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Abstract

Coccolithophores occupy a special position within the marine phytoplankton because of their production of intricate calcite scales, or coccoliths. Coccolithophores are major contributors to global ocean calcification and long-term carbon fluxes. The intracellular production of coccoliths requires modifications to cellular ultrastructure and metabolism that are surveyed here. In addition to calcification, which appears to have evolved with a diverse range of functions, several other remarkable features that likely underpin the ecological and evolutionary success of coccolithophores have recently been uncovered. These include complex and varied life cycle strategies related to abiotic and biotic interactions as well as a range of novel metabolic pathways and nutritional strategies. Together with knowledge of coccolithophore genetic and physiological variability, these findings are beginning to shed new light on species diversity, distribution, and ecological adaptation. Further advances in genetics and functional characterization at the cellular level will likely to lead to a rapid increase in this understanding.

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2017-01-03
2024-03-28
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Literature Cited

  1. Alcolombri U, Ben-Dor S, Feldmesser E, Levin Y, Tawfik DS, Vardi A. 2015. Identification of the algal dimethyl sulfide-releasing enzyme: a missing link in the marine sulfur cycle. Science 348:1466–69 [Google Scholar]
  2. Bach LT, Mackinder LCM, Schulz KG, Wheeler G, Schroeder DC. et al. 2013. Dissecting the impact of CO2 and pH on the mechanisms of photosynthesis and calcification in the coccolithophore Emiliania huxleyi. New Phytol. 199:121–34 [Google Scholar]
  3. Balch W, Drapeau D, Bowler B, Booth E. 2007. Prediction of pelagic calcification rates using satellite measurements. Deep-Sea Res. II 54:478–95 [Google Scholar]
  4. Bartal R, Shi BY, Cochlan WP, Carpenter EJ. 2015. A model system elucidating calcification functions in the prymnesiophyte Emiliania huxleyi reveals dependence of nitrate acquisition on coccoliths. Limnol. Oceanogr. 60:149–58 [Google Scholar]
  5. Bendif E, Probert I, Young JR, von Dassow P. 2015. Morphological and phylogenetic characterization of new Gephyrocapsa isolates suggests introgressive hybridization in the Emiliania/Gephyrocapsa complex (Haptophyta). Protist 166:323–36 [Google Scholar]
  6. Berry L, Taylor AR, Lucken U, Ryan KP, Brownlee C. 2002. Calcification and inorganic carbon acquisition in coccolithophores. Funct. Plant. Biol. 29:289–99 [Google Scholar]
  7. Bidle KD, Haramaty L, Barcelos ERJ, Falkowski P. 2007. Viral activation and recruitment of metacaspases in the unicellular coccolithophore, Emiliania huxleyi. PNAS 104:6049–54 [Google Scholar]
  8. Boeckel B, Baumann K-H. 2008. Vertical and lateral variations in coccolithophore community structure across the subtropical frontal zone in the South Atlantic Ocean. Mar. Micropaleontol. 67:255–73 [Google Scholar]
  9. Borman AH, Dejong EW, Huizinga M, Kok DJ, Westbroek P, Bosch L. 1982. The role in CaCO3 crystallization of an acid Ca2+-binding polysaccharide associated with coccoliths of Emiliania huxleyi. Eur. J. Biochem. 129:179–83 [Google Scholar]
  10. Brownlee C, Taylor AR. 2004. Calcification in coccolithophores: a cellular perspective. See Thierstein & Young 2004 31–49
  11. Brownlee C, Wheeler GL, Taylor AR. 2015. Coccolithophore biomineralization: new questions, new answers. Semin. Cell Dev. Biol. 46:11–16 [Google Scholar]
  12. Brun P, Vogt M, Payne MR, Gruber N, O'Brien CJ. et al. 2015. Ecological niches of open ocean phytoplankton taxa. Limnol. Oceanogr. 60:1020–38 [Google Scholar]
  13. Burki F, Kaplan M, Tikhonenkov DV, Zlatogursky V, Minh BQ. et al. 2016. Untangling the early diversification of eukaryotes: a phylogenomic study of the evolutionary origins of Centrohelida, Haptophyta and Cryptista. Proc. R. Soc. B 283:20152802 [Google Scholar]
  14. Chow JS, Lee C, Engel A. 2015. The influence of extracellular polysaccharides, growth rate, and free coccoliths on the coagulation efficiency of Emiliania huxleyi. Mar. Chem. 175:5–17 [Google Scholar]
  15. Conte MH, Thompson A, Eglinton G, Green JC. 1995. Lipid biomarker diversity in the coccolithophorid Emiliania huxleyi (Prymnesiophyceae) and related species Gephyrocapsa oceanica. J. Phycol. 31:272–82 [Google Scholar]
  16. Cooper MB, Smith AG. 2015. Exploring mutualistic interactions between microalgae and bacteria in the omics age. Curr. Opin. Plant. Biol. 26:147–53 [Google Scholar]
  17. Corstjens PLAM, Araki Y, González EL. 2001. A coccolithophorid calcifying vesicle with a vacuolar-type ATPase proton pump: cloning and immunolocalization of the V0 subunit c. J. Phycol. 37:71–78 [Google Scholar]
  18. Corstjens PLAM, Van Der Kooij A, Linschooten C, Brouwers GJ, Westbroek P, de Vrind-de Jong EW. 1998. GPA, a calcium-binding protein in the coccolithophorid Emiliania huxleyi (Prymnesiophyceae). J. Phycol. 34:622–30 [Google Scholar]
  19. Cros L, Estrada M. 2013. Holo-heterococcolithophore life cycles: ecological implications. Mar. Ecol. Prog. Ser. 492:57–68 [Google Scholar]
  20. Cros L, Kleijne A, Zeltner A, Billard C, Young JR. 2000. New examples of holococcolith-heterococcolith combination coccospheres and their implications for coccolithophorid biology. Mar. Micropaleontol. 39:1–34 [Google Scholar]
  21. Daniels CJ, Sheward RM, Poulton AJ. 2014. Biogeochemical implications of comparative growth rates of Emiliania huxleyi and Coccolithus species. Biogeosciences. 116915–25
  22. Danne JC, Gornik SG, Macrae JI, McConville MJ, Waller RF. 2013. Alveolate mitochondrial metabolic evolution: dinoflagellates force reassessment of the role of parasitism as a driver of change in apicomplexans. Mol. Biol. Evol. 30:123–39 [Google Scholar]
  23. Darroch LJ, Lavoie M, Levasseur M, Laurion I, Sunda WG. et al. 2015. Effect of short-term light- and UV-stress on DMSP, DMS, and DMSP lyase activity in Emiliania huxleyi. Aquat. Microb. Ecol. 74:173–85 [Google Scholar]
  24. De Vargas C, Aubry M-P, Probert I, Young JR. 2007. Origin and evolution of coccolithophores: from coastal hunters to oceanic farmers. The Evolution of Aquatic Photoautotrophs PG Falkowski, AH Knoll 251–85 New York: Academic [Google Scholar]
  25. Drescher B, Dillaman RM, Taylor AR. 2012. Calcification in the coccolithophore Scyphosphaera apsteinii (Prymnesiophycae). J. Phycol. 48:1343–61 [Google Scholar]
  26. Durak GM, Taylor AR, Walker CE, Probert I, de Vargas C. et al. 2016. A role for diatom-like silicon transporters in calcifying coccolithophores. Nat. Commun. 7:10543 [Google Scholar]
  27. Evans C, Malin G, Mills GP, Wilson WH. 2006. Viral infection of Emiliania huxleyi (Prymnesiophyceae) leads to elevated production of reactive oxygen species. J. Phycol. 42:1040–47 [Google Scholar]
  28. Fichtinger-Schepman AMJ, Kamperling JP, Versluis C, Vliegenthart JFG. 1981. Structural studies of the methylated, acid polysaccharides associated with coccoliths of Emiliania huxleyi (Lohmann) Kamptner. Carbohydr. Res. 93:105–23 [Google Scholar]
  29. Follows MJ, Dutkiewicz S. 2011. Modeling diverse communities of marine microbes. Annu. Rev. Mar. Sci. 3:427–51 [Google Scholar]
  30. Frada MJ, Bidle KD, Probert I, de Vargas C. 2012. In situ survey of life cycle phases of the coccolithophore Emiliania huxleyi (Haptophyta). Environ. Microbiol. 14:1558–69 [Google Scholar]
  31. Frada MJ, Percopo I, Young J, Zingone A, de Vargas C, Probert I. 2009. First observations of heterococcolithophore–holococcolithophore life cycle combinations in the family Pontosphaeraceae (Calcihaptophycideae, Haptophyta). Mar. Micropaleontol. 71:20–27 [Google Scholar]
  32. Frada MJ, Probert I, Allen MJ, Wilson WH, de Vargas C. 2008. The “Cheshire Cat” escape strategy of the coccolithophore Emiliania huxleyi in response to viral infection. PNAS 105:15944–49 [Google Scholar]
  33. Frada MJ, Vardi A. 2015. Algal viruses hitchhiking on zooplankton across phytoplankton blooms. Commun. Integr. Biol. 8:e1029210 [Google Scholar]
  34. Franklin DJ, Steinke M, Young J, Probert I, Malin G. 2010. Dimethylsulphoniopropionate (DMSP), DMSP-lyase activity (DLA) and dimethylsulphide (DMS) in 10 species of coccolithophore. Mar. Ecol. Prog. Ser. 410:13–23 [Google Scholar]
  35. Fredrickson KA, Strom SL. 2009. The algal osmolyte DMSP as a microzooplankton grazing deterrent in laboratory and field studies. J. Plankton Res. 31:135–52 [Google Scholar]
  36. Fresnel J. 1994. A heteromorphic life cycle in two coastal coccolithophorids, Hymenomonas lacuna and Hymenomonas coronata (Prymnesiophyceae). Can. J. Bot. 72:1455–62 [Google Scholar]
  37. Fulton JM, Fredricks HF, Bidle KD, Vardi A, Kendrick BJ. et al. 2014. Novel molecular determinants of viral susceptibility and resistance in the lipidome of Emiliania huxleyi. Environ. Microbiol. 16:1137–49 [Google Scholar]
  38. Garren M, Son K, Raina JB, Rusconi R, Menolascina F. et al. 2014. A bacterial pathogen uses dimethylsulfoniopropionate as a cue to target heat-stressed corals. ISME J 8:999–1007 [Google Scholar]
  39. Gebser B, Pohnert G. 2013. Synchronized regulation of different zwitterionic metabolites in the osmoadaption of phytoplankton. Mar. Drugs 11:2168–82 [Google Scholar]
  40. Geisen M, Billard C, Broerse A, Cros L, Probert I, Young J. 2002. Life-cycle associations involving pairs of holococcolithophorid species: intraspecific variation or cryptic speciation. Eur. J. Phycol. 37:531–50 [Google Scholar]
  41. Green DH, Echavarri-Bravo V, Brennan D, Hart MC. 2015. Bacterial diversity associated with the coccolithophorid algae Emilianiahuxleyi and Coccolithus pelagicus f. braarudii. BioMed Res. Int. 2015:194540 [Google Scholar]
  42. Hagino K, Tomioka N, Young JR, Takano Y, Onuma R, Horiguchi T. 2016. Extracellular calcification of Braarudosphaera bigelowii deduced from electron microscopic observations of cell surface structure and elemental composition of pentaliths. Mar. Micropaleontol. 125:85–94 [Google Scholar]
  43. Harris RP. 1994. Zooplankton grazing on the coccolithophore Emiliania huxleyi and its role in inorganic carbon flux. Mar. Biol. 119:431–39 [Google Scholar]
  44. Hartmann M, Grob C, Tarran GA, Martin AP, Burkill PH. et al. 2012. Mixotrophic basis of Atlantic oligotrophic ecosystems. PNAS 109:5756–60 [Google Scholar]
  45. Harvey EL, Bidle KD, Johnson MD. 2015. Consequences of strain variability and calcification in Emiliania huxleyi on microzooplankton grazing. J. Plankton Res. 37:1137–48 [Google Scholar]
  46. Harvey EL, Deering RW, Rowley DC, El Gamal A, Schorn M. et al. 2016. A bacterial quorum-sensing precursor induces mortality in the marine coccolithophore. Emiliania huxleyi. Front. Microbiol. 7:59 [Google Scholar]
  47. Hassenkam T, Johnsson A, Bechgaard K, Stipp SLS. 2011. Tracking single coccolith dissolution with picogram resolution and implications for CO2 sequestration and ocean acidification. PNAS 108:8571–76 [Google Scholar]
  48. Henriksen K, Stipp SLS. 2009. Controlling biomineralization: the effect of solution composition on coccolith polysaccharide functionality. Cryst. Growth Des. 9:2088–97 [Google Scholar]
  49. Henriksen K, Stipp SLS, Young JR, Marsh ME. 2004. Biological control on calcite crystallization: AFM investigation of coccolith polysaccharide function. Am. Mineral. 89:1709–16 [Google Scholar]
  50. Herfort L, Loste E, Meldrum F, Thake B. 2004. Structural and physiological effects of calcium and magnesium in Emiliania huxleyi (Lohmann) Hay and Mohler. J. Struct. Biol. 148:307–14 [Google Scholar]
  51. Hermoso M. 2014. Coccolith-derived isotopic proxies in palaeoceanography: where geologists need biologists. Cryptogamie Algol 35:323–51 [Google Scholar]
  52. Hirokawa Y, Fujiwara S, Tsuzuki M. 2005. Three types of acidic polysaccharides associated with coccolith of Pleurochrysis haptonemofera: comparison with Pleurochrysis carterae and analysis using fluorescein-isothiocyanate-labeled lectins. Mar. Biotechnol. 7:634–44 [Google Scholar]
  53. Holtz L-M, Thoms S, Langer G, Wolf-Gladrow DA. 2013. Substrate supply for calcite precipitation in Emiliania huxleyi: assessment of different model approaches. J. Phycol. 49:417–26 [Google Scholar]
  54. Houdan A, Billard C, Marie D, Not F, Sáez AG. et al. 2004. Holococcolithophore-heterococcolithophore (Haptophyta) life cycles: flow cytometric analysis of relative ploidy levels. Syst. Biodivers. 1:453–65 [Google Scholar]
  55. Houdan A, Probert I, Van Lenning K, Lefebvre S. 2005. Comparison of photosynthetic responses in diploid and haploid life-cycle phases of Emiliania huxleyi (Prymnesiophyceae). Mar. Ecol. Prog. Ser. 292:139–46 [Google Scholar]
  56. Houdan A, Probert I, Zatylny C, Veron B, Billard C. 2006. Ecology of oceanic coccolithophores. I. Nutritional preferences of the two stages in the life cycle of Coccolithusbraarudii and Calcidiscus leptoporus. Aquat. Microb. Ecol. 44:291–301 [Google Scholar]
  57. Hunter JE, Frada MJ, Fredricks HF, Vardi A, Van Mooy BAS. 2015. Targeted and untargeted lipidomics of Emiliania huxleyi viral infection and life cycle phases highlights molecular biomarkers of infection, susceptibility, and ploidy. Front. Mar. Sci. 2:81 [Google Scholar]
  58. Ihli J, Wong WC, Noel EH, Kim YY, Kulak AN. et al. 2014. Dehydration and crystallization of amorphous calcium carbonate in solution and in air. Nat. Commun. 5:3169 [Google Scholar]
  59. Kayano K, Saruwatari K, Kogure T, Shiraiwa Y. 2011. Effect of coccolith polysaccharides isolated from the coccolithophorid, Emiliania huxleyi, on calcite crystal formation in in vitro CaCO3 crystallization. Mar. Biotechnol. 13:83–92 [Google Scholar]
  60. Kayano K, Shiraiwa Y. 2009. Physiological regulation of coccolith polysaccharide production by phosphate availability in the coccolithophorid Emiliania huxleyi. Plant Cell Physiol 50:1522–31 [Google Scholar]
  61. Keller MD, Kiene RP, Matrai PA, Bellows WK. 1999. Production of glycine betaine and dimethylsulfoniopropionate in marine phytoplankton. II. N-limited chemostat cultures. Mar. Biol. 135:249–57 [Google Scholar]
  62. Kellermeier M, Melero-García E, Glaab F, Klein R, Drechsler M. et al. 2010. Stabilization of amorphous calcium carbonate in inorganic silica-rich environments. J. Am. Chem. Soc. 132:17859–66 [Google Scholar]
  63. Kinkel H, Baumann KH, Cepek M. 2000. Coccolithophores in the equatorial Atlantic Ocean: response to seasonal and Late Quaternary surface water variability. Mar. Micropaleontol. 39:87–112 [Google Scholar]
  64. Kobayashi Y, Torii A, Kato M, Adachi K. 2007. Accumulation of cyclitols functioning as compatible solutes in the haptophyte alga Pavlova sp. Phycol. Res. 55:81–90 [Google Scholar]
  65. Kolb A, Strom S. 2013. An inducible antipredatory defense in haploid cells of the marine microalga Emiliania huxleyi (Prymnesiophyceae). Limnol. Oceanogr. 58:932–44 [Google Scholar]
  66. Langer G, de Nooijer LJ, Oetjen K. 2010. On the role of the cytoskeleton in coccolith morphogenesis: the effect of cytoskeleton inhibitors. J. Phycol. 46:1252–56 [Google Scholar]
  67. Langer G, Gussone N, Nehrke G, Riebesell U, Eisenhauer A. et al. 2006. Coccolith strontium to calcium ratios in Emiliania huxleyi: the dependence on seawater strontium and calcium concentrations. Limnol. Oceanogr. 51:310–20 [Google Scholar]
  68. Lazarus DB, Kotrc B, Wulf G, Schmidt DN. 2009. Radiolarians decreased silicification as an evolutionary response to reduced Cenozoic ocean silica availability. PNAS 106:9333–38 [Google Scholar]
  69. Lee LJY, Klute MJ, Herman EK, Read B, Dacks JB. 2015. Losses, expansions, and novel subunit discovery of adaptor protein complexes in haptophyte algae. Protist 166:585–97 [Google Scholar]
  70. Lehahn Y, Koren I, Schatz D, Frada M, Sheyn U. et al. 2014. Decoupling physical from biological processes to assess the impact of viruses on a mesoscale algal bloom. Curr. Biol. 24:2041–46 [Google Scholar]
  71. Leonardos N, Read B, Thake B, Young JR. 2009. No mechanistic dependence of photosynthesis on calcification in the coccolithophorid Emiliania huxleyi (Haptophyta). J. Phycol. 45:1046–51 [Google Scholar]
  72. Levin LA, Honisch B, Frieder CA. 2015. Geochemical proxies for estimating faunal exposure to ocean acidification. Oceanography 28:262–73 [Google Scholar]
  73. Liu H, Aris-Brosou S, Probert I, de Vargas C. 2010. A time line of the environmental genetics of the haptophytes. Mol. Biol. Evol. 27:161–76 [Google Scholar]
  74. Lohbeck KT, Reibesell U, Reusch TBH. 2012. Adaptive evolution of a key phytoplankton species to ocean acidification. Nat. Geosci. 5:346–51 [Google Scholar]
  75. Mackinder LC, Wheeler G, Schroeder D, Riebesell U, Brownlee C. 2010. Molecular mechanisms underlying calcification in coccolithophores. Geomicrobiol. J. 27:585–95 [Google Scholar]
  76. Mackinder LC, Wheeler G, Schroeder D, von Dassow P, Riebesell U, Brownlee C. 2011. Expression of biomineralization-related ion transport genes in Emiliania huxleyi. Environ. Microbiol. 13:3250–65 [Google Scholar]
  77. Mackinder LC, Worthy CA, Biggi G, Hall M, Ryan KP. et al. 2009. A unicellular algal virus, Emiliania huxleyi virus 86, exploits an animal-like infection strategy. J. Gen. Virol. 90:2306–16 [Google Scholar]
  78. Maldonado M, Carmona MG, Uriz MJ, Cruzado A. 1999. Decline in Mesozoic reef-building sponges explained by silicon limitation. Nature 401:785–88 [Google Scholar]
  79. Malitsky S, Ziv C, Rosenwasser S, Zheng S, Schatz D. et al. 2016. Viral infection of the marine alga Emiliania huxleyi triggers lipidome remodeling and induces the production of highly saturated triacylglycerol. New Phytol 210:88–96 [Google Scholar]
  80. Marron AO, Alston MJ, Heavens D, Akam M, Caccamo M. et al. 2013. A family of diatom-like silicon transporters in the siliceous loricate choanoflagellates. Proc. R. Soc. B 280:20122543 [Google Scholar]
  81. Marsh ME. 1994. Polyanion-mediated mineralization—assembly and reorganization of acidic polysaccharides in the Golgi system of a coccolithophorid alga during mineral deposition. Protoplasma 177:108–22 [Google Scholar]
  82. Marsh ME, Chang DK, King GC. 1992. Isolation and characterization of a novel acidic polysaccharide containing tartrate and glyoxylate residues from the mineralized scales of a unicellular coccolithophorid alga Pleurochrysis carterae. J. Biol. Chem. 267:20507–12 [Google Scholar]
  83. Marsh ME, Ridall AL, Azadi P, Duke PJ. 2002. Galacturonomannan and Golgi-derived membrane linked to growth and shaping of biogenic calcite. J. Struct. Biol. 139:39–45 [Google Scholar]
  84. McKew BA, Davey P, Finch SJ, Hopkins J, Lefebvre SC. et al. 2013a. The trade-off between the light-harvesting and photoprotective functions of fucoxanthin-chlorophyll proteins dominates light acclimation in Emiliania huxleyi (clone CCMP 1516). New Phytol 200:74–85 [Google Scholar]
  85. McKew BA, Lefebvre SC, Achterberg EP, Metodieva G, Raines CA. et al. 2013b. Plasticity in the proteome of Emiliania huxleyi CCMP 1516 to extremes of light is highly targeted. New Phytol 200:61–73 [Google Scholar]
  86. McKew BA, Metodieva G, Raines CA, Metodiev MV, Geider RJ. 2015. Acclimation of Emiliania huxleyi (1516) to nutrient limitation involves precise modification of the proteome to scavenge alternative sources of N and P. Environ. Microbiol. 17:4050–62 [Google Scholar]
  87. Meyer J, Riebesell U. 2015. Reviews and syntheses: responses of coccolithophores to ocean acidification: a meta-analysis. Biogeosciences 12:1671–82 [Google Scholar]
  88. Mitchell JG, Seuront L, Doubell MJ, Losic D, Voelcker NH. et al. 2013. The role of diatom nanostructures in biasing diffusion to improve uptake in a patchy nutrient environment. PLOS ONE 8:e59548 [Google Scholar]
  89. Mitra A, Flynn KJ, Burkholder JM, Berge T, Calbet A. et al. 2014. The role of mixotrophic protists in the biological carbon pump. Biogeosciences 11:995–1005 [Google Scholar]
  90. Mizukawa Y, Miyashita Y, Satoh M, Shiraiwa Y, Iwasaka M. 2015. Light intensity modulation by coccoliths of Emiliania huxleyi as a micro-photo-regulator. Sci. Rep. 5:13577 [Google Scholar]
  91. Monier A, Pagarete A, de Vargas C, Allen MJ, Read B. et al. 2009. Horizontal gene transfer of an entire metabolic pathway between a eukaryotic alga and its DNA virus. Genome Res 19:1441–49 [Google Scholar]
  92. Moran MA, Reisch CR, Kiene RP, Whitman WB. 2012. Genomic insights into bacterial DMSP transformations. Annu. Rev. Mar. Sci. 4:523–42 [Google Scholar]
  93. Müller MN, Ramos JBE, Schulz KG, Riebesell U, Kaźmierczak J. et al. 2015. Phytoplankton calcification as an effective mechanism to alleviate cellular calcium poisoning. Biogeosciences 12:6493–501 [Google Scholar]
  94. Nanninga HJ, Tyrrell T. 1996. Importance of light for the formation of algal blooms by Emiliania huxleyi. Mar. Ecol. Prog. Ser. 136:195–203 [Google Scholar]
  95. Nöel M-H, Kawachi M, Inouye I. 2004. Induced dimorphic life cycle of a coccolithophorid, Calyptrosphaera sphaeroidea (Prymnesiophyceae, Haptophyta). J. Phycol. 40:112–29 [Google Scholar]
  96. Obata T, Schoenefeld S, Krahnert I, Bergmann S, Scheffel A, Fernie AR. 2013. Gas-chromatography mass-spectrometry (GC-MS) based metabolite profiling reveals mannitol as a major storage carbohydrate in the coccolithophorid alga Emiliania huxleyi. Metabolites 3:168–84 [Google Scholar]
  97. Okada H, Honjo S. 1973. Distribution of oceanic coccolithophorids in the Pacific. Deep-Sea Res. Oceanogr. Abstr. 20:355–64 [Google Scholar]
  98. Okumura T, Suzuki M, Nagasawa H, Kogure T. 2012. Microstructural variation of biogenic calcite with intracrystalline organic macromolecules. Cryst. Growth Des. 12:224–30 [Google Scholar]
  99. Oviedo A, Ziveri P, Alvarez M, Tanhua T. 2015. Is coccolithophore distribution in the Mediterranean Sea related to seawater carbonate chemistry. Ocean Sci 11:13–32 [Google Scholar]
  100. Ozaki N, Sakuda S, Nagasawa H. 2007. A novel highly acidic polysaccharide with inhibitory activity on calcification from the calcified scale “coccolith” of a coccolithophorid alga, Pleurochrysis haptonemofera. Biochem. Biophys. Res. Commun. 357:1172–76 [Google Scholar]
  101. Paasche E. 1968. Biology and physiology of coccolithophorids. Annu. Rev. Microbiol. 22:71–86 [Google Scholar]
  102. Paasche E. 2001. A review of the coccolithophorid Emiliania huxleyi (Prymnesiophyceae), with particular reference to growth, coccolith formation, and calcification-photosynthesis interactions. Phycologia 40:503–29 [Google Scholar]
  103. Pagarete A, Le Corguille G, Tiwari B, Ogata H, de Vargas C. et al. 2011. Unveiling the transcriptional features associated with coccolithovirus infection of natural Emiliania huxleyi blooms. FEMS Microbiol. Ecol. 78:555–64 [Google Scholar]
  104. Quinn PS, Cortes MY, Bollmann J. 2005. Morphological variation in the deep ocean-dwelling coccolithophore Florisphaera profunda (Haptophyta). Eur. J. Phycol. 40:123–33 [Google Scholar]
  105. Ramos JBE, Schulz KG, Febiri S, Riebesell U. 2012. Photoacclimation to abrupt changes in light intensity by Phaeodactylum tricornutum and Emiliania huxleyi: the role of calcification. Mar. Ecol. Prog. Ser. 452:11–26 [Google Scholar]
  106. Raven JA, Crawfurd K. 2012. Environmental controls on coccolithophore calcification. Mar. Ecol. Prog. Ser. 470:137–66 [Google Scholar]
  107. Raven JA, Giordano M. 2009. Biomineralization by photosynthetic organisms: evidence of coevolution of the organisms and their environment. Geobiology 7:140–54 [Google Scholar]
  108. Read BA, Kegel J, Klute MJ, Kuo A, Lefebvre SC. et al. 2013. Pan genome of the phytoplankton Emiliania underpins its global distribution. Nature 499:209–13 [Google Scholar]
  109. Rickaby REM, Henderiks J, Young JN. 2010. Perturbing phytoplankton: response and isotopic fractionation with changing carbonate chemistry in two coccolithophore species. Clim. Past 6:771–85 [Google Scholar]
  110. Rickaby REM, Hermoso M, Lee RBY, Rae BD, Heureux AMC. et al. 2016. Environmental carbonate chemistry selects for phenotype of recently isolated strains of Emiliania huxleyi. Deep-Sea Res. II 127:28–40 [Google Scholar]
  111. Ridgwell A, Schmidt DN, Turley C, Brownlee C, Maldonado MT. et al. 2009. From laboratory manipulations to Earth system models: scaling calcification impacts of ocean acidification. Biogeosciences 6:2611–23 [Google Scholar]
  112. Rohloff P, Miranda K, Rodrigues JC, Fang J, Galizzi M. et al. 2011. Calcium uptake and proton transport by acidocalcisomes of Toxoplasma gondii. PLOS ONE 6:e18390 [Google Scholar]
  113. Rokitta SD, de Nooijer LJ, Trimborn S, de Vargas C, Rost B, John U. 2011. Transcriptome analyses reveal differential gene expression patterns between the life-cycle stages of Emiliania huxleyi (Haptophyta) and reflect specialization to different ecological niches. J. Phycol. 47:829–38 [Google Scholar]
  114. Rokitta SD, von Dassow P, Rost B, John U. 2014. Emiliania huxleyi endures N-limitation with an efficient metabolic budgeting and effective ATP synthesis. BMC Genom 15:1051 [Google Scholar]
  115. Rose SL, Fulton JM, Brown CM, Natale F, Van Mooy BAS, Bidle KD. 2014. Isolation and characterization of lipid rafts in Emiliania huxleyi: a role for membrane microdomains in host-virus interactions. Environ. Microbiol. 16:1150–66 [Google Scholar]
  116. Rosenwasser S, Mausz MA, Schatz D, Sheyn U, Malitsky S. et al. 2014. Rewiring host lipid metabolism by large viruses determines the fate of Emiliania huxleyi, a bloom-forming alga in the ocean. Plant Cell 26:2689–707 [Google Scholar]
  117. Rost B, Riebesell U. 2004. Coccolithophores and the biological pump: responses to environmental changes. See Thierstein & Young 2004 99–125
  118. Rost B, Zondervan I, Wolf-Gladrow D. 2008. Sensitivity of phytoplankton to future changes in ocean carbonate chemistry: current knowledge, contradictions and research directions. Mar. Ecol. Prog. Ser. 373:227–37 [Google Scholar]
  119. Sand KK, Pedersen CS, Sjöberg S, Nielsen JW, Makovicky E, Stipp SLS. 2014. Biomineralization: long-term effectiveness of polysaccharides on the growth and dissolution of calcite. Cryst. Growth Des. 14:5486–94 [Google Scholar]
  120. Savoca MS, Nevitt GA. 2014. Evidence that dimethyl sulfide facilitates a tritrophic mutualism between marine primary producers and top predators. PNAS 111:4157–61 [Google Scholar]
  121. Schatz D, Shemi A, Rosenwasser S, Sabanay H, Wolf SG. et al. 2014. Hijacking of an autophagy-like process is critical for the life cycle of a DNA virus infecting oceanic algal blooms. New Phytol 204:854–63 [Google Scholar]
  122. Segev E, Castaneda IS, Sikes EL, Vlamakis H, Kolter R. 2016. Bacterial influence on alkenones in live microalgae. J. Phycol. 52:125–30 [Google Scholar]
  123. Seyedsayamdost MR, Case RJ, Kolter R, Clardy J. 2011. The Jekyll-and-Hyde chemistry of Phaeobacter gallaeciensis. Nat. Chem. 3:331–35 [Google Scholar]
  124. Seyedsayamdost MR, Wang R, Kolter R, Clardy J. 2014. Hybrid biosynthesis of roseobacticides from algal and bacterial precursor molecules. J. Am. Chem. Soc. 136:15150–53 [Google Scholar]
  125. Seymour JR, Simo R, Ahmed T, Stocker R. 2010. Chemoattraction to dimethylsulfoniopropionate throughout the marine microbial food web. Science 329:342–45 [Google Scholar]
  126. Sharoni S, Trainic M, Schatz D, Lehahn Y, Flores MJ. et al. 2015. Infection of phytoplankton by aerosolized marine viruses. PNAS 112:6643–47 [Google Scholar]
  127. Siever R. 1992. The silica cycle in the Precambrian. Geochim. Cosmochim. Acta 56:3265–72 [Google Scholar]
  128. Spero HJ, Eggins SM, Russell AD, Vetter L, Kilburn MR, Honisch B. 2015. Timing and mechanism for intratest Mg/Ca variability in a living planktic foraminifer. Earth Planet. Sci. Lett. 409:32–42 [Google Scholar]
  129. Steinke M, Stefels J, Stamhuis E. 2006. Dimethyl sulfide triggers search behavior in copepods. Limnol. Oceanogr. 51:1925–30 [Google Scholar]
  130. Steinke M, Wolfe GV, Kirst GO. 1998. Partial characterisation of dimethylsulfoniopropionate (DMSP) lyase isozymes in 6 strains of Emiliania huxleyi. Mar. Ecol. Prog. Ser. 175:215–25 [Google Scholar]
  131. Stiller JW, Schreiber J, Yue J, Guo H, Ding Q, Huang J. 2014. The evolution of photosynthesis in chromist algae through serial endosymbioses. Nat. Commun. 5:5764 [Google Scholar]
  132. Suffrian K, Schulz KG, Gutowska MA, Riebesell U, Bleich M. 2011. Cellular pH measurements in Emiliania huxleyi reveal pronounced membrane proton permeability. New Phytol 190:595–608 [Google Scholar]
  133. Sunda W, Kieber DJ, Kiene RP, Huntsman S. 2002. An antioxidant function for DMSP and DMS in marine algae. Nature 418:317–20 [Google Scholar]
  134. Sviben S, Gal A, Hood MA, Bertinetti L, Politi Y. et al. 2016. A vacuole-like compartment concentrates a disordered calcium phase in a key coccolithophorid alga. Nat. Commun. 7:11228 [Google Scholar]
  135. Takagi H, Moriya K, Ishimura T, Suzuki A, Kawahata H, Hirano H. 2015. Exploring photosymbiotic ecology of planktic foraminifers from chamber-by-chamber isotopic history of individual foraminifers. Paleobiology 41:108–21 [Google Scholar]
  136. Taylor AR, Brownlee C. 2016. Calcification. The Physiology of Microalgae AM Borowitzka, J Beardall, AJ Raven 301–18 Cham, Switz.: Springer [Google Scholar]
  137. Taylor AR, Chrachri A, Wheeler G, Goddard H, Brownlee C. 2011. A voltage-gated H+ channel underlying pH homeostasis in calcifying coccolithophores. PLOS Biol 9:e1001085 [Google Scholar]
  138. Taylor AR, Russell MA, Harper GM, Collins TFT, Brownlee C. 2007. Dynamics of formation and secretion of heterococcoliths by Coccolithus pelagicus ssp. braarudii. Eur. J. Phycol. 42:125–36 [Google Scholar]
  139. Thierstein HR, Young JR. 2004. Coccolithophores: From Molecular Processes to Global Impact Berlin: Springer
  140. Trimborn S, Langer G, Rost B. 2007. Effect of varying calcium concentrations and light intensities on calcification and photosynthesis in Emiliania huxleyi. Limnol. Oceanogr. 52:2285–93 [Google Scholar]
  141. Tsuji Y, Yamazaki M, Suzuki I, Shiraiwa Y. 2015. Quantitative analysis of carbon flow into photosynthetic products functioning as carbon storage in the marine coccolithophore. Emiliania huxleyi. Mar. Biotechnol. 17:428–40 [Google Scholar]
  142. Tyrrell T, Merico A. 2004. Emiliania huxleyi: bloom observations and the conditions that induce them. See Thierstein & Young 2004 75–97
  143. Unrein F, Gasol JM, Not F, Forn I, Massana R. 2014. Mixotrophic haptophytes are key bacterial grazers in oligotrophic coastal waters. ISME J 8:164–76 [Google Scholar]
  144. Van Oostende N, Moerdijk-Poortvliet TC, Boschker HT, Vyverman W, Sabbe K. 2013. Release of dissolved carbohydrates by Emiliania huxleyi and formation of transparent exopolymer particles depend on algal life cycle and bacterial activity. Environ. Microbiol. 15:1514–31 [Google Scholar]
  145. Vardi A, Haramaty L, Van Mooy BAS, Fredricks HF, Kimmance SA. et al. 2012. Host-virus dynamics and subcellular controls of cell fate in a natural coccolithophore population. PNAS 109:19327–32 [Google Scholar]
  146. Vardi A, Van Mooy BAS, Fredricks HF, Popendorf KJ, Ossolinski JE. et al. 2009. Viral glycosphingolipids induce lytic infection and cell death in marine phytoplankton. Science 326:861–65 [Google Scholar]
  147. von Dassow P, John U, Ogata H, Probert I, Bendif E. et al. 2015. Life-cycle modification in open oceans accounts for genome variability in a cosmopolitan phytoplankton. ISME J 9:1365–77 [Google Scholar]
  148. von Dassow P, Ogata H, Probert I, Wincker P, Da Silva C. et al. 2009. Transcriptome analysis of functional differentiation between haploid and diploid cells of Emiliania huxleyi, a globally significant photosynthetic calcifying cell. Genome Biol 10:R114 [Google Scholar]
  149. Ward BA, Follows MJ. 2016. Marine mixotrophy increases trophic transfer efficiency, mean organism size, and vertical carbon flux. PNAS 113:2958–63 [Google Scholar]
  150. Weitz JS, Stock CA, Wilhelm SW, Bourouiba L, Coleman ML. et al. 2015. A multitrophic model to quantify the effects of marine viruses on microbial food webs and ecosystem processes. ISME J 9:1352–64 [Google Scholar]
  151. Westbroek P, Young JR, Linschooten K. 1989. Coccolith production (biomineralization) in the marine alga Emiliania huxleyi. J. Protozool. 36:368–73 [Google Scholar]
  152. Wilken S, Huisman J, Naus-Wiezer S, Van Donk E. 2013. Mixotrophic organisms become more heterotrophic with rising temperature. Ecol. Lett. 16:225–33 [Google Scholar]
  153. Wilson WH, Schroeder DC, Allen MJ, Holden MTG, Parkhill J. et al. 2005. Complete genome sequence and lytic phase transcription profile of a Coccolithovirus. Science 309:1090–92 [Google Scholar]
  154. Winter A, Jordan JR, Roth PH. 1994. Biogeography of living coccolithophores in ocean waters. Coccolithophores A Winter, WG Siesser 161–78 Cambridge, UK: Cambridge Univ. Press [Google Scholar]
  155. Wolfe GV, Steinke M, Kirst GO. 1997. Grazing-activated chemical defence in a unicellular marine alga. Nature 387:894–97 [Google Scholar]
  156. Xu K, Gao KS. 2012. Reduced calcification decreases photoprotective capability in the coccolithophorid Emiliania huxleyi. Plant Cell Physiol. 53:1267–74 [Google Scholar]
  157. Xu K, Gao KS, Villafane VE, Helbling EW. 2011. Photosynthetic responses of Emiliania huxleyi to UV radiation and elevated temperature: roles of calcified coccoliths. Biogeosciences 8:1441–52 [Google Scholar]
  158. Young JR. 1994. Functions of coccoliths. Coccolithophores A Winter, WG Siesser 63–82 Cambridge, UK: Cambridge Univ. Press [Google Scholar]
  159. Young JR, Andruleit H, Probert I. 2009. Coccolith function and morphogenesis: insights from appendage-bearing coccolithophores of the family syracosphaeraceae (Haptophyta). J. Phycol. 45:213–26 [Google Scholar]
  160. Young JR, Davis SA, Bown PR, Mann S. 1999. Coccolith ultrastructure and biomineralisation. J. Struct. Biol. 126:195–215 [Google Scholar]
  161. Young JR, Geisen M, Probert I. 2005. Review of selected aspects of coccolithophore biology with implications for paleobiodiversity estimation. Micropaleontology 51:267–88 [Google Scholar]
  162. Young JR, Westbroek P. 1991. Genotypic variation in the coccolithophorid species Emiliania huxleyi. Mar. Micropaleontol. 18:5–23 [Google Scholar]
  163. Ziveri P, de Bernardi B, Baumann K-H, Stoll HM, Mortyn PG. 2007. Sinking of coccolith carbonate and potential contribution to organic carbon ballasting in the deep ocean. Deep-Sea Res. II 54:659–75 [Google Scholar]
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