Nutrients and Their Acquisition: Phosphorus Physiology in Microalgae

  • Sonya T. DyhrmanEmail author
Part of the Developments in Applied Phycology book series (DAPH, volume 6)


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.


Phosphorus Algae Cyanobacteria Phosphate Phosphonate Phosphite Organic phosphorus Redox cycling Phosphorus stress 



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.


  1. 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 190:8171–8184PubMedPubMedCentralCrossRefGoogle Scholar
  2. Ammerman J, Azam F (1985) Bacterial 5′ nucleotidase in aquatic ecosystems: a novel mechanism of phosphorus regeneration. Science 227:1338–1340PubMedCrossRefGoogle Scholar
  3. Ammerman JW, Azam F (1991) Bacterial 5′-nucleotidase activity in estuarine and coastal marine waters – role in phosphorus regeneration. Limnol Oceanogr 36:1437–1447CrossRefGoogle Scholar
  4. Anderson DM, Glibert PM, Burkholder JM (2002) Harmful algal blooms and eutrophication: nutrient sources, composition and consequences. Estuaries 25:704–726CrossRefGoogle Scholar
  5. 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 306:79–86PubMedCrossRefGoogle Scholar
  6. Azam F, Malfatti F (2007) Microbial structuring of marine ecosystems. Nat Rev Microbiol 5:782–791PubMedCrossRefGoogle Scholar
  7. 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):1557–1561Google Scholar
  8. Beardall J, Young E, Roberts S (2001) Approaches for determining phytoplankton nutrient limitation. Aquat Sci 63:44–69CrossRefGoogle Scholar
  9. 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 49:786–801CrossRefGoogle Scholar
  10. Benitez-Nelson CR (2000) The biogeochemical cycling of phosphorus in marine systems. Earth Sci Rev 51:109–135CrossRefGoogle Scholar
  11. 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 48:1721–1731CrossRefGoogle Scholar
  12. 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 18:1–15CrossRefGoogle Scholar
  13. Beversdorf LJ, White AE, Björkman KM, Letelier RM, Karl DM (2010) Phosphonate metabolism of Trichodesmium IMS101 and the production of greenhouse gases. Limnol Oceanogr 55:1768–1778CrossRefGoogle Scholar
  14. 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 111:265–273CrossRefGoogle Scholar
  15. 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 47:159–167CrossRefGoogle Scholar
  16. 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 PubMedPubMedCentralGoogle Scholar
  17. Blake RE, O’Neil JR, Surkov AV (2005) Biogeochemical cycling of phosphorus: insights from oxygen isotope effects of phosphoenzymes. Am J Sci 305:596–620CrossRefGoogle Scholar
  18. Bolier G, de Koningh CJ, Schmale JC, Donze M (1992) Differential luxury phosphate response of planktonic algae to phosphorus removal. Hydrobiologia 243/244:113–118CrossRefGoogle Scholar
  19. 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 655–681Google Scholar
  20. Cade-Menun BJ, Paytan A (2010) Nutrient temperature and light stress alter phosphorus and carbon forms in culture-grown algae. Mar Chem 121:27–36CrossRefGoogle Scholar
  21. 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 97:293–306CrossRefGoogle Scholar
  22. Capone DG, Zehr JP, Paerl HW, Bergman B, Carpenter E (1997) Trichodesmium, a globally significant marine cyanobacterium. Science 276:1221–1229CrossRefGoogle Scholar
  23. 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 58:31–44CrossRefGoogle Scholar
  24. 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 10:317–391CrossRefGoogle Scholar
  25. 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 11:13–81CrossRefGoogle Scholar
  26. Chisholm SW, Stross RG (1976) Phosphate uptake kinetics in Euglena gracilis (Euglenophyceae) grown on light/dark cycles. I. Synchronized batch cultures. J Phycol 12:210–217Google Scholar
  27. 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 69:754–759PubMedPubMedCentralCrossRefGoogle Scholar
  28. Clark LL, Ingall ED, Benner R (1998) Marine phosphorus is selectively remineralized. Nature 393:426CrossRefGoogle Scholar
  29. Clark LL, Ingall ED, Benner R (1999) Marine organic phosphorus cycling: novel insights from nuclear magnetic resonance. Am J Sci 299:724–737CrossRefGoogle Scholar
  30. Coleman ML, Chisholm SW (2010) Ecosystem-specific selection pressures revealed through comparative population genomics. Proc Natl Acad Sci U S A 107:18634–18639PubMedPubMedCentralCrossRefGoogle Scholar
  31. 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 102:13023–13028PubMedPubMedCentralCrossRefGoogle Scholar
  32. Costas AMG, White AK, Metcalf WW (2001) Purification and characterization of a novel phosphorus-oxidizing enzyme from Pseudomonas stutzeri WM88. J Biol Chem 276:17429–17436PubMedCrossRefGoogle Scholar
  33. 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 PubMedPubMedCentralGoogle Scholar
  34. 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 66:1175–1182PubMedPubMedCentralCrossRefGoogle Scholar
  35. 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 107:14679–14684PubMedPubMedCentralCrossRefGoogle Scholar
  36. Diaz JM, Ingall ED (2010) Fluorometric quantification of natural inorganic polyphosphate. Environ Sci Tech 44:4665–4671CrossRefGoogle Scholar
  37. 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 320:652–655PubMedCrossRefGoogle Scholar
  38. 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
  39. 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 48:29–38PubMedCrossRefGoogle Scholar
  40. 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 19:1793–1813CrossRefGoogle Scholar
  41. Droop MR (1973) Some thoughts on nutrient limitation in algae. J Phycol 9:264–272Google Scholar
  42. Duhamel S, Dyhrman ST, Karl DM (2010) Alkaline phosphatase activity and regulation in the north pacific subtropical gyre. Limnol Oceanogr 55:1414–1425CrossRefGoogle Scholar
  43. 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 67:225–238CrossRefGoogle Scholar
  44. Dyhrman ST (2005) Ectoenzymes in Prorocentrum minimum. Harmful Algae 4:619–627CrossRefGoogle Scholar
  45. Dyhrman ST (2008) Molecular approaches to diagnosing nutritional physiology in harmful algae: implications for studying the effects of eutrophication. Harmful Algae 8:167–174CrossRefGoogle Scholar
  46. Dyhrman ST, Haley ST (2006) Phosphorus scavenging in the unicellular marine diazotroph Crocosphaera watsonii. Appl Environ Microbiol 72:1452–1458PubMedPubMedCentralCrossRefGoogle Scholar
  47. Dyhrman ST, Palenik BP (1997) The identification and purification of a cell-surface alkaline phosphatase from the dinoflagellate Prorocentrum minimum (Dinophyceae). J Phycol 33:602–612CrossRefGoogle Scholar
  48. 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 65:3205–3212PubMedPubMedCentralGoogle Scholar
  49. Dyhrman ST, Palenik BP (2001) A single-cell immunoassay for phosphate stress in the dinoflagellate Prorocentrum minimum (Dinophyceae). J Phycol 37:400–410CrossRefGoogle Scholar
  50. Dyhrman ST, Palenik BP (2003) Characterization of ectoenzyme activity and phosphate-regulated proteins in the coccolithophorid Emiliania huxleyi. J Plankton Res 25:1215–1225CrossRefGoogle Scholar
  51. 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 51:1381–1390CrossRefGoogle Scholar
  52. 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 47:1823–1836CrossRefGoogle Scholar
  53. 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 439:68–71PubMedCrossRefGoogle Scholar
  54. 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 72:252–260PubMedPubMedCentralCrossRefGoogle Scholar
  55. Dyhrman ST, Ammerman JW, Van Mooy BAS (2007) Microbes and the marine phosphorus cycle. Oceanography 20:110–116CrossRefGoogle Scholar
  56. Dyhrman ST, Benitez-Nelson CR, Orchard ED, Haley ST, Pellechia PJ (2009) A microbial source of phosphonates in oligotrophic marine systems. Nat Geosci 2:696–699CrossRefGoogle Scholar
  57. 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 PubMedPubMedCentralCrossRefGoogle Scholar
  58. Eixler S, Karsten U, Selig U (2006) Phosphorus storage in Chlorella vulgaris (Trebouxiophyceae, Chlorophyta) cell and its dependence on phosphate supply. Phycologia 45:53–60CrossRefGoogle Scholar
  59. 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 PubMedPubMedCentralCrossRefGoogle Scholar
  60. 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 6:827–834PubMedPubMedCentralCrossRefGoogle Scholar
  61. Flynn KJ, Oepik H, Syrett PJ (1986) Localization of the alkaline phosphatase and 5′-nucleotidase activities of the diatom Phaeodactylum tricornutum. J Gen Microbiol 132:289–298Google Scholar
  62. Flynn KJ, Raven JA, Rees TA, Finkel Z, Quigg A, Beardall J (2010) Is the growth rate hypothesis applicable to microalgae? J Phycol 46:1–12CrossRefGoogle Scholar
  63. 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 PubMedPubMedCentralGoogle Scholar
  64. 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 41:62–73CrossRefGoogle Scholar
  65. 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 16:1137–1149PubMedCrossRefGoogle Scholar
  66. Fuszard MA, Wright PC, Biggs CA (2010) Cellular acclimation strategies of a minimal picocyanobacterium to phosphate stress. FEMS Microbiol Lett 306:127–134PubMedCrossRefGoogle Scholar
  67. Gifford SM, Sharma S, Rinta-Kanto JM, Moran MA (2011) Quantitative analysis of a deeply sequenced marine microbial metatranscriptome. ISME J 5:461–472PubMedPubMedCentralCrossRefGoogle Scholar
  68. 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 173–183CrossRefGoogle Scholar
  69. Girault M, Arakawa H, Hashihama F (2013) Phosphorus stress of microphytoplankton community in the western subtropical North Pacific. J Plankton Res 35:146–157CrossRefGoogle Scholar
  70. 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 108:4352–4357PubMedPubMedCentralCrossRefGoogle Scholar
  71. 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 302:601–609PubMedCrossRefGoogle Scholar
  72. 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 5:141–149PubMedPubMedCentralCrossRefGoogle Scholar
  73. 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 164:21–35CrossRefGoogle Scholar
  74. Grossman A (2000) Acclimation of Chlamydomonas reinhardtii to its nutrient environment. Protist 151:201–224PubMedCrossRefGoogle Scholar
  75. Grossman A, Takahashi H (2001) Macronutrient utilization by photosynthetic eukaryotes and the fabric of interactions. Annu Rev Plant Physiol Plant Mol Biol 52:163–210PubMedCrossRefGoogle Scholar
  76. 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 PubMedPubMedCentralCrossRefGoogle Scholar
  77. Harke MJ, Berry DL, Ammerman JW, Gobler CJ (2012) Molecular response of the bloom-forming cyanobacterium, Microcystis aeruginosa, to phosphorus limitation. Microb Ecol 63:188–198PubMedCrossRefGoogle Scholar
  78. 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 172:3066–3072PubMedPubMedCentralGoogle Scholar
  79. 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 324:513–516PubMedCrossRefGoogle Scholar
  80. Hynes AM, Chappell PD, Dyhrman ST, Doney SC, Webb EA (2009) Cross-basin comparison of phosphorus stress and nitrogen fixation in Trichodesmium. Limnol Oceanogr 54:1438–1448CrossRefGoogle Scholar
  81. 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–S187CrossRefGoogle Scholar
  82. Jacobson L, Halmann M (1982) Polyphosphate metabolism in the blue-green alga Microcystis aeruginosa. J Plankton Res 4:481–488CrossRefGoogle Scholar
  83. 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 CrossRefGoogle Scholar
  84. Jansson M (1988) Phosphate-uptake and utilization by bacteria and algae. Hydrobiologia 170:177–189CrossRefGoogle Scholar
  85. Jansson M, Olsson L, Pettersson K (1988) Phosphatases: origin, characteristics and function in lakes. Hydrobiologia 170:157–175CrossRefGoogle Scholar
  86. Karl DM (2014) Microbially mediated transformations of phosphorus in the sea: new views of an old cycle. Annu Rev Mar Sci 6:279–337CrossRefGoogle Scholar
  87. 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 249–366Google Scholar
  88. Karl DM, Björkman KM (2002) Dynamics of DOP. In: Hansell D, Carlson C (eds) Biogeochemistry of marine dissolved organic matter. Elsevier Science, Boston, pp 249–366CrossRefGoogle Scholar
  89. 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 344:416–420PubMedCrossRefGoogle Scholar
  90. Kathuria S, Martiny AC (2011) Prevalence of a calcium-based alkaline phosphatase associated with the marine cyanobacterium Prochlorococcus and other ocean bacteria. Environ Microbiol 13:74–83PubMedCrossRefGoogle Scholar
  91. Kittredge JS, Roberts EA (1969) A carbon-phosphorus bond in nature. Science 164:37–42PubMedCrossRefGoogle Scholar
  92. Kittredge JS, Horiguchi M, Williams PM (1969) Aminophosphonic acids: biosynthesis by marine phytoplankton. Comp Biochem Physiol 29:859–863PubMedCrossRefGoogle Scholar
  93. Komeili A, O’shea EK (1999) Roles of phosphorylation sites in regulating activity of the transcription factor pho4. Science 284:977–980PubMedCrossRefGoogle Scholar
  94. Kornberg A (1995) Inorganic polyphosphate: toward making a forgotten polymer unforgettable. J Bacteriol 177:491–496PubMedPubMedCentralGoogle Scholar
  95. Kornberg A, Rao N, Ault-Riche D (1999) Inorganic polyphosphate: a molecule of many functions. Ann Rev Biochem 68:89–125PubMedCrossRefGoogle Scholar
  96. 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 42:243–253CrossRefGoogle Scholar
  97. 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 15:2114–2128PubMedCrossRefGoogle Scholar
  98. 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 21:31–47CrossRefGoogle Scholar
  99. Kujawinski EB (2011) The impact of microbial metabolism on marine dissolved organic matter. Ann Rev Mar Sci 3:567–599PubMedCrossRefGoogle Scholar
  100. 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 73:4384–4399CrossRefGoogle Scholar
  101. Laws EA, Pei SF, Bienfang P, Grant S (2011) Phosphate-limited growth and uptake kinetics of the marine prasinophyte Tetraselmis suecica. Aquaculture 322:117–121CrossRefGoogle Scholar
  102. Lenburg ME, O’Shea EK (1996) Signaling phosphate starvation. Trends Biochem Sci 21:383–387PubMedCrossRefGoogle Scholar
  103. 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 340:95–104PubMedCrossRefGoogle Scholar
  104. 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 52:429–436PubMedCrossRefGoogle Scholar
  105. 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 73:3782–3794Google Scholar
  106. 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 15:425–436PubMedCrossRefGoogle Scholar
  107. Lomas MW, Swain A, Shelton R, Ammerman JW (2004) Taxonomic variability of phosphorus stress in Sargasso Sea phytoplankton. Limnol Oceanogr 49:2303-2309CrossRefGoogle Scholar
  108. 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 7:695–710CrossRefGoogle Scholar
  109. Macaulay IC, Voet T (2014) Single cell genomics: advances and future perspectives. PLoS Genet. doi: 10.1371/journal.pgen.1004126 PubMedPubMedCentralGoogle Scholar
  110. 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 PubMedPubMedCentralGoogle Scholar
  111. 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–E325PubMedPubMedCentralCrossRefGoogle Scholar
  112. 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 79:273–281PubMedPubMedCentralCrossRefGoogle Scholar
  113. 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 5:1057–1060PubMedPubMedCentralCrossRefGoogle Scholar
  114. 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 111:8089–8094PubMedPubMedCentralCrossRefGoogle Scholar
  115. 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 12:222–238PubMedCrossRefGoogle Scholar
  116. Martinez A, Osburne MS, Sharma AK, DeLong EF, Chisholm SW (2012) Phosphite utilization by the marine picocyanobacterium Prochlorococcus MIT9301. Environ Microbiol 14:1363–1377PubMedCrossRefGoogle Scholar
  117. 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 103:12552–12557PubMedPubMedCentralCrossRefGoogle Scholar
  118. Mateo P, Douterelo I, Berrendero E, Perona E (2006) Physiological differences between two species of cyanobacteria in relation to phosphorus limitation. J Phycol 42:61–66CrossRefGoogle Scholar
  119. 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 1:439–443CrossRefGoogle Scholar
  120. Mazard S, Wilson WH, Scanlan DJ (2012) Dissecting the physiological response to phosphorus stress in marine Synechococcus isolates (cyanophyceae). J Phycol 48:94–105CrossRefGoogle Scholar
  121. McGrath JW, Chin JP, Quinn JP (2013) Organophosphonates revealed: new insights into the microbial metabolism of ancient molecules. Nat Rev Microbiol 11:412–419PubMedCrossRefGoogle Scholar
  122. 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 CrossRefGoogle Scholar
  123. 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 27:375–387CrossRefGoogle Scholar
  124. 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 65:901–915PubMedCrossRefGoogle Scholar
  125. Merchant SS, Helmann JD (2012) Elemental economy: microbial strategies for optimizing growth in the face of nutrient limitation. Adv Microb Phys 60:91–210CrossRefGoogle Scholar
  126. 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 337:1104–1107PubMedPubMedCentralCrossRefGoogle Scholar
  127. Moore LR, Ostrowski M, Scanlan DJ, Feren K, Sweetsir T (2005) Ecotypic variation in phosphorus acquisition mechanisms within marine picocyanobacteria. Aquat Microb Ecol 39:257–269CrossRefGoogle Scholar
  128. Morel FMM (1987) Kinetics of nutrient uptake and growth in phytoplankton. J Phycol 23:137–150CrossRefGoogle Scholar
  129. 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 4:673–685PubMedCrossRefGoogle Scholar
  130. 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 258:3–17CrossRefGoogle Scholar
  131. 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 5:462–472PubMedCrossRefGoogle Scholar
  132. 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 51:874–883CrossRefGoogle Scholar
  133. 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 170:307–313CrossRefGoogle Scholar
  134. 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 13–21Google Scholar
  135. 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 11:4309–4321PubMedPubMedCentralCrossRefGoogle Scholar
  136. Orchard ED, Webb EA, Dyhrman ST (2009) Molecular analysis of the phosphorus starvation response in Trichodesmium spp. Environ Microbiol 11:2400–2411PubMedCrossRefGoogle Scholar
  137. 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 55:1390–1399CrossRefGoogle Scholar
  138. Orchard ED, Benitez-Nelson CR, Pellechia PJ, Lomas MW, Dyhrman ST (2010b) Polyphosphate in Trichodesmium from the low-phosphorus Sargasso Sea. Limnol Oceanogr 55:2161–2169CrossRefGoogle Scholar
  139. 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 4:908–921PubMedCrossRefGoogle Scholar
  140. 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 424:1037–1042PubMedCrossRefGoogle Scholar
  141. 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 45:345–357PubMedCrossRefGoogle Scholar
  142. Pasek MA, Sampson JM, Atlas Z (2014) Redox chemistry in the phosphorus biogeochemical cycle. Proc Natl Acad Sci U S A 111:15468–15473PubMedPubMedCentralCrossRefGoogle Scholar
  143. Pauli AL, Kaitala S (1997) Phosphate uptake kinetics by Acinetobacter isolates. Biotechnol Bioeng 53:304–309PubMedCrossRefGoogle Scholar
  144. Paytan A, McLaughlin K (2007) The oceanic phosphorus cycle. Chem Rev 107:563–576PubMedCrossRefGoogle Scholar
  145. Perry MJ (1976) Phosphate utilization by an oceanic diatom in phosphorus-limited chemostat culture and in oligotrophic waters of central North-Pacific. Limnol Oceanogr 21:88–107CrossRefGoogle Scholar
  146. 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 192:3512–3523PubMedPubMedCentralCrossRefGoogle Scholar
  147. Plaxton WC (1996) The organization and regulation of plant glycolysis. Annu Rev Plant Physiol Plant Mol Biol 47:185–214PubMedCrossRefGoogle Scholar
  148. Quisel JD, Wykoff DD, Grossman AR (1996) Biochemical characterization of the extracellular phosphatases produced by phosphorus-deprived Chlamydomonas reinhardtii. Plant Physiol 111:839–848PubMedPubMedCentralCrossRefGoogle Scholar
  149. 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 32:943–957CrossRefGoogle Scholar
  150. Raven JA (2013) RNA function and phosphorus use by photosynthetic organisms. Front Plant Sci 4:536. doi: 10.3389/fpls.2013.00536 PubMedPubMedCentralCrossRefGoogle Scholar
  151. Raven JA, Knoll AH (2010) Non-skeletal biomineralization by eukaryotes: matters of moment and gravity. Geomicrobiol J 27:572–584CrossRefGoogle Scholar
  152. 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 499:209–213PubMedCrossRefGoogle Scholar
  153. 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 15:2129–2143PubMedCrossRefGoogle Scholar
  154. 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 154:187–196PubMedPubMedCentralCrossRefGoogle Scholar
  155. 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 23:435–443CrossRefGoogle Scholar
  156. 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 48:1167–1175CrossRefGoogle Scholar
  157. 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 4:242–252PubMedPubMedCentralCrossRefGoogle Scholar
  158. 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 424:1042–1047PubMedCrossRefGoogle Scholar
  159. 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 30:935–942CrossRefGoogle Scholar
  160. 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 56:613–622PubMedCrossRefGoogle Scholar
  161. 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 CrossRefGoogle Scholar
  162. Rynearson TA, Palenik B (2011) Learning to read the oceans: genomics of marine phytoplankton. Adv Mar Biol 60:1–39PubMedCrossRefGoogle Scholar
  163. Sakamoto T, Murata N, Ohmori M (1991) The concentration of cyclic AMP and adenylate cyclase activity in cyanobacteria. Plant Cell Physiol 32:581–584Google Scholar
  164. Sato M, Sakuraba R, Hashihama F (2013) Phosphate monoesterase and diesterase activities in the North and South Pacific ocean. Biogeosciences 10:7677–7688CrossRefGoogle Scholar
  165. Scanlan DJ, Wilson WH (1999) Application of molecular techniques to addressing the role of P as a key effector in marine ecosystems. Hydrobiologia 401:149–175CrossRefGoogle Scholar
  166. 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 73:249–299PubMedPubMedCentralCrossRefGoogle Scholar
  167. Schindler DW (1977) Evolution of phosphorus limitation in lakes. Science 195:260–262PubMedCrossRefGoogle Scholar
  168. Sebastian M, Ammerman JW (2009) The alkaline phosphatase phoX is more widely distributed in marine bacteria than the classical phoA. ISME J 3:563–572PubMedCrossRefGoogle Scholar
  169. 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 335:457–458PubMedCrossRefGoogle Scholar
  170. 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 8:1476–1491Google Scholar
  171. 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 PubMedPubMedCentralCrossRefGoogle Scholar
  172. 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 3:93–105PubMedCrossRefGoogle Scholar
  173. Springer M, Wykoff DD, Miller N, O’Shea EK (2003) Partially phosphorylated pho4 activates transcription of a subset of phosphate-responsive genes. PLoS Biol 1:261–270CrossRefGoogle Scholar
  174. 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 14:3–13PubMedGoogle Scholar
  175. 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 PubMedPubMedCentralCrossRefGoogle Scholar
  176. 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 279:13234–13240PubMedCrossRefGoogle Scholar
  177. 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 3:835–849PubMedCrossRefGoogle Scholar
  178. Theodorou ME, Elrifi IR, Turpin DH, Plaxton WC (1991) Effects of phosphorus limitation on respiratory metabolism in the green-alga Selenastrum minutum. Plant Physiol 95:1089–1095PubMedPubMedCentralCrossRefGoogle Scholar
  179. 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 3–11Google Scholar
  180. 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 53:78–88Google Scholar
  181. 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 458:69–72PubMedCrossRefGoogle Scholar
  182. 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 6:422–429PubMedPubMedCentralCrossRefGoogle Scholar
  183. 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 304:66–74PubMedCrossRefGoogle Scholar
  184. Vila-Costa M, Sharma S, Moran MA, Casamayor EO (2013) Diel gene expression profiles of a phosphorus limited mountain lake using metatranscriptomics. Environ Microbiol 15:1190–1203PubMedCrossRefGoogle Scholar
  185. 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 PubMedPubMedCentralGoogle Scholar
  186. 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 PubMedPubMedCentralCrossRefGoogle Scholar
  187. Wagner ND, Hillebrand H, Wacker A, Frost PC (2013) Nutritional indicators and their uses in ecology. Ecol Lett 16:535–544PubMedCrossRefGoogle Scholar
  188. 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 1357–1381Google Scholar
  189. White A, Dyhrman S (2013) The marine phosphorus cycle. Front Microbiol 4:105. doi: 10.3389/fmicb.2013.00105 PubMedPubMedCentralGoogle Scholar
  190. White AK, Metcalf WW (2004a) The htx and ptx operons of Pseudomonas stutzeri WM88 are new members of the pho regulon. J Bacteriol 186:5876–5882PubMedPubMedCentralCrossRefGoogle Scholar
  191. 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 186:4730–4739PubMedPubMedCentralCrossRefGoogle Scholar
  192. White AK, Metcalf WW (2007) Microbial metabolism of reduced phosphorus compounds. Annu Rev Microbiol 61:379–400PubMedCrossRefGoogle Scholar
  193. White AK, Spitz Y, Karl DM, Letelier R (2006) Flexible elemental stoichiometry in Trichodesmium spp. and its ecological implications. Limnol Oceanogr 51:1777–1790CrossRefGoogle Scholar
  194. 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 PubMedPubMedCentralCrossRefGoogle Scholar
  195. 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 13:468–481PubMedPubMedCentralCrossRefGoogle Scholar
  196. 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 16:2444–2457Google Scholar
  197. Wykoff DD, O’shea EK (2001) Phosphate transport and sensing in Saccharomyces cerevisiae. Genetics 159:1491–1499PubMedPubMedCentralGoogle Scholar
  198. 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 96:15336–15341PubMedPubMedCentralCrossRefGoogle Scholar
  199. 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 42:835–844CrossRefGoogle Scholar
  200. Yamaguchi H, Arisaka H, Otsuka N, Tomaru Y (2014) Utilization of phosphate diesters by phosphodiesterase-producing marine diatoms. J Plankton Res 36:281–285CrossRefGoogle Scholar
  201. 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 345:1170–1173PubMedPubMedCentralCrossRefGoogle Scholar
  202. Young CL, Ingall ED (2010) Marine dissolved organic phosphorus composition: insights from samples recovered using combined electrodialysis/reverse osmosis. Aquat Geochem 16:563–574CrossRefGoogle Scholar

Copyright information

© Springer International Publishing Switzerland 2016

Authors and Affiliations

  1. 1.Department of Earth and Environmental Science, Lamont-Doherty Earth ObservatoryColumbia UniversityPalisadesUSA

Personalised recommendations