiology of Microalgae

Part of the book series: Developments in Applied Phycology ((DAPH,volume 6))

Abstract

The macronutrient phosphorus is critical to the physiological ecology of eukaryotic microalgae and cyanobacteria. What are the forms of phosphorus produced and used by these groups? This chapter reviews the distribution and processing of phosphorus in eukaryotic microalgae and cyanobacteria with a focus on how new so-called “omics” methods, advances in chemical analyses, and cell-specific approaches have driven new discoveries.

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Notes

  1. 1.

    Wherever possible the currently accepted names for species are used. The name used in the paper cited is also indicated. For details of names see chapter “Systematics, Taxonomy and Species Names: Do They Matter?” of this book (Borowitzka 2016).

References

  • Adams MM, Gomez-Garcia MR, Grossman AR, Bhaya D (2008) Phosphorus deprivation responses and phosphonate utilization in a thermophilic Synechococcus sp. from microbial mats. J Bacteriol 190:8171–8184

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Ammerman J, Azam F (1985) Bacterial 5′ nucleotidase in aquatic ecosystems: a novel mechanism of phosphorus regeneration. Science 227:1338–1340

    Article  CAS  PubMed  Google Scholar 

  • Ammerman JW, Azam F (1991) Bacterial 5′-nucleotidase activity in estuarine and coastal marine waters – role in phosphorus regeneration. Limnol Oceanogr 36:1437–1447

    Article  CAS  Google Scholar 

  • Anderson DM, Glibert PM, Burkholder JM (2002) Harmful algal blooms and eutrophication: nutrient sources, composition and consequences. Estuaries 25:704–726

    Article  Google Scholar 

  • Armbrust EV, Berges JA, Bowler C, Green BR, Martinez D, Putnam NH, Zhou SG, Allen AE, Apt KE, Bechner M, Brzezinski MA, Chaal BK, Chiovitti A, Davis AK, Demarest MS, Detter JC, Glavina T, Goodstein D, Hadi MZ, Hellsten U, Hildebrand M, Jenkins BD, Jurka J, Kapitonov VV, Kroger N, Lau WWY, Lane TW, Larimer FW, Lippmeier JC, Lucas S, Medina M, Montsant A, Obornik M, Parker MS, Palenik B, Pazour GJ, Richardson PM, Rynearson TA, Saito MA, Schwartz DC, Thamatrakoln K, Valentin K, Vardi A, Wilkerson FP, Rokhsar DS (2004) The genome of the diatom Thalassiosira pseudonana: ecology, evolution, and metabolism. Science 306:79–86

    Article  CAS  PubMed  Google Scholar 

  • Azam F, Malfatti F (2007) Microbial structuring of marine ecosystems. Nat Rev Microbiol 5:782–791

    Article  CAS  PubMed  Google Scholar 

  • Bar-Yosef Y, Sukenik A, Hadas O, Viner-Mozzinim Y, Kaplan A (2010) Enslavement in the water body by toxic Aphanizomenon ovalisporum, inducing alkaline phosphatase in phytoplanktons. Curr Biol 20(17):1557–1561

    Google Scholar 

  • Beardall J, Young E, Roberts S (2001) Approaches for determining phytoplankton nutrient limitation. Aquat Sci 63:44–69

    Article  CAS  Google Scholar 

  • Bench SR, Heller P, Frank I, Arciniega M, Shilova IN, Zehr JP (2013) Whole genome comparison of six Crocosphaera watsonii strains with differing phenotypes. J Phycol 49:786–801

    Article  Google Scholar 

  • Benitez-Nelson CR (2000) The biogeochemical cycling of phosphorus in marine systems. Earth Sci Rev 51:109–135

    Article  CAS  Google Scholar 

  • Bertilsson S, Berglund O, Karl D, Chisholm SW (2003) Elemental composition of marine Prochlorococcus and Synechococcus: implications for the ecological stoichiometry of the sea. Limnol Oceanogr 48:1721–1731

    Article  CAS  Google Scholar 

  • Beszteri S, Yang I, Jaeckisch N, Tillmann U, Frickenhaus S, Glockner G, Cembella A, John U (2012) Transcriptomic response of the toxic prymnesiophyte Prymnesium parvum (N. Carter) to phosphorus and nitrogen starvation. Harmful Algae 18:1–15

    Article  CAS  Google Scholar 

  • Beversdorf LJ, White AE, Björkman KM, Letelier RM, Karl DM (2010) Phosphonate metabolism of Trichodesmium IMS101 and the production of greenhouse gases. Limnol Oceanogr 55:1768–1778

    Article  CAS  Google Scholar 

  • Björkman K, Karl DM (1994) Bioavailability of inorganic and organic phosphorus-compounds to natural assemblages of microorganisms in Hawaiian coastal waters. Mar Ecol Prog Ser 111:265–273

    Article  Google Scholar 

  • Björkman KM, Karl DM (2001) A novel method for the measurement of dissolved adenosine and guanosine triphosphate in aquatic habitats: applications to marine microbial ecology. J Microbiol Meth 47:159–167

    Article  Google Scholar 

  • Björkman K, Duhamel S, Karl DM (2012) Microbial group specific uptake kinetics of inorganic phosphate and adenosine-5′-triphosphate (ATP) in the north pacific subtropical gyre. Front Microbiol 3:189. doi:10.3389/fmicb.2012.00189

    PubMed  PubMed Central  Google Scholar 

  • Blake RE, O’Neil JR, Surkov AV (2005) Biogeochemical cycling of phosphorus: insights from oxygen isotope effects of phosphoenzymes. Am J Sci 305:596–620

    Article  CAS  Google Scholar 

  • Bolier G, de Koningh CJ, Schmale JC, Donze M (1992) Differential luxury phosphate response of planktonic algae to phosphorus removal. Hydrobiologia 243/244:113–118

    Article  Google Scholar 

  • Borowitzka MA (2016) Systematics, taxonomy and species names: do they matter? In: Borowitzka MA, Beardall J, Raven JA (eds) The physiology of microalgae. Springer, Dordrecht, pp 655–681

    Google Scholar 

  • Cade-Menun BJ, Paytan A (2010) Nutrient temperature and light stress alter phosphorus and carbon forms in culture-grown algae. Mar Chem 121:27–36

    Article  CAS  Google Scholar 

  • Cade-Menun BJ, Benitez-Nelson CR, Pellechia P, Paytan A (2005) Refining 31P nuclear magnetic resonance spectroscopy for marine particulate samples: storage conditions and extraction recovery. Mar Chem 97:293–306

    Article  CAS  Google Scholar 

  • Capone DG, Zehr JP, Paerl HW, Bergman B, Carpenter E (1997) Trichodesmium, a globally significant marine cyanobacterium. Science 276:1221–1229

    Article  CAS  Google Scholar 

  • Casey JR, Lomas MW, Michelou VK, Dyhrman ST, Orchard ED, Ammerman JW, Sylvan JB (2009) Phytoplankton taxon-specific orthophosphate (Pi) and ATP utilization in the western subtropical North Atlantic. Aquat Microb Ecol 58:31–44

    Article  Google Scholar 

  • Cembella AD, Antia NJ, Harrison PJ (1984a) The utilization of inorganic and organic phosphorus compounds as nutrients by eukaryotic microalgae: a multidisciplinary perspective: Part I. CRC Crit Rev Microbiol 10:317–391

    Article  CAS  Google Scholar 

  • Cembella AD, Antia NJ, Harrison PJ (1984b) The utilization of inorganic and organic phosphorus compounds as nutrients by eukaryotic microalgae: a multidisciplinary perspective: Part II. CRC Crit Rev Microbiol 11:13–81

    Article  CAS  Google Scholar 

  • Chisholm SW, Stross RG (1976) Phosphate uptake kinetics in Euglena gracilis (Euglenophyceae) grown on light/dark cycles. I. Synchronized batch cultures. J Phycol 12:210–217

    CAS  Google Scholar 

  • Chung CC, Hwang SPL, Chang J (2003) Identification of a high-affinity phosphate transporter gene in a prasinophyte alga, Tetraselmis chui, and its expression under nutrient limitation. Appl Environ Microbiol 69:754–759

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Clark LL, Ingall ED, Benner R (1998) Marine phosphorus is selectively remineralized. Nature 393:426

    Article  CAS  Google Scholar 

  • Clark LL, Ingall ED, Benner R (1999) Marine organic phosphorus cycling: novel insights from nuclear magnetic resonance. Am J Sci 299:724–737

    Article  CAS  Google Scholar 

  • Coleman ML, Chisholm SW (2010) Ecosystem-specific selection pressures revealed through comparative population genomics. Proc Natl Acad Sci U S A 107:18634–18639

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Colman AS, Blake RE, Karl DM, Fogel ML, Turekian KK (2005) Marine phosphate oxygen isotopes and organic matter remineralization in the oceans. Proc Natl Acad Sci U S A 102:13023–13028

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Costas AMG, White AK, Metcalf WW (2001) Purification and characterization of a novel phosphorus-oxidizing enzyme from Pseudomonas stutzeri WM88. J Biol Chem 276:17429–17436

    Article  CAS  PubMed  Google Scholar 

  • Cox AD, Saito MA (2013) Proteomic responses of oceanic Synechococcus WH8102 to phosphate and zinc scarcity and cadmium additions. Front Microbiol 4:387. doi:10.3389/fmicb.2013.00387

    PubMed  PubMed Central  Google Scholar 

  • Crocetti GR, Hugenholtz P, Bond PL, Schuler A, Keller J, Jenkins D, Blackall LL (2000) Identification of polyphosphate-accumulating organisms and design of 16S rRNA-directed probes for their detection and quantification. Appl Environ Microbiol 66:1175–1182

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Cuvelier ML, Allen AE, Monier A, McCrow JP, Messie M, Tringe SG, Woyke T, Welsh RM, Ishoey T, Lee JH, Binder BJ, DuPont CL, Latasa M, Guigand C, Buck KR, Hilton J, Thiagarajan M, Caler E, Read B, Lasken RS, Chavez FP, Worden AZ (2010) Targeted metagenomics and ecology of globally important uncultured eukaryotic phytoplankton. Proc Natl Acad Sci U S A 107:14679–14684

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Diaz JM, Ingall ED (2010) Fluorometric quantification of natural inorganic polyphosphate. Environ Sci Tech 44:4665–4671

    Article  CAS  Google Scholar 

  • Diaz J, Ingall E, Benitez-Nelson C, Paterson D, de Jonge MD, McNulty I, Brandes JA (2008) Marine polyphosphate: a key player in geologic phosphorus sequestration. Science 320:652–655

    Article  CAS  PubMed  Google Scholar 

  • Diaz JM, Björkman KM, Haley ST, Ingall ED, Karl DM, Longo AF, Dyhrman ST (2015) Polyphosphate dynamics at Station ALOHA, North Pacific subtropical gyre. Limnol. Oceanogr. doi:10.1002/lno.10206

    Google Scholar 

  • Dignum M, Hoogveld HL, Matthijs HCP, Laanbroek HJ, Pel R (2004) Detecting the phosphate status of phytoplankton by enzyme-labeled fluorescence and flow cytometry. FEMS Microbiol Ecol 48:29–38

    Article  CAS  PubMed  Google Scholar 

  • Donald KM, Scanlan DJ, Carr NG, Mann NH, Joint I (1997) Comparative phosphorus nutrition of the marine cyanobacterium Synechococcus WH7803 and the marine diatom Thalassiosira weisflogii. J Plankton Res 19:1793–1813

    Article  CAS  Google Scholar 

  • Droop MR (1973) Some thoughts on nutrient limitation in algae. J Phycol 9:264–272

    CAS  Google Scholar 

  • Duhamel S, Dyhrman ST, Karl DM (2010) Alkaline phosphatase activity and regulation in the north pacific subtropical gyre. Limnol Oceanogr 55:1414–1425

    Article  CAS  Google Scholar 

  • Duhamel S, Björkman KM, Karl DM (2012) Light dependence of phosphorus uptake by microorganisms in the subtropical North and South Pacific ocean. Aquat Microb Ecol 67:225–238

    Article  Google Scholar 

  • Dyhrman ST (2005) Ectoenzymes in Prorocentrum minimum. Harmful Algae 4:619–627

    Article  CAS  Google Scholar 

  • Dyhrman ST (2008) Molecular approaches to diagnosing nutritional physiology in harmful algae: implications for studying the effects of eutrophication. Harmful Algae 8:167–174

    Article  CAS  Google Scholar 

  • Dyhrman ST, Haley ST (2006) Phosphorus scavenging in the unicellular marine diazotroph Crocosphaera watsonii. Appl Environ Microbiol 72:1452–1458

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Dyhrman ST, Palenik BP (1997) The identification and purification of a cell-surface alkaline phosphatase from the dinoflagellate Prorocentrum minimum (Dinophyceae). J Phycol 33:602–612

    Article  CAS  Google Scholar 

  • Dyhrman ST, Palenik BP (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

    CAS  PubMed  PubMed Central  Google Scholar 

  • Dyhrman ST, Palenik BP (2001) A single-cell immunoassay for phosphate stress in the dinoflagellate Prorocentrum minimum (Dinophyceae). J Phycol 37:400–410

    Article  CAS  Google Scholar 

  • Dyhrman ST, Palenik BP (2003) Characterization of ectoenzyme activity and phosphate-regulated proteins in the coccolithophorid Emiliania huxleyi. J Plankton Res 25:1215–1225

    Article  CAS  Google Scholar 

  • Dyhrman ST, Ruttenberg KC (2006) Presence and regulation of alkaline phosphatase activity in eukaryotic phytoplankton from the coastal ocean: implications for dissolved organic phosphorus remineralization. Limnol Oceanogr 51:1381–1390

    Article  CAS  Google Scholar 

  • Dyhrman ST, Webb E, Anderson DM, Moffett J, Waterbury J (2002) Cell-specific detection of phosphorus stress in Trichodesmium from the western North Atlantic. Limnol Oceanogr 47:1823–1836

    Article  Google Scholar 

  • Dyhrman ST, Chappell PD, Haley ST, Moffett JW, Orchard ED, Waterbury JB, Webb EA (2006a) Phosphonate utilization by the globally important marine diazotroph Trichodesmium. Nature 439:68–71

    Article  CAS  PubMed  Google Scholar 

  • Dyhrman ST, Haley ST, Birkeland SR, Wurch LL, Cipriano MJ, McArthur AG (2006b) 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

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Dyhrman ST, Ammerman JW, Van Mooy BAS (2007) Microbes and the marine phosphorus cycle. Oceanography 20:110–116

    Article  Google Scholar 

  • Dyhrman ST, Benitez-Nelson CR, Orchard ED, Haley ST, Pellechia PJ (2009) A microbial source of phosphonates in oligotrophic marine systems. Nat Geosci 2:696–699

    Article  CAS  Google Scholar 

  • Dyhrman ST, Jenkins BD, Rynearson TA, Saito MA, Mercier ML, Alexander H, Whitney LP, Drzewianowski A, Bulygin VV, Bertrand EM, Wu ZJ, Benitez-Nelson C, Heithoff A (2012) The transcriptome and proteome of the diatom Thalassiosira pseudonana reveal a diverse phosphorus stress response. PLoS One 7:e33768. doi:10.1371/journal.pone.0033768

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Eixler S, Karsten U, Selig U (2006) Phosphorus storage in Chlorella vulgaris (Trebouxiophyceae, Chlorophyta) cell and its dependence on phosphate supply. Phycologia 45:53–60

    Article  Google Scholar 

  • Erdner DL, Anderson DM (2006) Global transcriptional profiling of the toxic dinoflagellate Alexandrium fundyense using massively parallel signature sequencing. BMC Genomics 7:88. doi:10.1186/1471-2164-7-88

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  • Feingersch R, Philosof A, Mejuch T, Glaser F, Alalouf O, Shoham Y, Beja O (2012) Potential for phosphite and phosphonate utilization by Prochlorococcus. ISME J 6:827–834

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Flynn KJ, Oepik H, Syrett PJ (1986) Localization of the alkaline phosphatase and 5′-nucleotidase activities of the diatom Phaeodactylum tricornutum. J Gen Microbiol 132:289–298

    CAS  Google Scholar 

  • Flynn KJ, Raven JA, Rees TA, Finkel Z, Quigg A, Beardall J (2010) Is the growth rate hypothesis applicable to microalgae? J Phycol 46:1–12

    Article  CAS  Google Scholar 

  • Frischkorn K, Harke K, Gobler CJ, Dyhrman ST (2014) De novo assembly of Aureococcus anophagefferens transcriptomes reveals diverse responses to the low nutrient and low light conditions present during blooms. Front Microbiol 5:375. doi:10.3389/fmicb.2014.00375

    PubMed  PubMed Central  Google Scholar 

  • Fu FX, Zhang YH, Bell PRF, Hutchins DA (2005) Phosphate uptake and growth kinetics of Trichodesmium (cyanobacteria) isolates from the North Atlantic ocean and the great barrier reef, Australia. J Phycol 41:62–73

    Article  CAS  Google Scholar 

  • Fulton JM, Fredricks HF, Bidle KD, Vardi A, Kendrick BJ, DiTullio GR, Van Mooy BAS (2014) Novel molecular determinants of viral susceptibility and resistance in the lipidome of Emiliania huxleyi. Environ Microbiol 16:1137–1149

    Article  CAS  PubMed  Google Scholar 

  • Fuszard MA, Wright PC, Biggs CA (2010) Cellular acclimation strategies of a minimal picocyanobacterium to phosphate stress. FEMS Microbiol Lett 306:127–134

    Article  CAS  PubMed  Google Scholar 

  • Gifford SM, Sharma S, Rinta-Kanto JM, Moran MA (2011) Quantitative analysis of a deeply sequenced marine microbial metatranscriptome. ISME J 5:461–472

    Article  PubMed  PubMed Central  Google Scholar 

  • Gilbert JA, Laverock B, Temperton B, Thomas S, Muhling M, Hughes M (2011) Metagenomics. In: Kwon YM (ed) High-throughput next generation sequencing: methods and application, 1st edn. Springer, New York, pp 173–183

    Chapter  Google Scholar 

  • Girault M, Arakawa H, Hashihama F (2013) Phosphorus stress of microphytoplankton community in the western subtropical North Pacific. J Plankton Res 35:146–157

    Article  CAS  Google Scholar 

  • Gobler CJ, Berry DL, Dyhrman ST, Wilhelm SW et al (2011) Niche of harmful alga Aureococcus anophagefferens revealed through ecogenomics. Proc Natl Acad Sci U S A 108:4352–4357

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Gomez-Garcia MR, Losada M, Serrano A (2003) Concurrent transcriptional activation of ppA and ppX genes by phosphate deprivation in the cyanobacterium Synechocystis sp. strain PCC 6803. Biochem Biophys Res Commun 302:601–609

    Article  CAS  PubMed  Google Scholar 

  • Gomez-Garcia MR, Davison M, Blain-Hartnung M, Grossman AR, Bhaya D (2011) Alternative pathways for phosphonate metabolism in thermophilic cyanobacteria from microbial mats. ISME J 5:141–149

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • González-Gil S, Keafer B, Jovine RVM, Anderson DM (1998) Detection and quantification of alkaline phosphatase in single cells of phosphorus-limited marine phytoplankton. Mar Ecol Prog Ser 164:21–35

    Article  Google Scholar 

  • Grossman A (2000) Acclimation of Chlamydomonas reinhardtii to its nutrient environment. Protist 151:201–224

    Article  CAS  PubMed  Google Scholar 

  • Grossman A, Takahashi H (2001) Macronutrient utilization by photosynthetic eukaryotes and the fabric of interactions. Annu Rev Plant Physiol Plant Mol Biol 52:163–210

    Article  CAS  PubMed  Google Scholar 

  • Harke MJ, Gobler CJ (2013) Global transcriptional responses of the toxic cyanobacterium, Microcystis aeruginosa, to nitrogen stress, phosphorus stress, and growth on organic matter. PLoS One 8:e69834. doi:10.1371/journal.pone.0069834

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Harke MJ, Berry DL, Ammerman JW, Gobler CJ (2012) Molecular response of the bloom-forming cyanobacterium, Microcystis aeruginosa, to phosphorus limitation. Microb Ecol 63:188–198

    Article  CAS  PubMed  Google Scholar 

  • Hidaka T, Imai S, Hara O, Anzai H, Murakami T, Nagaoka K, Seto H (1990) Carboxyphosphonoenolpyruvate phosphonomutase, a novel enzyme catalyzing C-P bond formation. J Bacteriol 172:3066–3072

    CAS  PubMed  PubMed Central  Google Scholar 

  • Hothorn M, Neumann H, Lenherr ED, Wehner M, Rybin V, Hassa PO, Uttenweiler A, Reinhardt M, Schmidt A, Seiler J, Ladurner AG, Herrmann C, Scheffzek K, Mayer A (2009) Catalytic core of a membrane-associated eukaryotic polyphosphate polymerase. Science 324:513–516

    Article  CAS  PubMed  Google Scholar 

  • Hynes AM, Chappell PD, Dyhrman ST, Doney SC, Webb EA (2009) Cross-basin comparison of phosphorus stress and nitrogen fixation in Trichodesmium. Limnol Oceanogr 54:1438–1448

    Article  CAS  Google Scholar 

  • Ito T, Tanaka M, Shinkawa H, Nakada T, Ano Y, Kurano N, Soga T, Tomita M (2013) Metabolic and morphological changes of an oil accumulating trebouxiophycean alga in nitrogen-deficient conditions. Metabolomics 9:S178–S187

    Article  CAS  Google Scholar 

  • Jacobson L, Halmann M (1982) Polyphosphate metabolism in the blue-green alga Microcystis aeruginosa. J Plankton Res 4:481–488

    Article  CAS  Google Scholar 

  • Jakuba RW, Moffett JW, Dyhrman ST (2008) Evidence for the linked biogeochemical cycling of zinc, cobalt, and phosphorus in the western North Atlantic ocean. Global Biogeochem Cycles 22:GB4012. doi:10.1029/2007GB003119

    Article  CAS  Google Scholar 

  • Jansson M (1988) Phosphate-uptake and utilization by bacteria and algae. Hydrobiologia 170:177–189

    Article  CAS  Google Scholar 

  • Jansson M, Olsson L, Pettersson K (1988) Phosphatases: origin, characteristics and function in lakes. Hydrobiologia 170:157–175

    Article  CAS  Google Scholar 

  • Karl DM (2014) Microbially mediated transformations of phosphorus in the sea: new views of an old cycle. Annu Rev Mar Sci 6:279–337

    Article  Google Scholar 

  • Karl D, Björkman KM (2001) Phosphorus cycle in seawater: dissolved and particulate pool inventories and selected phosphorus fluxes. In: Paul JH (ed) Marine microbiology. Academic, San Diego, pp 249–366

    Google Scholar 

  • Karl DM, Björkman KM (2002) Dynamics of DOP. In: Hansell D, Carlson C (eds) Biogeochemistry of marine dissolved organic matter. Elsevier Science, Boston, pp 249–366

    Chapter  Google Scholar 

  • Kashtan N, Roggensack SE, Rodrigue S, Thompson JW, Biller SJ, Coe A, Ding H, Marttinen P, Malmstron R, Stocker R, Follows MJ, Stepanauskas R, Chisholm SW (2014) Single-cell genomics reveals hundreds of coexisting subpopulations in wild Prochlorococcus. Science 344:416–420

    Article  CAS  PubMed  Google Scholar 

  • Kathuria S, Martiny AC (2011) Prevalence of a calcium-based alkaline phosphatase associated with the marine cyanobacterium Prochlorococcus and other ocean bacteria. Environ Microbiol 13:74–83

    Article  CAS  PubMed  Google Scholar 

  • Kittredge JS, Roberts EA (1969) A carbon-phosphorus bond in nature. Science 164:37–42

    Article  CAS  PubMed  Google Scholar 

  • Kittredge JS, Horiguchi M, Williams PM (1969) Aminophosphonic acids: biosynthesis by marine phytoplankton. Comp Biochem Physiol 29:859–863

    Article  CAS  PubMed  Google Scholar 

  • Komeili A, O’shea EK (1999) Roles of phosphorylation sites in regulating activity of the transcription factor pho4. Science 284:977–980

    Article  CAS  PubMed  Google Scholar 

  • Kornberg A (1995) Inorganic polyphosphate: toward making a forgotten polymer unforgettable. J Bacteriol 177:491–496

    CAS  PubMed  PubMed Central  Google Scholar 

  • Kornberg A, Rao N, Ault-Riche D (1999) Inorganic polyphosphate: a molecule of many functions. Ann Rev Biochem 68:89–125

    Article  CAS  PubMed  Google Scholar 

  • Krauk JM, Villareal TA, Sohm JA, Montoya JP, Capone DG (2006) Plasticity of N: P ratios in laboratory and field populations of Trichodesmium spp. Aquat Microb Ecol 42:243–253

    Article  Google Scholar 

  • Krumhardt KM, Callnan K, Roache-Johnson K, Swett T, Robinson D, Reistetter EN, Saunders JK, Rocap G, Moore LR (2013) Effects of phosphorus starvation versus limitation on the marine cyanobacterium Prochlorococcus MED4 I: uptake physiology. Environ Microbiol 15:2114–2128

    Article  CAS  PubMed  Google Scholar 

  • Kudela RM, Cochlan WP (2000) Nitrogen and carbon uptake kinetics and the influence of irradiance for a red tide bloom off southern California. Aquat Microb Ecol 21:31–47

    Article  Google Scholar 

  • Kujawinski EB (2011) The impact of microbial metabolism on marine dissolved organic matter. Ann Rev Mar Sci 3:567–599

    Article  PubMed  Google Scholar 

  • Kujawinski EB, Longnecker K, Blough NV, Del Vecchio R, Finlay L, Kitner JB, Giovannoni SJ (2009) Identification of possible source markers in marine dissolved organic matter using ultrahigh resolution mass spectrometry. Geochim Cosmochim Acta 73:4384–4399

    Article  CAS  Google Scholar 

  • Laws EA, Pei SF, Bienfang P, Grant S (2011) Phosphate-limited growth and uptake kinetics of the marine prasinophyte Tetraselmis suecica. Aquaculture 322:117–121

    Article  CAS  Google Scholar 

  • Lenburg ME, O’Shea EK (1996) Signaling phosphate starvation. Trends Biochem Sci 21:383–387

    Article  CAS  PubMed  Google Scholar 

  • Li QY, Gao XS, Sun Y, Zhang QQ, Song RT, Xu ZK (2006) Isolation and characterization of a sodium-dependent phosphate transporter gene in Dunaliella viridis. Biochem Biophys Res Commun 340:95–104

    Article  CAS  PubMed  Google Scholar 

  • Li SH, Xia BB, Zhang C, Cao J, Bai LH (2012) Cloning and characterization of a phosphate transporter gene in Dunaliella salina. J Basic Microbiol 52:429–436

    Article  CAS  PubMed  Google Scholar 

  • Liang YH, Blake RE (2009) Compound- and enzyme-specific phosphodiester hydrolysis mechanisms revealed by δ18O of dissolved inorganic phosphate: implications for marine P cycling. Geochim Cosmochim Acta 73:3782–3794

    Google Scholar 

  • Lin HY, Shih CY, Liu HC, Chang J, Chen YL, Chen YR, Lin HT, Chang YY, Hsu CH, Lin HJ (2013) Identification and characterization of an extracellular alkaline phosphatase in the marine diatom Phaeodactylum tricornutum. Mar Biotechnol 15:425–436

    Article  CAS  PubMed  Google Scholar 

  • Lomas MW, Swain A, Shelton R, Ammerman JW (2004) Taxonomic variability of phosphorus stress in Sargasso Sea phytoplankton. Limnol Oceanogr 49:2303-2309

    Article  Google Scholar 

  • Lomas MW, Burke AL, Lomas DA, Bell DW, Shen C, Dyhrman ST, Ammerman JW (2010) Sargasso sea phosphorus biogeochemistry: an important role for dissolved organic phosphorus (DOP). Biogeosciences 7:695–710

    Article  CAS  Google Scholar 

  • Macaulay IC, Voet T (2014) Single cell genomics: advances and future perspectives. PLoS Genet. doi:10.1371/journal.pgen.1004126

    PubMed  PubMed Central  Google Scholar 

  • Mackey KRM, Mioni CE, Ryan JP, Paytan A (2012) Phosphorus cycling in the red tide incubator region of Monterey Bay in response to upwelling. Front Microbiol 3:33. doi:10.3389/fmicb.2012.00033

    CAS  PubMed  PubMed Central  Google Scholar 

  • Marchetti A, Schruth DM, Durkin CA, Parker MS, Kodner RB, Berthiaume CT, Morales R, Allen AE, Armbrust EV (2012) Comparative metatranscriptomics identifies molecular bases for the physiological responses of phytoplankton to varying iron availability. Proc Natl Acad Sci U S A 109:E317–E325

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Martin P, Van Mooy BAS (2013) Fluorometric quantification of polyphosphate in environmental plankton samples: extraction protocols, matrix effects, and nucleic acid interference. Appl Environ Microbiol 79:273–281

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • 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

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Martin P, Dyhrman ST, Lomas ML, Poulton NJ, Van Mooy BAS (2014) Accumulation and enhanced cycling of polyphosphate by Sargasso Sea plankton in response to low phosphorus. Proc Natl Acad Sci U S A 111:8089–8094

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Martinez A, Tyson GW, DeLong EF (2010) Widespread known and novel phosphonate utilization pathways in marine bacteria revealed by functional screening and metagenomic analyses. Environ Microbiol 12:222–238

    Article  CAS  PubMed  Google Scholar 

  • Martinez A, Osburne MS, Sharma AK, DeLong EF, Chisholm SW (2012) Phosphite utilization by the marine picocyanobacterium Prochlorococcus MIT9301. Environ Microbiol 14:1363–1377

    Article  CAS  PubMed  Google Scholar 

  • Martiny AC, Coleman ML, Chisholm SW (2006) Phosphate acquisition genes in Prochlorococcus ecotypes: evidence for genome-wide adaptation. Proc Natl Acad Sci U S A 103:12552–12557

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Mateo P, Douterelo I, Berrendero E, Perona E (2006) Physiological differences between two species of cyanobacteria in relation to phosphorus limitation. J Phycol 42:61–66

    Article  CAS  Google Scholar 

  • Mather RL, Reynolds SE, Wolff GA, Williams RG, Torres-Valdes S, Woodsward EMS, Landolfi A, Pan X, Sanders R, Achterberg EP (2008) Phosphorus cycling in the North and South Atlantic ocean subtropical gyres. Nat Geosci 1:439–443

    Article  CAS  Google Scholar 

  • Mazard S, Wilson WH, Scanlan DJ (2012) Dissecting the physiological response to phosphorus stress in marine Synechococcus isolates (cyanophyceae). J Phycol 48:94–105

    Article  CAS  Google Scholar 

  • McGrath JW, Chin JP, Quinn JP (2013) Organophosphonates revealed: new insights into the microbial metabolism of ancient molecules. Nat Rev Microbiol 11:412–419

    Article  CAS  PubMed  Google Scholar 

  • McLaughlin K, Kendall C, Silva SR, Young M, Paytan A (2006) Phosphate oxygen isotope ratios as a tracer for sources and cycling of phosphate in north San Francisco Bay, California. J Geophys Res Biogeosci 111:G3. doi:10.1029/2005JG000079

    Article  CAS  Google Scholar 

  • McLaughlin K, Sohm JA, Cutter GA, Lomas MW, Paytan A (2013) Phosphorus cycling in the Sargasso Sea: investigation using the oxygen isotopic composition of phosphate, enzyme-labeled fluorescence, and turnover times. Global Biogeochem Cycles 27:375–387

    Article  CAS  Google Scholar 

  • McLean TI (2013) “Eco-omics”: a review of the application of genomics, transcriptomics, and proteomics for the study of the ecology of harmful algae. Microb Ecol 65:901–915

    Article  CAS  PubMed  Google Scholar 

  • Merchant SS, Helmann JD (2012) Elemental economy: microbial strategies for optimizing growth in the face of nutrient limitation. Adv Microb Phys 60:91–210

    Article  CAS  Google Scholar 

  • Metcalf WW, Griffin BM, Cicchillo RM, Gao JT, Janga SC, Cooke HA, Circello BT, Evans BS, Martens-Habbena W, Stahl DA, van der Donk WA (2012) Synthesis of methylphosphonic acid by marine microbes: a source for methane in the aerobic ocean. Science 337:1104–1107

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Moore LR, Ostrowski M, Scanlan DJ, Feren K, Sweetsir T (2005) Ecotypic variation in phosphorus acquisition mechanisms within marine picocyanobacteria. Aquat Microb Ecol 39:257–269

    Article  Google Scholar 

  • Morel FMM (1987) Kinetics of nutrient uptake and growth in phytoplankton. J Phycol 23:137–150

    Article  CAS  Google Scholar 

  • Morris RM, Nunn BL, Frazar C, Goodlett DR, Ting YS, Rocap G (2010) Comparative metaproteomics reveals ocean-scale shifts in microbial nutrient utilization and energy transduction. ISME J 4:673–685

    Article  CAS  PubMed  Google Scholar 

  • Mulholland MR, Lee C, Glibert PM (2003) Extracellular enzyme activity and uptake of carbon and nitrogen along an estuarine salinity and nutrient gradients. Mar Ecol Prog Ser 258:3–17

    Article  CAS  Google Scholar 

  • Nedoma J, Strojsová A, Vrba J, Komárková J, Simek K (2003) Extracellular phosphatase activity of natural plankton studied with ELF-97 phosphate: fluorescence quantification and labeling kinetics. Environ Microbiol 5:462–472

    Article  CAS  PubMed  Google Scholar 

  • Nicholson D, Dyhrman S, Chavez F, Paytan A (2006) Alkaline phosphatase activity in the phytoplankton communities of Monterey Bay and San Francisco Bay. Limnol Oceanogr 51:874–883

    Article  Google Scholar 

  • Nishikawa K, Machida H, Yamakoshi Y, Ohtomo R, Saito K, Saito M, Tominaga N (2006) Polyphosphate metabolism in an acidophilic alga Chlamydomonas acidophila KT-1 (Chlorophyta) under phosphate stress. Plant Sci 170:307–313

    Article  CAS  Google Scholar 

  • Nishikawa K, Tominaga N, Uchino T, Oikawa A, and Tokunaga H (2009) Polyphosphate contributes to Cd tolerance in Chlamydomonas acidophila KT-1. In: Hagen KN (ed) Algae: nutrition, pollution control and energy sources, Nova Science Publishers, pp 13–21

    Google Scholar 

  • 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. Mol Biol Cell 11:4309–4321

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Orchard ED, Webb EA, Dyhrman ST (2009) Molecular analysis of the phosphorus starvation response in Trichodesmium spp. Environ Microbiol 11:2400–2411

    Article  CAS  PubMed  Google Scholar 

  • Orchard ED, Ammerman JW, Lomas MW, Dyhrman ST (2010a) Dissolved inorganic and organic phosphorus uptake in Trichodesmium and the microbial community: the importance of phosphorus ester in the Sargasso Sea. Limnol Oceanogr 55:1390–1399

    Article  CAS  Google Scholar 

  • Orchard ED, Benitez-Nelson CR, Pellechia PJ, Lomas MW, Dyhrman ST (2010b) Polyphosphate in Trichodesmium from the low-phosphorus Sargasso Sea. Limnol Oceanogr 55:2161–2169

    Article  CAS  Google Scholar 

  • Ostrowski M, Mazard S, Tetu SG, Phillippy K, Johnson A, Palenik B, Paulsen IT, Scanlan DJ (2010) PtrA is required for coordinate regulation of gene expression during phosphate stress in a marine Synechococcus. ISME J 4:908–921

    Article  CAS  PubMed  Google Scholar 

  • Palenik B, Brahamsha B, Larimer FW, Land M, Hauser L, Chain P, Lamerdin J, Regala W, Allen EE, McCarren J, Paulsen I, Dufresne A, Partensky F, Webb EA, Waterbury J (2003) The genome of a motile marine Synechococcus. Nature 424:1037–1042

    Article  CAS  PubMed  Google Scholar 

  • Paragas VB, Zhang Y, Haughland P, Singer VL (1997) The EL-97 alkaline phosphatase substrate provides a bright, photostable, fluorescent signal amplification method for fish. J Histochem Cytochem 45:345–357

    Article  CAS  PubMed  Google Scholar 

  • Pasek MA, Sampson JM, Atlas Z (2014) Redox chemistry in the phosphorus biogeochemical cycle. Proc Natl Acad Sci U S A 111:15468–15473

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Pauli AL, Kaitala S (1997) Phosphate uptake kinetics by Acinetobacter isolates. Biotechnol Bioeng 53:304–309

    Article  CAS  PubMed  Google Scholar 

  • Paytan A, McLaughlin K (2007) The oceanic phosphorus cycle. Chem Rev 107:563–576

    Article  CAS  PubMed  Google Scholar 

  • Perry MJ (1976) Phosphate utilization by an oceanic diatom in phosphorus-limited chemostat culture and in oligotrophic waters of central North-Pacific. Limnol Oceanogr 21:88–107

    Article  CAS  Google Scholar 

  • Pitt FD, Mazard S, Humphreys L, Scanlan DJ (2010) Functional characterization of Synechocystis sp. strain PCC 6803 pst1 and pst2 gene clusters reveals a novel strategy for phosphate uptake in a freshwater cyanobacterium. J Bacteriol 192:3512–3523

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Plaxton WC (1996) The organization and regulation of plant glycolysis. Annu Rev Plant Physiol Plant Mol Biol 47:185–214

    Article  CAS  PubMed  Google Scholar 

  • Quisel JD, Wykoff DD, Grossman AR (1996) Biochemical characterization of the extracellular phosphatases produced by phosphorus-deprived Chlamydomonas reinhardtii. Plant Physiol 111:839–848

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Ranhofer ML, Lawrenz E, Pinckney JL, Benitez-Nelson CR, Richardson TL (2009) Cell-specific alkaline phosphatase expression by phytoplankton from Winyah Bay, South Carolina, USA. Estuar Coasts 32:943–957

    Article  CAS  Google Scholar 

  • Raven JA (2013) RNA function and phosphorus use by photosynthetic organisms. Front Plant Sci 4:536. doi:10.3389/fpls.2013.00536

    Article  PubMed  PubMed Central  Google Scholar 

  • Raven JA, Knoll AH (2010) Non-skeletal biomineralization by eukaryotes: matters of moment and gravity. Geomicrobiol J 27:572–584

    Article  CAS  Google Scholar 

  • Read BA, Kegel J, Klute MJ, Kuo A, Lefebvre SC, Maumus F, Mayer C, Miller J, Monier A, Salamov A, Young J, Aguilar M, Claverie JM, Frickenhaus S, Gonzalez K, Herman EK, Lin YC, Napier J, Ogata H, Sarno AF, Shmutz J, Schroeder D, de Vargas C, Verret F, von Dassow P, Valentin K, Van de Peer Y, Wheeler G, Dacks JB, Delwiche CF, Dyhrman ST, Glockner G, John U, Richards T, Worden AZ, Zhang XY, Grigoriev IV et al (2013) Pan genome of the phytoplankton Emiliania underpins its global distribution. Nature 499:209–213

    Article  CAS  PubMed  Google Scholar 

  • Reistetter EN, Krumhardt K, Callnan K, Roache-Johnson K, Saunders JK, Moore LR, Rocap G (2013) Effects of phosphorus starvation versus limitation on the marine cyanobacterium Prochlorococcus MED4 II: Gene expression. Environ Microbiol 15:2129–2143

    Article  CAS  PubMed  Google Scholar 

  • Renberg L, Johansson AI, Shutova T, Stenlund H, Aksmann A, Raven JA, Gardestrom P, Moritz T, Samuelsson G (2010) A metabolomic approach to study major metabolite changes during acclimation to limiting CO2 in Chlamydomonas reinhardtii. Plant Physiol 154:187–196

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Rengefors K, Pettersson K, Blenckner T, Anderson DM (2001) Species-specific alkaline phosphatase activity in freshwater spring phytoplankton: application of a novel method. J Plankton Res 23:435–443

    Article  CAS  Google Scholar 

  • Rengefors K, Ruttenberg KC, Haupert C, Taylor C, Howes BL, Anderson DM (2003) Experimental investigation of taxon-specific response of alkaline phosphatase activity in natural freshwater phytoplankton. Limnol Oceanogr 48:1167–1175

    Article  CAS  Google Scholar 

  • Riekhof WR, Sears BB, Benning C (2005) Annotation of genes involved in glycerolipid biosynthesis in Chlamydomonas reinhardtii: discovery of the betaine lipid synthase BTA1. Eukaryot Cell 4:242–252

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Rocap G, Larimer FW, Lamerdin J, Malfatti S, Chain P, Ahlgren NA, Arellano A, Coleman M, Hauser L, Hess WR, Johnson ZI, Land M, Lindell D, Post AF, Regala W, Shah M, Shaw SL, Steglich C, Sullivan MB, Ting CS, Tolonen A, Webb EA, Zinser ER, Chisholm SW (2003) Genome divergence in two Prochlorococcus ecotypes reflects oceanic niche differentiation. Nature 424:1042–1047

    Article  CAS  PubMed  Google Scholar 

  • Romans KM, Carpenter EJ, Bergman B (1994) Buoyancy regulation in the colonial diazotrophic cyanobacterium Trichodesmium tenue: ultrastructure and storage of carbohydrate, polyphosphate, and nitrogen. J Phycol 30:935–942

    Article  Google Scholar 

  • Rubio L, Linares-Rueda A, García-Sánchez MJ, Fernández JA (2004) Physiological evidence for a sodium-dependent high affinity phosphate and nitrate transport at the plasma membrane of leaf and root cells of Zostera marina L. J Exp Bot 56:613–622

    Article  PubMed  CAS  Google Scholar 

  • Ruttenberg KC, Dyhrman ST (2005) Temporal and spatial variability of dissolved organic and inorganic phosphorus, and metrics of phosphorus bioavailability in an upwelling-dominated coastal system. J Geophys Res Oceans 110:C10S13. doi:10.1029/2004JC002837

    Article  CAS  Google Scholar 

  • Rynearson TA, Palenik B (2011) Learning to read the oceans: genomics of marine phytoplankton. Adv Mar Biol 60:1–39

    Article  PubMed  Google Scholar 

  • Sakamoto T, Murata N, Ohmori M (1991) The concentration of cyclic AMP and adenylate cyclase activity in cyanobacteria. Plant Cell Physiol 32:581–584

    CAS  Google Scholar 

  • Sato M, Sakuraba R, Hashihama F (2013) Phosphate monoesterase and diesterase activities in the North and South Pacific ocean. Biogeosciences 10:7677–7688

    Article  CAS  Google Scholar 

  • Scanlan DJ, Wilson WH (1999) Application of molecular techniques to addressing the role of P as a key effector in marine ecosystems. Hydrobiologia 401:149–175

    Article  CAS  Google Scholar 

  • Scanlan DJ, Ostrowski M, Mazard S, Dufresne A, Garczarek L, Hess WR, Post AF, Hagemann M, Paulsen I, Partensky F (2009) Ecological genomics of marine picocyanobacteria. Microbiol Mol Biol Rev 73:249–299

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Schindler DW (1977) Evolution of phosphorus limitation in lakes. Science 195:260–262

    Article  CAS  PubMed  Google Scholar 

  • Sebastian M, Ammerman JW (2009) The alkaline phosphatase phoX is more widely distributed in marine bacteria than the classical phoA. ISME J 3:563–572

    Article  CAS  PubMed  Google Scholar 

  • Seidel HM, Freeman S, Seto H, Knowles JR (1988) Phosphonate biosynthesis – isolation of the enzyme responsible for the formation of a carbon phosphorus bond. Nature 335:457–458

    Article  CAS  PubMed  Google Scholar 

  • Shilova IN, Robidart JC, Tripp HJ, Turck-Kubo K, Wwrik B, Post AF, Thompson AW, Ward BB, Hollibaugh JT, Millard A, Ostrowski M, Scanlan DJ, Paerl HW, Stuart R, Zehr JP (2014) A microarray for assessing transcription from pelagic marine microbial taxa. ISME J 8:1476–1491

    Google Scholar 

  • Sinha R, Pearson LA, Davis TW, Muenchhoff J, Pratama R, Jex A, Burford MA, Neilan BA (2014) Comparative genomics of Cylindrospermopsis raciborskii strains with differential toxicities. BMC Genomics 15:83 doi:10.1186/1471-2164-15-83

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  • Sowell SM, Wilhelm LJ, Norbeck AD, Lipton MS, Nicora CD, Barofsky DF, Carlson CA, Smith RD, Giovanonni SJ (2009) Transport functions dominate the SAR11 metaproteome at low-nutrient extremes in the Sargasso Sea. ISME J 3:93–105

    Article  CAS  PubMed  Google Scholar 

  • Springer M, Wykoff DD, Miller N, O’Shea EK (2003) Partially phosphorylated pho4 activates transcription of a subset of phosphate-responsive genes. PLoS Biol 1:261–270

    Article  CAS  Google Scholar 

  • Su Z, Dam P, Chen X, Olman V, Jiang T, Palenik B, Xu Y (2003) Computational inference of regulatory pathways in microbes: an application to phosphorus assimilation pathways in Synechococcus WH8102. Genome Inform 14:3–13

    CAS  PubMed  Google Scholar 

  • Su ZC, Olman V, Xu Y (2007) Computational prediction of pho regulons in cyanobacteria. BMC Genomics 8:156. doi:10.1186/1471-2164-8-156

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  • Suzuki S, Ferjani A, Suzuki I, Murata N (2004) The sphS-sphR two component system is the exclusive sensor for the induction of gene expression in response to phosphate limitation in Synechocystis. J Biol Chem 279:13234–13240

    Article  CAS  PubMed  Google Scholar 

  • Tetu SG, Brahamsha B, Johnson DA, Tai V, Phillippy K, Palenik B, Paulsen IT (2009) Microarray analysis of phosphate regulation in the marine cyanobacterium Synechococcus sp. WH8102. ISME J 3:835–849

    Article  CAS  PubMed  Google Scholar 

  • 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

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Torriani-Gorini A (1987) The birth and death of the pho regulon. In: Torriani-Gorini A, Rothman FG, Silver S, Wright A, Yagil E (eds) Phosphate metabolism and cellular regulation in microorganisms. ASM Press, Washington, DC, pp 3–11

    Google Scholar 

  • Van Mooy BAS, Devol AH (2008) Assessing nutrient limitation of Prochlorococcus in the North Pacific subtropical gyre by using an RNA capture method. Limnol Oceanogr 53:78–88

    Google Scholar 

  • Van Mooy BAS, Fredricks HF, Pedler BE, Dyhrman ST, Karl DM, Koblizek M, Lomas ML, Mincer TJ, Moore LR, Moutin T, Rappe MS (2009) Phytoplankton in the ocean use non-phosphorus lipids in response to phosphorus scarcity. Nature 458:69–72

    Article  PubMed  CAS  Google Scholar 

  • Van Mooy BAS, Hmelo LR, Sofen LE, Campagna SR, May AL, Dyhrman ST, Heithoff A, Webb EA, Momper L, Mincer TJ (2012) Quorum sensing control of phosphorus acquisition in Trichodesmium consortia. ISME J 6:422–429

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  • Venter JC, Remington K, Heidelberg JF, Halpern AL, Rusch D, Eisen JA, Wu DY, Paulsen I, Nelson KE, Nelson W, Fouts DE, Levy S, Knap AH, Lomas MW, Nealson K, White O, Peterson J, Hoffman J, Parsons R, Baden-Tillson H, Pfannkoch C, Rogers YH, Smith HO (2004) Environmental genome shotgun sequencing of the Sargasso Sea. Science 304:66–74

    Article  CAS  PubMed  Google Scholar 

  • Vila-Costa M, Sharma S, Moran MA, Casamayor EO (2013) Diel gene expression profiles of a phosphorus limited mountain lake using metatranscriptomics. Environ Microbiol 15:1190–1203

    Article  CAS  PubMed  Google Scholar 

  • Villarreal-Chiu JF, Quinn JP, McGrath JW (2012) The genes and enzymes of phosphonate metabolism by bacteria, and their distribution in the marine environment. Front Microbiol 3:19. doi:10.3389/fmicb.2012.00019

    CAS  PubMed  PubMed Central  Google Scholar 

  • Voss B, Bolhuis H, Fewer DP, Kopf M, Moke F, Haas F, El-Shehawy R, Hayes P, Bergman B, Sivonen K, Dittmann E, Scanlan DJ, Hagemann M, Stal LJ, Hess WR (2013) Insights into the physiology and ecology of the brackish-water-adapted cyanobacterium Nodularia spumigena CYY9414 based on a genome-transcriptome analysis. PLoS One 8:e60224. doi:10.1371/journal.pone.0060224

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Wagner ND, Hillebrand H, Wacker A, Frost PC (2013) Nutritional indicators and their uses in ecology. Ecol Lett 16:535–544

    Article  PubMed  Google Scholar 

  • Wanner BL (1996) Phosphorus assimilation and control of the phosphate regulon. In: Neidhardt FC (ed) Escherichia coli and salmonella cellular and molecular biology. ASM Press, Washington, DC, pp 1357–1381

    Google Scholar 

  • White A, Dyhrman S (2013) The marine phosphorus cycle. Front Microbiol 4:105. doi:10.3389/fmicb.2013.00105

    CAS  PubMed  PubMed Central  Google Scholar 

  • White AK, Metcalf WW (2004a) The htx and ptx operons of Pseudomonas stutzeri WM88 are new members of the pho regulon. J Bacteriol 186:5876–5882

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • White AK, Metcalf WW (2004b) Two c-p lyase operons in pseudomonas stutzeri and their roles in the oxidation of phosphonates, phosphite, and hypophosphite. J Bacteriol 186:4730–4739

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • White AK, Metcalf WW (2007) Microbial metabolism of reduced phosphorus compounds. Annu Rev Microbiol 61:379–400

    Article  CAS  PubMed  Google Scholar 

  • White AK, Spitz Y, Karl DM, Letelier R (2006) Flexible elemental stoichiometry in Trichodesmium spp. and its ecological implications. Limnol Oceanogr 51:1777–1790

    Article  CAS  Google Scholar 

  • Wurch LL, Bertrand EM, Saito MA, Van Mooy BAS, Dyhrman ST (2011a) Proteome changes driven by phosphorus deficiency and recovery in the brown tide-forming alga Aureococcus anophagefferens. PLoS One 6:e28949. doi:10.1371/journal.pone.0028949

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Wurch LL, Haley ST, Orchard ED, Gobler CJ, Dyhrman ST (2011b) Nutrient-regulated transcriptional responses in the brown tide forming alga Aureococcus anophagefferens. Environ Microbiol 13:468–481

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Wurch LL, Gobler CJ, Dyhrman ST (2014) Expression of a xanthine permease and phosphate transporter in cultures and field populations of the harmful alga Aureococcus anophagefferens: tracking nutritional deficiency during brown tides. Environ Microbiol 16:2444–2457

    Google Scholar 

  • Wykoff DD, O’shea EK (2001) Phosphate transport and sensing in Saccharomyces cerevisiae. Genetics 159:1491–1499

    CAS  PubMed  PubMed Central  Google Scholar 

  • Wykoff DD, Grossman AR, Weeks DP, Usuda H, Shimogawara K (1999) Psr1, a nuclear localized protein that regulates phosphorus metabolism in Chlamydomonas. Proc Natl Acad Sci U S A 96:15336–15341

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Xu Y, Wahlund TM, Feng L, Shaked Y, Morel FMM (2006) A novel alkaline phosphatase in the coccolithophore Emiliania huxleyi (Prymnesiophyceae) and its regulation by phosphorus. J Phycol 42:835–844

    Article  CAS  Google Scholar 

  • Yamaguchi H, Arisaka H, Otsuka N, Tomaru Y (2014) Utilization of phosphate diesters by phosphodiesterase-producing marine diatoms. J Plankton Res 36:281–285

    Article  CAS  Google Scholar 

  • Yong SC, Roversi P, Lillington J, Rodriguez F, Krehenbrink M, Zeldin OB, Garman EF, Lea SM, Berks BC (2014) A complex iron-calcium cofactor catalyzing phosphotransfer chemistry. Science 345:1170–1173

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Young CL, Ingall ED (2010) Marine dissolved organic phosphorus composition: insights from samples recovered using combined electrodialysis/reverse osmosis. Aquat Geochem 16:563–574

    Article  CAS  Google Scholar 

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Acknowledgements

This work was in part supported by NSF OCE 13-16036, the Center for Microbial Oceanography: Research and Education, and the Woods Hole Oceanographic Institution (WHOI) Coastal Ocean Institute. The author thanks Sheean Haley for editorial assistance, Kathleen Ruttenberg for helpful discussions, and Kyle Frischkorn and the WHOI Graphics Department for assistance with figures.

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  1. Department of Earth and Environmental Science, Lamont-Doherty Earth Observatory, Columbia University, 61 Route 9W, Palisades, NY, 10964, USA

    Sonya T. Dyhrman

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  1. School of Veterinary and Life Sciences, Murdoch University, Algae R&D Centre, Murdoch, West Australia, Australia

    Michael A. Borowitzka

  2. School of Biological Sciences, Monash University, Clayton, Victoria, Australia

    John Beardall

  3. Division of Plant Biology, University of Dundee at the James Hutton, Dundee, United Kingdom

    John A. Raven

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Dyhrman, S.T. (2016). Nutrients and Their Acquisition: Phosphorus Physiology in Microalgae. In: Borowitzka, M., Beardall, J., Raven, J. (eds) The Physiology of Microalgae. Developments in Applied Phycology, vol 6. Springer, Cham. https://doi.org/10.1007/978-3-319-24945-2_8

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