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Annual Review of Marine Science

Volume 7, 2015

Phytoplankton Strategies for Photosynthetic Energy Allocation

Abstract

Phytoplankton physiology is dynamic and highly responsive to the environment. Phytoplankton acclimate to changing environmental conditions by a complex reallocation of carbon and energy through metabolic pathways to optimize growth. Considering the tremendous diversity of phytoplankton, it is not surprising that different phytoplankton taxa use different strategies to partition carbon and energy resources. It has therefore been satisfying to discover that general principles of energetic stoichiometry appear to govern these complex processes and can be broadly applied to interpret phytoplankton distributions, productivity, and food web dynamics. The expectation of future changes in aquatic environments brought on by climate change warrants gathering knowledge about underlying patterns of photosynthetic energy allocation and their impacts on community structure and ecosystem productivity.

Keyword(s): growth strategies, metabolism, physiology, resource allocation, traits
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2015-01-03
2024-05-02
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Literature Cited

  1. Allen AE, La Roche J, Maheswari U, Lommer M, Schauer N. et al. 2008. Whole-cell response of the pennate diatom Phaeodactylum tricornutum to iron starvation. Proc. Natl. Acad. Sci. USA 105:10438–43 [Google Scholar]
  2. Allen JF. 2003. Cyclic, pseudocyclic and noncyclic photophosphorylation: new links in the chain. Trends Plant Sci. 8:15–19 [Google Scholar]
  3. Alric J. 2010. Cyclic electron flow around photosystem I in unicellular green algae. Photosynth. Res. 106:47–56 [Google Scholar]
  4. Asada K. 1999. The water-water cycle in chloroplasts: scavenging of active oxygens and dissipation of excess photons. Annu. Rev. Plant Physiol. Plant Mol. Biol. 50:601–39 [Google Scholar]
  5. Bailey S, Mells A, Mackey KRM, Cardol P, Finazzi G. et al. 2008. Alternative photosynthetic electron flow to oxygen in marine Synechococcus. Biochim. Biophys. Acta 1777:269–76 [Google Scholar]
  6. Baran R, Bowen BP, Northen TR. 2011. Untargeted metabolic footprinting reveals a surprising breadth of metabolite uptake and release by Synechococcus sp. PCC 7002. Mol. Biosyst. 7:3200–6 [Google Scholar]
  7. Barnett AM, Hirota J. 1967. Changes in the apparent rate of 14C uptake with length of incubation period in natural phytoplankton populations. Limnol. Oceanogr. 12:349–53 [Google Scholar]
  8. Batchelor GK. 1953. The Theory of Homogenous Turbulence Cambridge, UK: Cambridge Univ. Press
  9. Behrenfeld MJ. 2010. Abandoning Sverdrup's Critical Depth Hypothesis on phytoplankton blooms. Ecology 91:977–89 [Google Scholar]
  10. Behrenfeld MJ, Boss ES, Siegel DA, Shea DM. 2005. Carbon-based ocean productivity and phytoplankton physiology from space. Glob. Biogeochem. Cycles 19:GB1006 [Google Scholar]
  11. Behrenfeld MJ, Doney SC, Lima I, Boss ES, Siegel DA. 2013. Annual cycles of ecological disturbance and recovery underlying the subarctic Atlantic spring plankton bloom. Glob. Biogeochem. Cycles 27:526–40 [Google Scholar]
  12. Behrenfeld MJ, Halsey KH, Milligan AJ. 2008. Evolved physiological responses of phytoplankton to their integrated growth environment. Philos. Trans. R. Soc. B 363:2687–703 [Google Scholar]
  13. Behrenfeld MJ, Kolber ZS. 1999. Widespread iron limitation of phytoplankton in the South Pacific Ocean. Science 283:840–43 [Google Scholar]
  14. Behrenfeld MJ, Milligan AJ. 2012. Photophysiological expressions of iron stress in phytoplankton. Annu. Rev. Mar. Sci. 5:217–46 [Google Scholar]
  15. Behrenfeld MJ, Prasil O, Babin M, Bruyant F. 2004. In search of a physiological basis for covariations in light-limited and light-saturated photosynthesis. J. Phycol. 40:4–25 [Google Scholar]
  16. Behrenfeld MJ, Prasil O, Kolber Z, Babin M, Falkowski PG. 1998. Compensatory changes in photosystem II electron turnover rates protect photosynthesis from photoinhibition. Photosynth. Res. 58:259–68 [Google Scholar]
  17. Behrenfeld MJ, Worthington K, Sherrell RM, Chavez FP, Strutton P. et al. 2006. Controls on tropical Pacific Ocean productivity revealed through nutrient stress diagnostics. Nature 442:1025–28 [Google Scholar]
  18. Bell G. 2012. Experimental evolution of heterotrophy in a green alga. Evolution 67:468–76 [Google Scholar]
  19. Ben-Amotz A, Tornabene TG, Thomas WH. 1985. Chemical profile of selected species of microalgae with emphasis on lipids. J. Phycol. 21:72–81 [Google Scholar]
  20. Bowler CB, Allen AE, Badger JH, Grimwood J, Jabbari K. et al. 2008. The Phaeodactylum genome reveals the evolutionary history of diatom genomes. Nature 456:239–44 [Google Scholar]
  21. Bruyant F, Babin M, Genty B, Prasil O, Behrenfeld MJ. et al. 2005. Diel variations in the photosynthetic parameters of Prochlorococcus strain 9511: combined effects of light and cell cycle. Limnol. Oceanogr. 50:850–63 [Google Scholar]
  22. Bruyant F, Babin M, Sciandra A, Marie D, Genty B. et al. 2001. An axenic cyclostat of Prochlorococcus strain PCC9511 with a simulator of natural light regimes. J. Appl. Phycol. 13:135–42 [Google Scholar]
  23. Bull AT. 2010. The renaissance of continuous culture in the post-genomics age. J. Ind. Microbiol. Biotechnol. 37:993–1021 [Google Scholar]
  24. Burbage CD, Binder BJ. 2007. Relationship between cell cycle and light-limited growth rate in oceanic Prochlorococcus (MIT9312) and Synechococcus (WH8103) (Cyanobacteria). J. Phycol. 43:266–74 [Google Scholar]
  25. Capone DG. 2000. The marine microbial nitrogen cycle. Microbial Ecology of the Oceans DL Kirchman 455–93 New York: Wiley-Liss [Google Scholar]
  26. Cardol P, Bailleul B, Rappaport F, Derelle E, Beal D. et al. 2008. An original adaptation of photosynthesis in the marine green alga Ostreococcus. Proc. Natl. Acad. Sci. USA 105:7881–86 [Google Scholar]
  27. Claquin P, Kromkamp JC, Martin-Jezequel V. 2004. Relationship between photosynthetic metabolism and cell cycle in a synchronized culture of the marine alga Cylindrotheca fusiformis (Bacillariophyceae). Eur. J. Phycol. 39:33–41 [Google Scholar]
  28. Collins S, Bell G. 2004. Phenotypic consequences of 1,000 generations of selection at elevated CO2 in a green alga. Nature 431:566–69 [Google Scholar]
  29. Cuhel RL, Ortner PB, Lean DRS. 1984. Night synthesis of protein by algae. Limnol. Oceanogr. 29:731–44 [Google Scholar]
  30. Dacey JWH, Wakeham SG. 1986. Oceanic dimethylsulfide—production during zooplankton grazing on phytoplankton. Science 233:1314–16 [Google Scholar]
  31. de Madariaga I. 2002. Short-term variations in the physiological state of phytoplankton in a shallow temperate estuary. Nutrients and Eutrophication in Estuaries and Coastal Waters E Orive, M Elliott, VN de Jonge 345–58 Dordrecht, Neth: Kluwer Acad. [Google Scholar]
  32. de Madariaga I, Joint I. 1992. A comparative study of physiological indicators. J. Exp. Mar. Biol. Ecol. 158:149–65 [Google Scholar]
  33. de Zwart JMM, Nelisse PN, Kuenen JG. 1996. Isolation and characterization of Methylophaga sulfidovorans sp. nov.: an obligately methylotrophic, aerobic, dimethylsulfide oxidizing bacterium from a microbial mat. FEMS Microbiol. Ecol. 20:261–70 [Google Scholar]
  34. Dixon JL, Beale R, Nightingale PD. 2011. Microbial methanol uptake in northeast Atlantic waters. ISME J. 5:704–16 [Google Scholar]
  35. Doty MS, Oguri M. 1957. Evidence for a photosynthetic daily periodicity. Limnol. Oceanogr. 2:37–40 [Google Scholar]
  36. Dring MJ, Jewson JH. 1982. What does the 14C uptake by phytoplankton really measure? A theoretical modeling approach. Proc. R. Soc. B 214:351–68 [Google Scholar]
  37. Fábregas J, Patiño M, Arredondo-Vega BO, Tobar JL, Otero A. 1995. Renewal rate and nutrient concentration as tools to modify productivity and biochemical composition of cyclostat cultures of the marine microalga Dunaliella tertiolecta. Appl. Microbiol. Biotechnol. 44:287–92 [Google Scholar]
  38. Fábregas J, Patiño M, Morales ED, Cordero B, Otero A. 1996. Optimal renewal rate and nutrient concentration for the production of the marine microalga Phaeodactylum tricornutum in semicontinuous cultures. Appl. Environ. Microbiol. 62:266–68 [Google Scholar]
  39. Falkowski PG. 1981. Effects of growth irradiance levels on the ratio of reaction centers in two species of marine phytoplankton. Plant Physiol. 68:969–73 [Google Scholar]
  40. Falkowski PG. 2000. Rationalizing elemental ratios in unicellular algae. J. Phycol. 36:3–6 [Google Scholar]
  41. Finazzi G. 2005. The central role of the green alga Chlamydomonas reinhardtii in revealing the mechanism of state transitions. J. Exp. Bot. 56:383–88 [Google Scholar]
  42. Flynn KJ. 2001. A mechanistic model for describing dynamic multi-nutrient, light, temperature interactions in phytoplankton. J. Plankton Res. 23:977–97 [Google Scholar]
  43. Follows MJ, Dutkiewicz S. 2011. Modeling diverse communities of marine microbes. Annu. Rev. Mar. Sci. 3:427–51 [Google Scholar]
  44. Foyer CH, Neukermans J, Queval G, Noctor G, Harbinson J. 2012. Photosynthetic control of electron transport and the regulation of gene expression. J. Exp. Bot. 63:1637–61 [Google Scholar]
  45. Foyer CH, Noctor G. 2000. Oxygen processing in photosynthesis: regulation and signalling. New Phytol. 146:359–88 [Google Scholar]
  46. Fraser JM, Tulk SE, Jeans JA, Campbell DA, Bibby TS, Cockshutt AM. 2013. Photophysiological and photosynthetic complex changes during iron starvation in Synechocystis sp. PCC 6803 and Synechococcus elongatus PCC 7942. PLoS ONE 8:e59861 [Google Scholar]
  47. Gao S, Shen SD, Wang GC, Niu JF, Lin AP, Pan GH. 2011. PSI-driven cyclic electron flow allows intertidal macro-algae Ulva sp. (Chlorophyta) to survive in desiccated conditions. Plant Cell Physiol. 52:885–93 [Google Scholar]
  48. Garczarek L, Partensky F, Irlbacher H, Holtzendorff J, Babin M. et al. 2001. Differential expression of antenna and core genes in Prochlorococcus PCC 9511 (Oxyphotobacteria) grown under a modulated light-dark cycle. Environ. Microbiol. 3:168–75 [Google Scholar]
  49. Gebser B, Pohnert G. 2013. Synchronized regulation of different zwitterionic metabolites in the osmoadaptation of phytoplankton. Mar. Drugs 11:2168–82 [Google Scholar]
  50. Geider RJ, La Roche J. 2002. Redfield revisited: variability of C:N:P in marine microalgae and its biochemical basis. Eur. J. Phycol. 37:1–17 [Google Scholar]
  51. Geider RJ, MacIntyre HL, Graziano LM, McKay RML. 1998a. Responses of the photosynthetic apparatus of Dunaliella tertiolecta (Chlorophyceae) to nitrogen and phosphorus limitation. Eur. J. Phycol. 33:315–32 [Google Scholar]
  52. Geider RJ, MacIntyre HL, Kana TM. 1997. Dynamic model of phytoplankton growth and acclimation: responses of the balanced growth rate and the chlorophyll a:carbon ratio to light, nutrient-limitation and temperature. Mar. Ecol. Prog. Ser. 148:187–200 [Google Scholar]
  53. Geider RJ, MacIntyre HL, Kana TM. 1998b. A dynamic regulatory model of phytoplankton acclimation to light, nutrients, and temperature. Limnol. Oceanogr. 43:679–94 [Google Scholar]
  54. Geider RJ, Moore CM, Ross ON. 2009. The role of cost-benefit analysis in models of phytoplankton growth and acclimation. Plant Ecol. Divers. 2:165–78 [Google Scholar]
  55. Geider RJ, Osborne BA. 1989. Respiration and microalgal growth: a review of the quantitative relationship between dark respiration and growth. New Phytol. 112:327–41 [Google Scholar]
  56. Glover H. 1977. Effects of iron deficiency on Isochrysis galbana (Chrysophyceae) and Phaeodactylum tricornutum (Bacillariophyceae). J. Phycol. 13:208–12 [Google Scholar]
  57. Goldman JC, Peavey DG. 1979. Steady-state growth and chemical composition of the marine chlorophyte Dunaliella tertiolecta in nitrogen-limited continuous cultures. Appl. Environ. Microbiol. 38:894–901 [Google Scholar]
  58. Graff JR, Milligan AJ, Behrenfeld MJ. 2012. The measurement of phytoplankton biomass using flow cytometric sorting and elemental analysis of carbon. Limnol. Oceanogr. Methods 10:910–20 [Google Scholar]
  59. Granum E, Kirkvold S, Myklestad SM. 2002. Cellular and extracellular production of carbohydrates and amino acids by the marine diatom Skeletonema costatum: diel variations and effects of N depletion. Mar. Ecol. Prog. Ser. 242:83–94 [Google Scholar]
  60. Griffiths MJ, Harrison STL. 2009. Lipid productivity as a key characteristic for choosing algal species for biodiesel production. J. Appl. Phycol. 21:493–507 [Google Scholar]
  61. Halsey KH, Carter AE, Giovannoni SJ. 2012. Synergistic metabolism of a broad range of C1 compounds in the marine methylotrophic bacterium HTCC2181. Environ. Microbiol. 14:630–40 [Google Scholar]
  62. Halsey KH, Milligan AJ, Behrenfeld MJ. 2010. Physiological optimization underlies growth rate-independent chlorophyll-specific gross and net primary production. Photosynth. Res. 103:125–37 [Google Scholar]
  63. Halsey KH, Milligan AJ, Behrenfeld MJ. 2011. Linking time-dependent carbon-fixation efficiencies in Dunaliella tertiolecta (Chlorophyceae) to underlying metabolic pathways. J. Phycol. 47:66–76 [Google Scholar]
  64. Halsey KH, Milligan AJ, Behrenfeld MJ. 2014. Contrasting strategies of photosynthetic energy utilization drive lifestyle strategies in ecologically important picoeukaryotes. Metabolites 4:260–80 [Google Scholar]
  65. Halsey KH, O'Malley RT, Graff JR, Milligan AJ, Behrenfeld MJ. 2013. A common partitioning strategy for photosynthetic products in evolutionarily distinct phytoplankton species. New Phytol. 198:1030–38 [Google Scholar]
  66. Harding LW, Prezelin BB, Sweeney BM, Cox JL. 1981. Diel oscillations in the photosynthesis-irradiance relationship of a planktonic marine diatom. J. Phycol. 17:389–94 [Google Scholar]
  67. Hellebust JA. 2000. Extracellular products. Dissolved Organic Carbon from Phytoplankton SM Myklestad 838–63 Berlin: Springer-Verlag [Google Scholar]
  68. Helman Y, Tchernov D, Reinhold L, Shibata M, Ogawa T. et al. 2003. Genes encoding A-type flavoproteins are essential for photoreduction of O2 in cyanobacteria. Curr. Biol. 13:230–35 [Google Scholar]
  69. Hendricks MB, Bender ML, Barnett BA, Strutton P, Chavez FP. 2005. Triple oxygen isotope composition of dissolved O2 in the equatorial Pacific: a tracer of mixing, production, and respiration. J. Geophys. Res. 110:C12021 [Google Scholar]
  70. Herbert SK, Samson G, Fork DC, Laudenbach DE. 1992. Characterization of damage to photosystems I and II in a cyanobacterium lacking detectable iron superoxide dismutase activity. Proc. Natl. Acad. Sci. USA 89:8716–20 [Google Scholar]
  71. Hoegh-Guldberg O. 2010. Dangerous shifts in ocean ecosystem function?. ISME J. 4:1090–92 [Google Scholar]
  72. Jacquet S, Partensky F, Lennon JF, Vaulot D. 2001. Diel patterns of growth and division in marine picoplankton in culture. J. Phycol. 37:357–69 [Google Scholar]
  73. Jakob T, Wagner H, Stehfest K, Wilhelm C. 2007. A complete energy balance from photons to new biomass reveals a light- and nutrient-dependent variability in the metabolic costs of carbon assimilation. J. Exp. Bot. 58:2101–12 [Google Scholar]
  74. Jebsen C, Norici A, Wagner H, Palmucci M, Giordano M, Wilhelm C. 2012. FTIR spectra of algal species can be used as physiological fingerprints to assess their actual growth potential. Physiol. Plant. 146:427–38 [Google Scholar]
  75. Jones RH, Flynn KJ. 2005. Nutritional status and diet composition affect the value of diatoms as copepod prey. Science 301:1457–58 [Google Scholar]
  76. Juranek LW, Quay PD. 2013. Using triple isotopes of dissolved oxygen to evaluate global marine productivity. Annu. Rev. Mar. Sci. 5:503–24 [Google Scholar]
  77. Karl DM, Björkman KM, Dore JE, Fujieki L, Hebel DV. et al. 2001. Ecological nitrogen-to-phosphorus stoichiometry at station ALOHA. Deep-Sea Res. II 48:1529–66 [Google Scholar]
  78. Kettle AJ, Andreae MO. 2000. Flux of dimethylsulfide from the oceans: a comparison of updated data sets and flux models. J. Geophys. Res. 105:26793–808 [Google Scholar]
  79. Klausmeier CA, Litchman E, Daufresne T, Levin SA. 2004. Optimal nitrogen-to-phosphorus stoichiometry of phytoplankton. Nature 429:171–74 [Google Scholar]
  80. Klein Breteler WCM, Schogt N, Rampen S. 2005. Effect of diatom nutrient limitation on copepod development: role of essential lipids. Mar. Ecol. Prog. Ser. 291:125–33 [Google Scholar]
  81. Kliphuis AMJ, Klok AJ, Martens DE, Lamers PP, Janssen M, Wijffels RH. 2012. Metabolic modeling of Chlamydomonas reinhardtii: energy requirements for photoautotrophic growth and maintenance. J. Appl. Phycol. 24:253–66 [Google Scholar]
  82. Kranz SA, Levitan O, Richter KU, Prasil O, Berman-Frank I, Rost B. 2010. Combined effects of CO2 and light on the N2-fixing cyanobacterium Trichodesmium IMS101: physiological responses. Plant Physiol. 154:334–45 [Google Scholar]
  83. Kromkamp JC, Forster RM. 2003. The use of variable fluorescence measurements in aquatic ecosystems: differences between multiple and single turnover measuring protocols and suggested terminology. Eur. J. Phycol. 38:103–12 [Google Scholar]
  84. Kroon BMA, Thoms S. 2006. From electron to biomass: a mechanistic model to describe phytoplankton photosynthesis and steady-state growth rates. J. Phycol. 42:593–609 [Google Scholar]
  85. Kruskopf M, Flynn KJ. 2006. Chlorophyll content and fluorescence responses cannot be used to gauge reliably phytoplankton biomass, nutrient status or growth rate. New Phytol. 169:525–36 [Google Scholar]
  86. Kunath C, Jakob T, Wilhelm C. 2012. Different phycobilin antenna organisations affect the balance between light use and growth rate in the cyanobacterium Microcystis aeruginosa and in the cryptophyte Cryptomonas ovata. Photosynth. Res. 111:173–83 [Google Scholar]
  87. Labiosa RG, Arrigo KR, Tu CJ, Bhaya D, Bay S. et al. 2006. Examination of diel changes in global transcript accumulation in Synechocystis (Cyanobacteria). J. Phycol. 42:622–36 [Google Scholar]
  88. Lacour T, Sciandra A, Talec A, Mayzaud P, Bernard O. 2010. Neutral lipid and carbohydrate productivities as a response to nitrogen status in Isochrysis sp. (T-ISO; Haptophyceae): starvation versus limitation. J. Phycol. 48:647–56 [Google Scholar]
  89. Lancelot C, Mathot S. 1985. Biochemical fractionation of primary production by phytoplankton in Belgian coastal waters during short- and long-term incubations with 14C-bicarbonate: I. Mixed diatom population. Mar. Biol. 86:219–26 [Google Scholar]
  90. Laws EA. 1991. Photosynthetic quotients, new production and net community production in the open ocean. Deep-Sea Res. I 38:143–67 [Google Scholar]
  91. Laws EA, Bannister TT. 1980. Nutrient- and light-limited growth of Thalassiosira fluviatilis in continuous culture, with implications for phytoplankton growth in the ocean. Limnol. Oceanogr. 25:457–73 [Google Scholar]
  92. Leboulanger C, Martin-Jezequel V, Descolas-Gros C, Sciandra A, Jupin HJ. 1998. Photorespiration in continuous culture of Dunaliella teriolecta (Chlorophyta): relationships between serine, glycine, and extracellular glycolate. J. Phycol. 34:651–54 [Google Scholar]
  93. Lenton TM, Watson AJ. 2000. Redfield revisited: I. Regulation of nitrate, phosphate and oxygen in the ocean. Glob. Biogeochem. Cycles 14:225–48 [Google Scholar]
  94. Li WKW, Harrison WG. 1982. Carbon flow into the end-products of photosynthesis in short and long incubations of a natural phytoplankton population. Mar. Biol. 72:175–82 [Google Scholar]
  95. Litchman E, Klausmeier CA. 2008. Trait-based community ecology of phytoplankton. Annu. Rev. Ecol. Evol. Syst. 39:615–39 [Google Scholar]
  96. Lomas MW, Glibert PM. 2000. Comparisons of nitrate uptake, storage, and reduction in marine diatoms and flagellates. J. Phycol. 36:903–13 [Google Scholar]
  97. Lomas MW, Rumbley CJ, Glibert PM. 2000. Ammonium release by nitrogen sufficient diatoms in response to rapid increases in irradiance. J. Plankton Res. 22:2351–66 [Google Scholar]
  98. Luz B, Barkan E. 2000. Assessment of oceanic productivity with the triple-isotope composition of dissolved oxygen. Science 288:2028–31 [Google Scholar]
  99. Luz B, Barkan E. 2005. The isotopic ratios 17O/16O and 18O/16O in molecular oxygen and their significance in biogeochemistry. Geochim. Cosmochim. Acta 69:1099–110 [Google Scholar]
  100. MacIntyre HL, Cullen JJ. 2005. Using cultures to investigate the physiological ecology of microalgae. Algal Culturing Techniques RA Andersen 287–326 Amsterdam: Elsevier [Google Scholar]
  101. Mackey KRM, Paytan A, Grossman AR, Bailey S. 2008. A photosynthetic strategy for coping in a high-light, low nutrient environment. Limnol. Oceanogr. 53:900–13 [Google Scholar]
  102. Malin G, Wilson WH, Bratbak G, Liss PS, Mann NH. 1998. Elevated production of dimethylsulfide resulting from viral infection of cultures of Phaeocystis pouchetii. Limnol. Oceanogr. 43:1389–93 [Google Scholar]
  103. Marra J. 2002. Approaches to the measurement of plankton productivity. Phytoplankton Productivity: Carbon Assimilation in Marine and Freshwater Ecosystems PJLB Williams, DN Thomas, CS Reynolds 78–108 Oxford, UK: Blackwell Sci. [Google Scholar]
  104. Matsumura K, Yagi T, Hattori A, Soloviev M, Yasuda K. 2010. Using single cell cultivation system for on-chip monitoring of the interdivision timer in Chlamydomonas reinhardtii cell cycle. J. Nanobiotechnol. 8:23 [Google Scholar]
  105. Mehler AH. 1957. Studies on reactions of illuminated chloroplasts: I. Mechanism of the reduction of oxygen and other Hill reagents. Arch. Biochem. Biophys. 33:65–77 [Google Scholar]
  106. Meng Y, Yao C, Xue S, Yang H. 2014. Application of Fourier transform infrared (FT-IR) spectroscopy in determination of microalgal compositions. Bioresour. Technol. 151:347–54 [Google Scholar]
  107. Michaels AF, Karl DM, Capone DG. 2001. Elemental stoichiometry, new production, and nitrogen fixation. Oceanography 14:468–77 [Google Scholar]
  108. Milligan AJ, Berman-Frank I, Gerchman Y, Dismukes GC, Falkowski PG. 2007. Light-dependent oxygen consumption in nitrogen-fixing cyanobacteria plays a key role in nitrogenase protection. J. Phycol. 43:845–52 [Google Scholar]
  109. Mills MM, Arrigo K. 2010. Magnitude of oceanic nitrogen fixation influenced by the nutrient uptake ratio of phytoplankton. Nat. Geosci. 3:412–16 [Google Scholar]
  110. Minkevich IG, Fursova PV, Tjorlova LD, Tsygankov AA, Riznichenko GY. 2013. The stoichiometry and energetics of oxygenic phototrophic growth. Photosynth. Res. 116:55–78 [Google Scholar]
  111. Miyake C. 2010. Alternative electron flows (water-water cycle and cyclic electron flow around PSI) in photosynthesis: molecular mechanisms and physiological functions. Plant Cell Physiol. 51:1951–63 [Google Scholar]
  112. Miyake C, Asada K. 2003. The water-water cycle in algae. Photosynthesis in Algae AWD Larkum, SE Douglas, JA Raven 183–204 Dordrecht, Neth: Kluwer Acad. [Google Scholar]
  113. Moore LR, Goericke RE, Chisholm SW. 1995. Comparative physiology of Synechococcus and Prochlorococcus: influence of light and temperature on growth, pigments, fluorescence and absorptive properties. Mar. Ecol. Prog. Ser. 116:259–75 [Google Scholar]
  114. Morris I. 1980. Paths of carbon assimilation in marine phytoplankton. Primary Productivity in the Sea PG Falkowski 139–59 New York: Plenum [Google Scholar]
  115. Morris I, Glover HE, Yentsch CS. 1974. Products of photosynthesis by marine phytoplankton: the effect of environmental factors on the relative rates of protein synthesis. Mar. Biol. 27:1–9 [Google Scholar]
  116. Moseley JL, Alinger T, Herzong S, Hoerth P, Wehinger E. et al. 2002. Adaptation to Fe-deficiency requires remodeling of the photosynthetic apparatus. EMBO J. 21:6709–20 [Google Scholar]
  117. Myklestad SM. 1974. Production of carbohydrates by marine planktonic diatoms. I. Composition of nine different species in culture. J. Exp. Mar. Biol. Ecol. 15:261–74 [Google Scholar]
  118. Myklestad SM. 2000. Dissolved organic carbon from phytoplankton. The Handbook of Environmental Chemistry P Wangersky 111–48 Berlin: Springer-Verlag [Google Scholar]
  119. Neufeld JD, Schafer H, Cox MJ, Boden R, McDonald IR, Murrell JC. 2007. Stable-isotope probing implicates Methylophaga spp and novel Gammaproteobacteria in marine methanol and methylamine metabolism. ISME J. 1:480–91 [Google Scholar]
  120. Nogales J, Gudmundsson S, Knight EM, Palsson BO, Thiele I. 2012. Detailing the optimality of photosynthesis in cyanobacteria through systems biology analysis. Proc. Natl. Acad. Sci. USA 109:2678–83 [Google Scholar]
  121. Otero A, Fábregas J. 1997. Changes in the nutrient composition of Tetraselmis suecica cultured semicontinuously with different nutrient concentrations and renewal rates. Aquaculture 159:111–23 [Google Scholar]
  122. Parkhill J-P, Maillet G, Cullen JJ. 2001. Fluorescence-based maximal quantum yield for PSII as a diagnostic of nutrient stress. J. Phycol. 37:517–29 [Google Scholar]
  123. Paul C, Pohnert G. 2011. Production and role of volatile halogenated compounds from marine algae. Nat. Prod. Rep. 28:186–95 [Google Scholar]
  124. Pei S, Laws EA. 2013. Does the 14C method estimate net photosynthesis? Implications from batch and continuous culture studies of marine phytoplankton. Deep-Sea Res. I 82:1–9 [Google Scholar]
  125. Pichard SL, Campbell L, Kang JB, Tabita FR, Paul JH. 1996. Regulation of ribulose bisphosphate carboxylase gene expression in natural phytoplankton communities. I. Diel rhythms. Mar. Ecol. Prog. Ser. 139:257–65 [Google Scholar]
  126. Prezelin BB. 1992. Diel periodicity in phytoplankton productivity. Hydrobiologia 238:1–35 [Google Scholar]
  127. Raghavendra AS, Padmasree K. 2003. Beneficial interactions of mitochondrial metabolism with photosynthetic carbon assimilation. Trends Plant Sci. 8:546–53 [Google Scholar]
  128. Raven JA. 1972. Endogenous inorganic carbon sources in plant photosynthesis: I. Occurrence of the dark respiratory pathways in illuminated green cells. New Phytol. 71:227–41 [Google Scholar]
  129. Reinfelder JR. 2011. Carbon concentrating mechanisms in eukaryotic marine phytoplankton. Annu. Rev. Mar. Sci. 3:291–315 [Google Scholar]
  130. Richards SR, Rudd JWM, Kelly CA. 1994. Organic volatile sulfur in lakes ranging in sulfate and dissolved salt concentration over five orders of magnitude. Limnol. Oceanogr. 39:562–72 [Google Scholar]
  131. Richardson AD, Carbone MS, Keenan TF, Czimczik CI, Hollinger DY. et al. 2013. Seasonal dynamics and age of stemwood nonstructural carbohydrates in temperate forest trees. New Phytol. 197:850–61 [Google Scholar]
  132. Richardson B, Orcutt DM, Schwertner HA, Martinez CL. 1969. Effects of nitrogen limitation on the growth and composition of unicellular algae in continuous culture. Appl. Microbiol. 18:245–50 [Google Scholar]
  133. Rosenwasser S, van Creveld SG, Schatz D, Malitsky S, Tzfadia O. et al. 2014. Mapping the diatom redox-sensitive proteome provides insight into response to nitrogen stress in the marine environment. Proc. Natl. Acad. Sci. USA. 111:2740–45 [Google Scholar]
  134. Ryther JH. 1954. The ratio of photosynthesis to respiration in marine plankton algae and its effect upon the measurement of productivity. Deep-Sea Res. 2:134–39 [Google Scholar]
  135. Satoh K, Fork DC. 1983. The relationship between state II to state I transitions and cyclic electron flow around photosystem I. Photosynth. Res. 4:245–56 [Google Scholar]
  136. Schafer H. 2007. Isolation of Methylophaga spp. from marine dimethylsulfide-degrading enrichment cultures and identification of polypeptides induced during growth on dimethylsulfide. Appl. Environ. Microbiol. 73:2580–91 [Google Scholar]
  137. Scheibe R. 2004. Malate valves to balance cellular energy supply. Physiol. Plant. 120:21–26 [Google Scholar]
  138. Schrader PS, Milligan AJ, Behrenfeld MJ. 2011. Surplus photosynthetic antennae complexes underlie diagnostics of iron limitation in a cyanobacterium. PLoS ONE 6:e18753 [Google Scholar]
  139. Schreiber U, Endo T, Mi H, Asada K. 1995. Quenching analysis of chlorophyll fluorescence by the saturation pulse method: particular aspects relating to the study of eukaryotic algae and cyanobacteria. Plant Cell Physiol. 36:873–82 [Google Scholar]
  140. Shifrin NS, Chisholm SW. 1981. Phytoplankton lipids: interspecific differences and effects of nitrate, silicate and light-dark cycles. J. Phycol. 17:374–84 [Google Scholar]
  141. Shuter B. 1979. A model of physiological adaptation in unicellular algae. J. Theor. Biol. 78:519–52 [Google Scholar]
  142. Siegel DA, Behrenfeld MJ, Maritorena S, McClain CR, Antoine D. et al. 2013. Regional to global assessments of phytoplankton dynamics from the SeaWiFS mission. Remote Sens. Environ. 135:77–91 [Google Scholar]
  143. Six C, Finkel ZV, Rodriguez F, Marie D, Partensky F, Campbell DA. 2008. Contrasting photoacclimation costs in ecotypes of the marine eukaryotic picoplankter Ostreococcus. Limnol. Oceanogr. 53:255–65 [Google Scholar]
  144. Smith REH, D'Souza FML. 1993. Macromolecular labelling patterns and inorganic nutrient limitation of a North Atlantic spring bloom. Mar. Ecol. Prog. Ser. 92:111–18 [Google Scholar]
  145. Smith REH, Geider RJ. 1985. Kinetics of intracellular carbon allocation in a marine diatom. J. Exp. Mar. Biol. Ecol. 93:191–210 [Google Scholar]
  146. Smith REH, Platt T. 1984. Carbon exchange and 14C tracer methods in a nitrogen-limited diatom, Thalassiosira pseudonana. Mar. Ecol. Prog. Ser. 16:75–87 [Google Scholar]
  147. Solomon S, Garcia RR, Ravishankara AR. 1994. On the role of iodine in ozone depletion. J. Geophys. Res. 99:20491–500 [Google Scholar]
  148. Søndergaard M. 2002. A biography of Einer Steemann Nielsen: the man and his science. Phytoplankton Productivity: Carbon Assimilation in Marine and Freshwater Ecosystems PJLB Williams, DN Thomas, CS Reynolds 1–15 Oxford, UK: Blackwell Sci. [Google Scholar]
  149. Sorribas A, Poso C, Vilaprinyo E, Guillén-Gosálbez G, Jiménez L, Alves R. 2010. Optimization and evolution in metabolic pathways: global optimization techniques in generalized mass action models. J. Biotechnol. 149:141–53 [Google Scholar]
  150. Spoehr HA, Milner HW. 1949. The chemical composition of Chlorella; effect of environmental conditions. Plant Physiol. 24:120–49 [Google Scholar]
  151. Steemann Nielsen E. 1952. The use of radioactive carbon (14C) for measuring organic production in the sea. J. Cons. Int. Explor. Mer 18:117–40 [Google Scholar]
  152. Steemann Nielsen E. 1955. The interaction of photosynthesis and respiration and its importance for the determination of 14C discrimination in photosynthesis. Physiol. Plant. 8:945–53 [Google Scholar]
  153. Steemann Nielsen E, Jensen AE. 1957. Primary oceanic production: the autotrophic production of organic matter in the oceans. Galathea Rep. 1:49–136 [Google Scholar]
  154. Steuer R. 2007. Computational approaches to the topology, stability and dynamics of metabolic networks. Phytochemistry 68:2139–51 [Google Scholar]
  155. Sukenik A, Livne A. 1991. Variations in lipid and fatty-acid content in relation to acetyl CoA carboxylase in the marine prymnesiophyte Isochrysis galbana. Plant Cell Physiol. 32:371–78 [Google Scholar]
  156. Sun J, Steindler L, Thrash JC, Halsey KH, Smith DP. et al. 2011. One carbon metabolism in SAR11 pelagic marine bacteria. PLoS ONE 6:e23973 [Google Scholar]
  157. Takahashi H, Clowez S, Wollman FA, Vallon O, Rappaport F. 2013. Cyclic electron flow is redox-controlled but independent of state transition. Nat. Commun. 4:1954 [Google Scholar]
  158. Talmy D, Blackford J, Hardman-Mountford NJ, Dumbrell AJ, Geider RJ. 2013. An optimality model of photoadaptation in contrasting aquatic light regimes. Limnol. Oceanogr. 58:1802–18 [Google Scholar]
  159. Taub FB, Dollar AM. 1965. Control of protein level of algae, Chlorella. J. Food Sci. 30:359–64 [Google Scholar]
  160. Taylor JR, Stocker R. 2012. Trade-offs of chemotactic foraging in turbulent water. Science 338:675–79 [Google Scholar]
  161. Temperton B, Giovannoni SJ. 2012. Metagenomics: microbial diversity through a scratched lens. Curr. Opin. Microbiol. 15:605–12 [Google Scholar]
  162. Treusch AH, Demir-Hilton E, Vergin KL, Worden AZ, Carlson CA. et al. 2012. Phytoplankton distribution patterns in the northwestern Sargasso Sea revealed by small subunit rRNA genes from plastids. ISME J. 6:481–92 [Google Scholar]
  163. Vaulot D. 1995. The cell cycle of phytoplankton: coupling cell growth to population growth. Molecular Ecology of Aquatic Microbes I Joint 303–22 Berlin: Springer-Verlag [Google Scholar]
  164. Vaulot D, Marie D. 1999. Diel variability of phyotosynthetic picoplankton in the equatorial Pacific. J. Geophys. Res. 104:3297–310 [Google Scholar]
  165. Vergin K, Beszteri B, Monier A, Thrash JC, Temperton B. et al. 2013. High-resolution SAR11 ecotype dynamics at the Bermuda Atlantic Time-series Study site by phylogenetic placement of pyrosequences. ISME J. 7:1322–32 [Google Scholar]
  166. Wagner H, Jakob T, Wilhelm C. 2006. Balancing the energy flow from captured light to biomass under fluctuating light conditions. New Phytol. 169:95–108 [Google Scholar]
  167. Wagner H, Liu Z, Langner U, Stehfest K, Wilhelm C. 2010. The use of FTIR spectroscopy to assess quantitative changes in the biochemical composition of microalgae. J. Biophoton. 3:557–66 [Google Scholar]
  168. Westberry TK, Behrenfeld MJ, Siegel DA, Boss ES. 2008. Carbon-based primary productivity modeling with vertically resolved photoacclimation. Glob. Biogeochem. Cycles 22:GB2024 [Google Scholar]
  169. Westberry TK, Williams PJLB, Behrenfeld MJ. 2012. Global net community production and the putative net heterotrophy of the oligotrophic oceans. Glob. Biogeochem. Cycles 26:GB4019 [Google Scholar]
  170. Wetz MS, Wheeler PA. 2003. Production and partitioning of organic matter during simulated phytoplankton blooms. Limnol. Oceanogr. 48:1808–17 [Google Scholar]
  171. Wilhelm C, Buchel C, Fisahn J, Goss R, Jakob T. et al. 2006. The regulation of carbon and nutrient assimilation in diatoms is significantly different from green algae. Protist 157:91–124 [Google Scholar]
  172. Wilhelm C, Jakob T. 2011. From photons to biomass and biofuels: evaluation of different strategies for the improvement of algal biotechnology based on comparative energy balances. Appl. Microbiol. Biotechnol. 92:909–19 [Google Scholar]
  173. Williams PJLB, Robertson JE. 1991. Overall planktonic oxygen and carbon dioxide metabolisms: the problem of reconciling observations and calculations of photosynthetic quotients. J. Plankton Res. 13:Suppl. 1153–69 [Google Scholar]
  174. Wolfe GV, Steinke M. 1996. Grazing-activated production of dimethyl sulfide (DMS) by two clones of Emiliania huxleyi. Limnol. Oceanogr. 41:1151–60 [Google Scholar]
  175. Worden AZ, Lee J-H, Mock T, Rouzé P, Simmons MP. et al. 2009. Green evolution and dynamic adaptations revealed by genomes of the marine picoeukaryotes Micromonas. Science 324:268–72 [Google Scholar]
  176. Zinser ER, Lindell D, Johnson ZI, Futschik ME, Steglich C. et al. 2009. Choreography of the transcriptome, photophysiology, and cell cycle of a minimal photoautotroph, Prochlorococcus. PLoS ONE 4:1–18 [Google Scholar]
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Phytoplankton Strategies for Photosynthetic Energy Allocation
Annual Review of Marine Science 7, 265 (2015); https://doi.org/10.1146/annurev-marine-010814-015813
/content/journals/10.1146/annurev-marine-010814-015813
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