Induction of Glycerol Synthesis and Release in Cultured Symbiodinium

PLoS ONE

Volumn 7, Issue 10, 2012, Pages

  Suescún Bolívar, Luis P ^a   Iglesias Prieto, Roberto ^a   Thomé, Patricia E ^a  

^a UNIVERSIDAD NACIONAL AUTÓNOMA DE MÉXICO   (Mexico)

Author keywords

[No Author keywords available]

Indexed keywords

CHLOROPHYLL A; COMPLEMENTARY DNA; GLYCEROL; GLYCEROL 3 PHOSPHATE DEHYDROGENASE; RIBULOSEBISPHOSPHATE CARBOXYLASE; RNA;

AMINO ACID SEQUENCE; ARTICLE; BIOSYNTHESIS; CARBON FIXATION; CELL DENSITY; CELL SUSPENSION; CHLOROPHYLL CONTENT; CONCENTRATION (PARAMETERS); CONTROLLED STUDY; DINOFLAGELLATE; GENE EXPRESSION REGULATION; GENE LOCUS; GROWTH RATE; IN VITRO STUDY; LIGHT STRESS; NONHUMAN; OSMOLARITY; OSMOREGULATION; OSMOTIC STRESS; PHOTOACCLIMATIZATION; PHOTOSYSTEM II; PROTEIN EXPRESSION; PROTEIN SYNTHESIS; REVERSE TRANSCRIPTION POLYMERASE CHAIN REACTION; SYMBIODINIUM; SYMBIONT;

CARBON CYCLE; DINOFLAGELLIDA; GLYCEROL; OSMOTIC PRESSURE; PHOTOSYNTHESIS; PHOTOSYSTEM II PROTEIN COMPLEX; SYMBIOSIS;

EID: 84867423233     PISSN: None     EISSN: 19326203     Source Type: Journal    
DOI: 10.1371/journal.pone.0047182     Document Type: Article

References (63)

1. Stanley GD, (2003) The evolution of modern corals and their early history. Earth-Science Reviews 60: 195-225.
2. Trench RK, (1974) Nutritional potentials in Zoanthus sociatus (Coelenterata, Anthozoa). Helgoländer wiss Meeresunters 26: 174-216.
3. Muscatine L, Porter JW, (1977) Reef Corals: mutualistic symbioses adapted to nutrient-poor environments. Bioscience 27: 454-460.
4. Iglesias-Prieto R, Trench RK, (1997) Acclimation and adaptation to irradiance in symbiotic dinoflagellates. II. Response of chlorophyll-protein complexes to different photon-flux densities. Mar Biol 130: 23-33.
5. Spencer-Davies P, (1984) The role of zooxanthellae in the nutritional energy requirements of Pocillopora eydouxi. Coral Reefs 2: 181-186.
6. Muscatine L, Weis VM (1992) Productivity of zooxanthellae and biogeochemical cycles. In: Falkowski PG, Woodhead AD, editors. Primary Productivity and Biogeochemical Cycles in the Sea. New York: Plenum Press. 257-271.
7. Falkowski P, Dubinzky Z, Muscatine L, MacClosky L, (1993) Population control in symbiotic corals. Ammonium ions and organic materials maintain the density of zooxanthellae. Bioscience 43: 606-611.
8. Muscatine L, (1967) Glycerol excretion by symbiotic algae from corals and Tridacna and its control on the host. Science 156: 516-519.
9. Trench RK, (1971b) The physiology and biochemistry of zooxanthellae symbiotic with marine coelenterates. II. Liberation of fixed 14C by zooxanthellae in vitro. Proc. Roy. Soc. London B 177: 237-250.
10. Colombo-Pallotta MF, Rodríguez-Román A, Iglesias-Prieto R, (2010) Calcification in bleached and unbleached Montastrea faveolata: evaluating the role of oxygen and glycerol. Coral Reefs 29: 899-907.
11. Reynaud-Vaganay S, Juillet-Leclere A, Joubert J, Gattuso J-P, (2001) Effect of light on skeletal δ13C and δ18O, in interaction with photosynthesis, respiration and calcification in two zooxanthellate scleractinian corals. Paleogeography, Paleoclimatology, Paleoecology 175: 393-404.
12. Grottoli AG, Rodrigues LJ, Palardy JE, (2006) Heterotrophic plasticity and resilience in bleached corals. Nature 44027: 1186-1189.
13. Whiters KJT, Grant AL, Hinde R, (1998) Effects of free amino acids on the isolated symbiotic algae of the coral Plesiastrea versipora (Lamarck): Absence of a host release factor response. Compar Biochem Physiol Part A 120: 599-607.
14. Davy SK, Cook CB, (2001) The influence of 'host release factor' on carbon release by zooxanthellae isolated from fed and starved Aiptasia pallida (Verrill). Compar Biochem Physiol Part A. 129: 487-494.
15. Trench RK, (1971c) The physiology and biochemistry of zooxanthellae symbiotic with marine coelenterates. III. The effect of homogenates of host tissues on the excretion of photosynthetic products in vitro by zooxanthellae from two marine coelenterates. Proc. Roy. Soc. London B 177: 251-264.
16. Battey JF, Patton JS, (1987) Glycerol translocation in Condylactis gigatea. Mar Biol 95: 37-46.
17. Grant AJ, Rémond M, People J, Hinde R, (1997) Effects of host-tissue homogenate of the scleractinian coral Plesiastrea versipora on glycerol metabolism in isolated symbiotic dinoflagellates. Mar Biol 128: 665-670.
18. Gates RD, Hoegh-Gulderg O, McFall-Ngai MJ, Bil KY, Muscatine L, (1995) Free amino acids exhibit anthozoan "host factor" activity: they induce the release of photosynthate from symbiotic dinoflagellates in vitro. Proc Natl Acad Sci USA 92: 7430-7434.
19. Ritchie RJ, Grant AJ, Eltringham K, Hinde R, (1997) Clotrimazole, a model compound for the host release factor of the coral Plesiastrea versipora. Functional Plant Biol 24: 283-290.
20. Grant AJ, Trautman DA, Frankland S, Hinde R, (2003) A symbiosome membrane is not required for the actions of two host signaling compounds regulating photosynthesis in symbiotic algae isolated from cnidarians. Comp Biochem Physiol Part A 135: 337-345.
21. Trench RK, (1971a) The physiology and biochemistry of zooxanthellae symbiotic with marine coelenterates. I. The assimilation of photosynthetic products of zooxanthellae by two marine coelenterates. Proc. Roy. Soc. London B 177: 225-235.
22. Sachs JL, Wilcox TP, (2006) A shift to parasitism in the jellyfish symbiont Symbiodinium microadriaticum Proc R Soc B. 273: 425-429.
23. Loram JE, Trapido-Rosenthal HG, Douglas AE, (2007) Functional significance of genetically different symbiotic algae Symbiodinium in a coral symbiosis. Mol Ecol 16: 4849-4857.
24. Henneige SJ, Sugget DJ, Warner ME, McDougall KE, Smith DJ, (2009) Photobiology of Symbiodinium revisited: bio-physical and bio-optical signatures. Coral Reefs 28: 179-195.
25. Avron M, (1986) The osmotic components of halotolerant algae. Trends Biochem Sci 11: 5-6.
26. Hohmann S, (2002) Osmotic stress signaling and omsoadaptation in yeasts. Microbil Mol Biol Rev 66: 300-372.
27. Husic DH, Tolbert NE, (1986) Effect of osmotic stress on carbon metabolism in Chlamydomonas reinhardtii. Plant Physiol 82: 594-596.
28. Mayfield AB, Gates RD, (2007) Osmoregulation in anthozoan-dinoflagellate symbiosis Comp Biochem Physiol Part A. 147: 1-10.
29. Iglesias-Prieto R, Trench RK, (1994) Acclimation and adaptation to irradiance in symbiotic dinoflagellates. I. Responses of the photosynthetic unit changes in photon flux density. Mar Ecol Prog Ser 113: 163-175.
30. Iglesias-Prieto R, Veltrán VH, LaJeunesse TC, Reyes-Bonilla H, Thomé PE, (2004) Different algal symbionts explain the vertical distribution of dominant reef corals in the eastern Pacific. Proc R Soc London B 271: 1757-1763.
31. Rodríguez-Román A, Iglesias-Prieto R, (2005) Regulation of photochemical activity in cultured symbiotic dinoflagellates under nitrate limitation and deprivation. Mar Biol 146: 1063-1073.
32. Rowan R, Whitney SM, Fowler A, Yellowlees D, (1996) Rubisco in marine symbiotic dinoflagellates: Form II enzymes in eukaryotic oxygenic phototrophs encoded by a nuclear multigene family. Plant Cell 8: 539-553.
33. Liska AJ, Shevchenko A, Pick U, Katz A, (2004) Enhanced photosynthesis and redox energy production contribute to salinity tolerance in Dunaliella as revealed by homology-based proteomics. Plant Physiol 136: 2806-2817.
34. Muscatine L, Hand C, (1958) Direct evidence for the transfer of materials from symbiotic algae to the tissues of a coelenterate. Proc Natl Acad Sci USA 44: 1259-1263.
35. Yancey PH, Clark ME, Hand SC, Bowlus DR, Somero GN, (1982) Living with water stress: Evolution of osmolyte systems. Science 217: 1214-1222.
36. Kremer BP, (1980) Taxonomic implications of algal photoassimilate patterns. Br Phycol J 15: 399-409.
37. Sutton DC, Hoegh-Guldberg O, (1990) Host-zooxanthellae interactions in four temperate marine invertebrate symbioses: assessment of effect of host extracts on symbionts. Biol Bull 178: 175-186.
38. Yancey PH, Heppenstall M, Ly S, Andrell RM, Gates RD, et al. (2010) Betaines and dimethylsulfoniopropionate as major osmolytes in cnidaria with endosymbiotic dinoflagellates. Physiol Biochem Zool 83: 167-173.
39. Muscatine L, Pool RR, Cernichiari E, (1972) Some factors influencing the selective release of soluble organic material by zooxanthellae from reef corals. Mar Biol 13: 298-308.
40. Ahmad I, Hellebust JA, (1986) The role of glycerol and inorganic ions in osmoregulatiory responses of the euryhaline flagellate Chlamydomonas pulsatilla Wollenweber. Plant Physiol 82: 406-410.
41. Chitlaru E, Pick U, (1991) Regulation of glycerol synthesis in response to osmotic changes in Dunaliella. Plant Physiol 96: 50-60.
42. Goyal A, (2007) Osmoreglation in Dunaliella, Part I: Effects of osmotic stress on photosynthesis, dark respiration and glycerol metabolism in Dunaliella tertiolecta and its salt-sensitive mutant (HL 25/8). Plant Physiol Biochem 45: 696-704.
43. Ahmad I, Hellebust JA, (1984) Osmoregulation in the extremely euryhline marine micro-alga Chlorella autotrophica. Plant Physiol 74: 1010-1015.
44. Hagedorn M, Carter VL, Ly S, Andrell RM, Yancey PH, et al. (2010) Analysis of internal osmolarity in developing coral larvae, Fungi scutaria. Physiol Biochem Zool 83: 157-166.
45. Rees TAV, (1991) Are symbiotic algae nutrient deficient? Proc R Soc London B 243: 227-233.
46. Grant AJ, Rémond M, Starke-Peterkovic T, Hinde R, (2006) A cell signal from the coral Plesiastrea versipora reduces starch synthesis in its symbiotic alga, Symbiodinium sp. Comp Biochem Physiol A 144: 458-463.
47. Cook CB, Davy S, (2001) Are free amino acids responsible for the "host factor" effects on symbiotic zooxanthellae in extracts of host tissue? Hydrobiol 461: 71-78.
48. Warner ME, Fitt WK, Schmidt GW, (1999) Damage to photosystem II in symbiotic dinoflagellates: a determinant of coral bleaching. Proc Nat Acad Sci USA 96: 8007-8012.
49. Schaller GE, Kieber JJ, Shiu S, (2008) Two-component signaling elements and histidyl-aspartyl phosphorelays. The Arabidopsis Book 6: e0112 doi:10.1199/tab.0112.
50. Sayeed WMH, Baenzinger JE, (2009) Structural characterization of the osmosensor ProP. BBA Biomembr 1788: 1108-1115.
51. Maeda T, Wurgler-Murphy SH, Saito H, (1994) A two-component system that regulates an osmosensing MAP kinase cascade in yeast. Nature 369: 242-245.
52. Saito H, (2001) Histidine phosphorylation and two-component signaling in eukaryotic cells. Chem Rev 101: 2497-2509.
53. Reiser V, Raitt DC, Saito H, (2003) Yeast osmosensor Sln1 and plant cytokinin receptor Cre1 respond to changes in turgor pressure. J Cell Biol 161: 1035-1040.
54. Narang SS, Malone CL, Deschenes RJ, Fassler JA, (2008) Modulation of yeast Sln1 kinase activity by the Ccw 12 cell wall protein. J Biol Chem 283: 1962-1973.
55. Ault AD, Fassier JS, Deschenes RJ, (2002) Altered phosphotransfer in an activated mutant of the Saccharomyces cerevisiae two-componnet osmosensor Sln1p. Euk Cell 1: 174-180.
56. Venn AA, Loram JE, Douglas AE, (2006) Photosynthetic symbioses in animals. J Exp Botany 59: 1069-1080.
57. Cantin NE, van Oppen MJH, Willis BL, Mieog JC, Negri AP, (2009) Juvenile corals can acquire more carbon from high-performance algal symbionts. Coral Reefs 28: 405-414.
58. Blank RJ, (1987) Cell architecture of the dinoflagellate Symbiodinium sp. inhabiting the Hawaiian coral Montipora verrucosa. Mar Biol 94: 143-155.
59. Jassby AD, Platt T, (1976) Mathematical formulation of the relationship between photosynthesis and light for phytoplankton. Limnol Oceanogr 4: 540-547.
60. Iglesias-Prieto R, Matta JL, Robins WA, Trench RK, (1992) Photosynthetic response to elevated temperature in the symbiotic dinoflagellate Symbiodinium microadriaticum in culture. Proc Natl Acad Sci USA 89: 10302-10305.
61. Rosic NN, Hoegh-Guldber O, (2010) A method for extracting high-quality RNA from Symbiodinium sp. J Appl Phycol 22: 139-146.
62. Takishita K, Ishida K, Murayama T, (2003) An enigmatic GAPDH gene in the symbiotic dinoflagellate genus Symbiodinium and its related species (the Order Suessiales): Possible lateral gene transfer between two eukaryotic algae, dinoflagellate and euglenophyte. Protist 154: 443-454.
63. Seneca FO, Fôret S, Ball EE, Smith-Keune C, Miller DJ, et al. (2010) Patterns of gene expression in a scleractinian coral undergoing natural bleaching. Mar Biotechnol 12: 594-604.