Coccolithophore Cell Biology: Chalking Up Progress

Annual Review of Marine Science

Volumn 9, Issue 1, 2017, Pages 283-310

  Taylor, Alison R ^a   Brownlee, Colin ^b,c   Wheeler, Glen ^b  

^a UNIVERSITY OF NORTH CAROLINA WILMINGTON   (United States)

^b THE LABORATORY   (United Kingdom)

^c UNIVERSITY OF SOUTHAMPTON   (United Kingdom)

Author keywords

Calcification; Dimethylsulfoniopropionate; Emiliania; Haptophyte; Mixotrophy; Vesicle; Virus

Indexed keywords

BONE; CALCIFICATION (BIOCHEMISTRY); CALCITE; CYTOLOGY; ECOLOGY; MARINE BIOLOGY; METABOLISM; PHYTOPLANKTON; VIRUSES;

DIMETHYLSULFONIOPROPIONATE; EMILIANIA; HAPTOPHYTE; MIXOTROPHY; VESICLE;

BIOMINERALIZATION;

BIOLOGICAL PRODUCTION; CALCIFICATION; CARBON CYCLE; CELLS AND CELL COMPONENTS; COCCOLITH; FUNCTIONAL GROUP; GLOBAL OCEAN; LIFE CYCLE ANALYSIS; METABOLISM; MIXOTROPHY; NUTRIENT AVAILABILITY; PHYTOPLANKTON; VESICLE; VIRUS;

EMILIANIA; HAPTOPHYCEAE;

CALCIUM CARBONATE;

BONE MINERALIZATION; CARBON CYCLE; HAPTOPHYTA; PHYSIOLOGY; PHYTOPLANKTON;

CALCIFICATION, PHYSIOLOGIC; CALCIUM CARBONATE; CARBON CYCLE; HAPTOPHYTA; PHYTOPLANKTON;

EID: 85008889471     PISSN: 19411405     EISSN: 19410611     Source Type: Journal    
DOI: 10.1146/annurev-marine-122414-034032     Document Type: Article

References (163)

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
2. Bach LT,Mackinder LCM, Schulz KG, Wheeler G, SchroederDC, et al. 2013. Dissecting the impact ofCO2 and pH on the mechanisms of photosynthesis and calcification in the coccolithophore Emiliania huxleyi. New Phytol. 199:121-34
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
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
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
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
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
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
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
10. Brownlee C, Taylor AR. 2004. Calcification in coccolithophores: a cellular perspective. See Thierstein &Young 2004, pp. 31-49
11. Brownlee C, Wheeler GL, Taylor AR. 2015. Coccolithophore biomineralization: new questions, new answers. Semin. Cell Dev. Biol. 46:11-16
12. Brun P, Vogt M, PayneMR, GruberN,O'Brien CJ, et al. 2015. Ecological niches of open ocean phytoplankton taxa. Limnol. Oceanogr. 60:1020-38
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
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
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
16. Cooper MB, Smith AG. 2015. Exploring mutualistic interactions between microalgae and bacteria in the omics age. Curr. Opin. Plant. Biol. 26:147-53
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
18. Corstjens PLAM, Van Der Kooij A, Linschooten C, Brouwers GJ, Westbroek P, Vrind-Jong EW. 1998. GPA, a calcium-binding protein in the coccolithophorid Emiliania huxleyi (Prymnesiophyceae). J. Phycol. 34:622-30
19. Cros L, Estrada M. 2013. Holo-heterococcolithophore life cycles: ecological implications. Mar. Ecol. Prog. Ser. 492:57-68
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
21. Daniels CJ, Sheward RM, Poulton AJ. 2014. Biogeochemical implications of comparative growth rates of Emiliania huxleyi and Coccolithus species. Biogeosciences 11:6915-25
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
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
24. De Vargas C, AubryM-P, Probert I, Young JR. 2007. Origin and evolution of coccolithophores: from coastal hunters to oceanic farmers. In The Evolution of Aquatic Photoautotrophs, ed. PG Falkowski, AH Knoll, pp. 251-85. New York: Academic
25. Drescher B, Dillaman RM, Taylor AR. 2012. Calcification in the coccolithophore Scyphosphaera apsteinii (Prymnesiophycae). J. Phycol. 48:1343-61
26. Durak GM, Taylor AR, Walker CE, Probert I, Vargas C, et al. 2016. A role for diatom-like silicon transporters in calcifying coccolithophores. Nat. Commun. 7:10543
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
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
29. Follows MJ, Dutkiewicz S. 2011. Modeling diverse communities of marine microbes. Annu. Rev. Mar. Sci. 3:427-51
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
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
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
33. Frada MJ, Vardi A. 2015. Algal viruses hitchhiking on zooplankton across phytoplankton blooms. Commun. Integr. Biol. 8:e1029210
34. Franklin DJ, SteinkeM, Young J, Probert I, Malin G. 2010. Dimethylsulphoniopropionate (DMSP), DMSPlyase activity (DLA) and dimethylsulphide (DMS) in 10 species of coccolithophore. Mar. Ecol. Prog. Ser. 410:13-23
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
36. Fresnel J. 1994. A heteromorphic life cycle in two coastal coccolithophorids, Hymenomonas lacuna and Hymenomonas coronata (Prymnesiophyceae). Can. J. Bot. 72:1455-62
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
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
39. Gebser B, Pohnert G. 2013. Synchronized regulation of different zwitterionic metabolites in the osmoadaption of phytoplankton. Mar. Drugs 11:2168-82
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
41. Green DH, Echavarri-Bravo V, Brennan D, Hart MC. 2015. Bacterial diversity associated with the coccolithophorid algae Emiliania huxleyi and Coccolithus pelagicus f. braarudii. BioMed Res. Int. 2015:194540
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
43. Harris RP. 1994. Zooplankton grazing on the coccolithophore Emiliania huxleyi and its role in inorganic carbon flux. Mar. Biol. 119:431-39
44. Hartmann M, Grob C, Tarran GA, Martin AP, Burkill PH, et al. 2012. Mixotrophic basis of Atlantic oligotrophic ecosystems. PNAS 109:5756-60
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
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
47. Hassenkam T, JohnssonA, BechgaardK, Stipp SLS. 2011. Tracking single coccolith dissolution with picogram resolution and implications for CO2 sequestration and ocean acidification. PNAS 108:8571-76
48. Henriksen K, Stipp SLS. 2009. Controlling biomineralization the effect of solution composition on coccolith polysaccharide functionality. Cryst. Growth Des. 9:2088-97
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
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
51. HermosoM. 2014. Coccolith-derived isotopic proxies in palaeoceanography:where geologists need biologists. Cryptogamie Algol. 35:323-51
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 fluoresceinisothiocyanate-labeled lectins. Mar. Biotechnol. 7:634-44
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
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
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
56. Houdan A, Probert I, ZatylnyC,Veron B, BillardC. 2006. Ecology of oceanic coccolithophores. I.Nutritional preferences of the two stages in the life cycle of Coccolithus braarudii and Calcidiscus leptoporus. Aquat. Microb. Ecol. 44:291-301
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
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
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
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
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
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
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
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
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
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
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
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
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
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
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
72. Levin LA, Honisch B, Frieder CA. 2015. Geochemical proxies for estimating faunal exposure to ocean acidification. Oceanography 28(2):62-73
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
74. Lohbeck KT, Reibesell U, Reusch TBH. 2012. Adaptive evolution of a key phytoplankton species to ocean acidification. Nat. Geosci. 5:346-51
75. Mackinder LC, Wheeler G, Schroeder D, Riebesell U, Brownlee C. 2010. Molecular mechanisms underlying calcification in coccolithophores. Geomicrobiol. J. 27:585-95
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
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
78. MaldonadoM, CarmonaMG,UrizMJ, CruzadoA. 1999. Decline inMesozoic reef-building sponges explained by silicon limitation. Nature 401:785-88
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
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
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
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
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
84. McKew BA, Davey P, Finch SJ, Hopkins J, Lefebvre SC, et al. 2013a. The trade-off between the lightharvesting and photoprotective functions of fucoxanthin-chlorophyll proteins dominates light acclimation in Emiliania huxleyi (clone CCMP 1516). New Phytol. 200:74-85
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
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
87. Meyer J, Riebesell U. 2015. Reviews and syntheses: responses of coccolithophores to ocean acidification: a meta-analysis. Biogeosciences 12:1671-82
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
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
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
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
92. Moran MA, Reisch CR, Kiene RP,Whitman WB. 2012. Genomic insights into bacterial DMSP transformations. Annu. Rev. Mar. Sci. 4:523-42
93. Muller MN, Ramos JBE, Schulz KG, Riebesell U, Kázmierczak J, et al. 2015. Phytoplankton calcification as an effective mechanism to alleviate cellular calcium poisoning. Biogeosciences 12:6493-501
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
95. Noel M-H, Kawachi M, Inouye I. 2004. Induced dimorphic life cycle of a coccolithophorid, Calyptrosphaera sphaeroidea (Prymnesiophyceae, Haptophyta). J. Phycol. 40:112-29
96. Obata T, Schoenefeld S, Krahnert I, Bergmann S, Scheffel A, Fernie AR. 2013. Gas-chromatography massspectrometry (GC-MS) based metabolite profiling reveals mannitol as a major storage carbohydrate in the coccolithophorid alga Emiliania huxleyi. Metabolites 3:168-84
97. Okada H, Honjo S. 1973. Distribution of oceanic coccolithophorids in the Pacific. Deep-Sea Res. Oceanogr. Abstr. 20:355-64
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
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
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
101. Paasche E. 1968. Biology and physiology of coccolithophorids. Annu. Rev. Microbiol. 22:71-86
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
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
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
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
106. Raven JA, Crawfurd K. 2012. Environmental controls on coccolithophore calcification. Mar. Ecol. Prog. Ser. 470:137-66
107. Raven JA, Giordano M. 2009. Biomineralization by photosynthetic organisms: evidence of coevolution of the organisms and their environment? Geobiology 7:140-54
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
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
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
111. Ridgwell A, SchmidtDN, Turley C, Brownlee C, MaldonadoMT, et al. 2009. From laboratorymanipulations to Earth system models: scaling calcification impacts of ocean acidification. Biogeosciences 6:2611-23
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
113. Rokitta SD, Nooijer LJ, Trimborn S, 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
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
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
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
117. Rost B, Riebesell U. 2004. Coccolithophores and the biological pump: responses to environmental changes. See Thierstein &Young 2004, pp. 99-125
118. Rost B, Zondervan I,Wolf-GladrowD. 2008. Sensitivity of phytoplankton to future changes in ocean carbonate chemistry: current knowledge, contradictions and research directions. Mar. Ecol. Prog. Ser. 373:227-37
119. Sand KK, Pedersen CS, Sj oberg 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
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
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
122. Segev E, Castaneda IS, Sikes EL, Vlamakis H, Kolter R. 2016. Bacterial influence on alkenones in live microalgae. J. Phycol. 52:125-30
123. Seyedsayamdost MR, Case RJ, Kolter R, Clardy J. 2011. The Jekyll-and-Hyde chemistry of Phaeobacter gallaeciensis. Nat. Chem. 3:331-35
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
125. Seymour JR, Simo R, Ahmed T, StockerR. 2010. Chemoattraction to dimethylsulfoniopropionate throughout the marine microbial food web. Science 329:342-45
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
127. Siever R. 1992. The silica cycle in the Precambrian. Geochim. Cosmochim. Acta 56:3265-72
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
129. SteinkeM, Stefels J, Stamhuis E. 2006. Dimethyl sulfide triggers search behavior in copepods. Limnol.Oceanogr. 51:1925-30
130. SteinkeM,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
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
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
133. SundaW, Kieber DJ, Kiene RP, Huntsman S. 2002. An antioxidant function for DMSP and DMS in marine algae. Nature 418:317-20
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
135. Takagi H, Moriya K, Ishimura T, Suzuki A, KawahataH,HiranoH. 2015. Exploring photosymbiotic ecology of planktic foraminifers from chamber-by-chamber isotopic history of individual foraminifers. Paleobiology 41:108-21
136. Taylor AR, Brownlee C. 2016. Calcification. In The Physiology of Microalgae, ed. AM Borowitzka, J Beardall, AJ Raven, pp. 301-18. Cham, Switz.: Springer
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
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
139. Thierstein HR, Young JR, eds. 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
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
142. Tyrrell T, Merico A. 2004. Emiliania huxleyi: bloom observations and the conditions that induce them. See Thierstein &Young 2004, pp. 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
144. Van Oostende N, Moerdijk-Poortvliet TC, Boschker HT, VyvermanW, 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
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
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
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
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
149. Ward BA, Follows MJ. 2016. Marine mixotrophy increases trophic transfer efficiency, mean organism size, and vertical carbon flux. PNAS 113:2958-63
150. Weitz JS, Stock CA, Wilhelm SW, Bourouiba L, ColemanML, 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
151. Westbroek P, Young JR, Linschooten K. 1989. Coccolith production (biomineralization) in the marine alga Emiliania huxleyi. J. Protozool. 36:368-73
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
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
154. Winter A, Jordan JR, Roth PH. 1994. Biogeography of living coccolithophores in ocean waters. In Coccolithophores, ed. AWinter, WG Siesser, pp. 161-78. Cambridge, UK: Cambridge Univ. Press
155. Wolfe GV, Steinke M, Kirst GO. 1997. Grazing-activated chemical defence in a unicellular marine alga. Nature 387:894-97
156. Xu K, Gao KS. 2012. Reduced calcification decreases photoprotective capability in the coccolithophorid Emiliania huxleyi. Plant Cell Physiol. 53:1267-74
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
158. Young JR. 1994. Functions of coccoliths. In Coccolithophores, ed. AWinter,WGSiesser, pp. 63-82. Cambridge, UK: Cambridge Univ. Press
159. Young JR, Andruleit H, Probert I. 2009. Coccolith function and morphogenesis: insights from appendagebearing coccolithophores of the family syracosphaeraceae (Haptophyta). J. Phycol. 45:213-26
160. Young JR, Davis SA, Bown PR, Mann S. 1999. Coccolith ultrastructure and biomineralisation. J. Struct. Biol. 126:195-215
161. Young JR, Geisen M, Probert I. 2005. Review of selected aspects of coccolithophore biology with implications for paleobiodiversity estimation. Micropaleontology 51:267-88
162. Young JR, Westbroek P. 1991. Genotypic variation in the coccolithophorid species Emiliania huxleyi. Mar. Micropaleontol. 18:5-23
163. Ziveri P, 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