Symbiodinium transcriptome and global responses of cells to immediate changes in light intensity when grown under autotrophic or mixotrophic conditions

Plant Journal

Volumn 82, Issue 1, 2015, Pages 67-80

  Xiang, Tingting ^a   Nelson, William ^a,b   Rodriguez, Jesse ^c   Tolleter, Dimitri ^a,d,e   Grossman, Arthur R ^a  

^a GEOPHYSICAL LABORATORY   (United States)

^b Genestamp Inc ^*  (United States)

^c STANFORD UNIVERSITY   (United States)

^d AUSTRALIAN NATIONAL UNIVERSITY   (Australia)

^e AUSTRALIAN NATIONAL UNIVERSITY   (Australia)

Author keywords

cell adhesion; chromatin condensation; dinoflagellate cnidarian symbiosis; light acclimation; RNA Seq; spliced leader; Symbiodinium transcriptome

Indexed keywords

ALGAE; CELL ADHESION; CELL MEMBRANES; CONDENSATION; ECOSYSTEMS; ENCODING (SYMBOLS); GENE EXPRESSION; MORPHOLOGY; PHYSIOLOGICAL MODELS; PROTEINS; REEFS; SIGNAL ENCODING; SURFACE MORPHOLOGY;

CELL-ADHESION PROTEINS; CHROMATIN CONDENSATION; DINOFLAGELLATE-CNIDARIAN SYMBIOSIS; ENVIRONMENTAL CONDITIONS; ENVIRONMENTAL STRESSORS; EXTRACELLULAR MATRICES; SPLICED LEADER; TRANSCRIPTOMES;

LIGHT;

ACTINIARIA; ALGAE; ANIMALIA; ANTHOZOA; CHLAMYDOMONAS; DINOPHYCEAE; SYMBIODINIUM;

MESSENGER RNA; SPLICED LEADER RNA; TRANSCRIPTOME;

ANIMAL; ANTHOZOA; CORAL REEF; DINOFLAGELLATE; GENE EXPRESSION PROFILING; GENE EXPRESSION REGULATION; GENETICS; LIGHT; PHYSIOLOGY; RADIATION RESPONSE; SCANNING ELECTRON MICROSCOPY; SEA ANEMONE; SYMBIOSIS; ULTRASTRUCTURE;

ANIMALS; ANTHOZOA; CORAL REEFS; DINOFLAGELLIDA; GENE EXPRESSION PROFILING; GENE EXPRESSION REGULATION; LIGHT; MICROSCOPY, ELECTRON, SCANNING; RNA, MESSENGER; RNA, SPLICED LEADER; SEA ANEMONES; SYMBIOSIS; TRANSCRIPTOME;

EID: 84925654868     PISSN: 09607412     EISSN: 1365313X     Source Type: Journal    
DOI: 10.1111/tpj.12789     Document Type: Article

References (80)

1. Adams, J., Kelso, R., and, Cooley, L., (2000) The kelch repeat superfamily of proteins: propellers of cell function. Trends Cell Biol. 10, 17-24.
2. Aranda, M., Banaszak, A.T., Bayer, T., Luyten, J.R., Medina, M., and, Voolstra, C.R., (2011) Differential sensitivity of coral larvae to natural levels of ultraviolet radiation during the onset of larval competence. Mol. Ecol. 20, 2955-2972.
3. Bahler, M., and, Rhoads, A., (2002) Calmodulin signaling via the IQ motif. FEBS Lett. 513, 107-113.
4. Barbrook, A.C., Voolstra, C.R., and, Howe, C.J., (2014) The chloroplast genome of a Symbiodinium sp. clade C3 isolate. Protist, 165, 1-13.
5. Barshis, D.J., Ladner, J.T., Oliver, T.A., Seneca, F.O., Traylor-Knowles, N., and, Palumbi, S.R., (2013) Genomic basis for coral resilience to climate change. Proc. Natl. Acad. Sci. USA, 110, 1387-1392.
6. Barshis, D.J., Ladner, J.T., Oliver, T.A., and, Palumbi, S.R., (2014) Lineage specific transcriptional profiles of Symbiodinium spp. unaltered by heat stress in a coral host. Mol. Biol. Evol., 31, 1343-1352.
7. Baumgarten, S., Bayer, T., Aranda, M., Liew, Y.J., Carr, A., Micklem, G., and, Voolstra, C.R., (2013) Integrating microRNA and mRNA expression profiling in Symbiodinium microadriaticum, a dinoflagellate symbiont of reef-building corals. BMC Genom. 14, 704.
8. Bayer, T., Aranda, M., Sunagawa, S., Yum, L.K., Desalvo, M.K., Lindquist, E., Coffroth, M.A., Voolstra, C.R., and, Medina, M., (2012) Symbiodinium transcriptomes: genome insights into the dinoflagellate symbionts of reef-building corals. PLoS ONE, 7, e35269.
9. Beel, B., Prager, K., Spexard, M., et al. (2012) A flavin binding cryptochrome photoreceptor responds to both blue and red light in Chlamydomonas reinhardtii. Plant Cell, 24, 2992-3008.
10. Béjà, O., Koonin, E.V., Aravind, L., et al. (2000) Bacterial rhodopsin: evidence for a new type of phototrophy in the sea. Science, 289, 1902-1906.
11. Canton, J., Neculai, D., and, Grinstein, S., (2013) Scavenger receptors in homeostasis and immunity. Nat. Rev. Immunol. 13, 621-634.
12. Chae, E., Tan, Q.K., Hill, T.A., and, Irish, V.F., (2008) An Arabidopsis F-box protein acts as a transcriptional co-factor to regulate floral development. Development, 135, 1235-1245.
13. Chaves, I., Pokorny, R., Byrdin, M., Hoang, N., Ritz, T., Brettel, K., Essen, L.O., van der Horst, G.T., Batschauer, A., and, Ahmad, M., (2011) The cryptochromes: blue light photoreceptors in plants and animals. Annu. Rev. Plant Biol. 62, 335-364.
14. Chen, S.M., Tsai, Y.S., Wu, C.M., Liao, S.K., Wu, L.C., Chang, C.S., Liu, Y.H., and, Tsai, P.J., (2010) Streptococcal collagen-like surface protein 1 promotes adhesion to the respiratory epithelial cell. BMC Microbiol. 10, 320.
15. Davy, S.K., Allemand, D., and, Weis, V.M., (2012) Cell biology of cnidarian-dinoflagellate symbiosis. Microbiol. Mol. Biol. Rev. 76, 229-261.
16. DeSalvo, M.K., Voolstra, C.R., Sunagawa, S., Schwarz, J.A., Stillman, J.H., et al. (2008) Differential gene expression during thermal stress and bleaching in the Caribbean coral Montastraea faveolata. Mol. Ecol. 17, 3952-3971.
17. DeSalvo, M.K., Sunagawa, S., Fisher, P.L., Voolstra, C.R., Iglesias-Prieto, R., and, Medina, M., (2010) Coral host transcriptomic states are correlated with Symbiodinium genotypes. Mol. Ecol. 19, 1174-1186.
18. DeSalvo, M.K., Estrada, A., Sunagawa, S., and, Medina, M., (2012) Transcriptomic responses to darkness stress point to common coral bleaching mechanisms. Coral Reefs, 31, 215-228.
19. Dodge, J.D., and, Greuet, C., (1987) Dinoflagellate ultrastructure and complex organelles. In Botanical Monographs (, Taylor, F.J.R., ed.). Oxford: Blackwell Scientific Publications, pp. 92-142.
20. Ernst, O.P., et al. (2014) Microbial and animal rhodopsins: structures, functions, and. molecular mechanisms. Chem. Rev. 114, 126-163.
21. Falkowski, P., Dubinsky, Z., Muscatine, L., and, Porter, J., (1984) Light and the bioenergetics of a symbiotic coral. Bioscience, 34, 705-709.
22. Fauvart, M., and, Michiels, J., (2008) Rhizobial secreted proteins as determinants of host specificity in the rhizobium-legume symbiosis. FEMS Microbiol. Lett. 285, 1-9.
23. Gonzalez-Ballester, D., Casero, D., Cokus, S., Pellegrini, M., Merchant, S.S., and, Grossman, A.R., (2010) RNA-Seq analysis of sulfur-deprived Chlamydomonas cells reveals aspects of acclimation critical for cell survival. Plant Cell, 22, 1-27.
24. Goreau, T., (1959) The ecology of Jamaican coral reefs I. Species composition and zonation. Ecology, 40, 67-90.
25. Gornik, S.G., Ford, K.L., Mulhern, T.D., Bacic, A., McFadden, G.I., and, Waller, R.F., (2012) Loss of nucleosomal DNA condensation coincides with appearance of a novel nuclear protein in dinoflagellates. Curr. Biol. 22, 2303-2312.
26. Gupta, S.K., Carmi, S., Waldman Ben-Asher, H., Tkacz, I.D., Naboishchikov, I., and, Michaeli, S., (2013) Basal splicing factors regulate the stability of mature mRNAs in trypanosomes. J. Biol. Chem. 288, 4991-5006.
27. Hadjebi, O., Casas-Terradellas, E., Garcia-Gonzalo, F.R., and, Rosa, J.L., (2008) The RCC1 superfamily: from genes, to function, to disease. Biochim. Biophys. Acta, 1783, 1467-1479.
28. Han, L., Mason, M., Risseeuw, E.P., Crosby, W.L., and, Somers, D.E., (2004) Formation of an SCF(ZTL) complex is required for proper regulation of circadian timing. Plant J. 40, 291-301.
29. Hennige, S.J., Suggett, D.J., Warner, M.E., McDougall, K.E., and, Smith, D.J., (2009) Photobiology of Symbiodinium revisited: bio-physical and bio-optical signatures. Coral Reefs, 28, 179-195.
30. Hoegh-Guldberg, O., (1999) Climate change, coral bleaching and the future of the world's coral reefs. Mar. Freshw. Res. 50, 839-866.
31. Hoegh-Guldberg, O., and, Smith, G.J., (1989) The effect of sudden changes in temperature, irradiance and salinity on the population density and export of zooxanthellae from the reef corals Stylophora pistillata (Esper 1797) and Seriatopora hystrix (Dana 1846). Exp. Mar. Biol. Ecol. 129, 279-303.
32. Houille-Vernes, L., Rappaport, F., Wollman, F.A., Alric, J., and, Johnson, X., (2011) Plastid terminal oxidase 2 (PTOX2) is the major oxidase involved in chlororespiration in Chlamydomonas. Proc. Natl Acad. Sci. USA, 108, 20820-20825.
33. Iglesias-Prieto, R., and, Trench, R.K., (1994) Adaptation and acclimation to irradiance in symbiotic dinoflagellates. I. Response of the photosynthetic unit to changes in photon flux density. Mar. Ecol. Prog. Ser. 113, 163-175.
34. Iglesias-Prieto, R., and, Trench, R.K., (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.
35. Jiao, Y., Ma, L., Strickland, E., and, Deng, X.W., (2005) Conservation and divergence of light-regulated genome expression patterns during seedling development in rice and Arabidopsis. Plant Cell, 17, 3239-3256.
36. Jones, R.J., and, Hoegh-Guldberg, O., (2001) Diurnal changes in the photochemical efficiency of the symbiotic dinoflagellates (Dinophyceae) of corals: photoprotection, photoinactivation and the relationship to coral bleaching. Plant, Cell Environ. 24, 89-99.
37. Jurado, S., Abraham, Z., Manzano, C., Lopez-Torrejon, G., Pacios, L.F., and, Del Pozo, J.C., (2010) The Arabidopsis cell cycle F-box protein SKP2A binds to auxin. Plant Cell, 22, 3891-3904.
38. Kepinski, S., and, Leyser, O., (2005) The Arabidopsis F-box protein TIR1 is an auxin receptor. Nature, 435, 446-451.
39. Knudsen, B., and, Hein, J., (2003) Pfold: RNA secondary structure prediction using stochastic context-free grammars. Nucleic Acids Res. 31, 3423-3428.
40. Ladner, J.T., Barshis, D.J., and, Palumbi, S.R., (2012) Protein evolution in two co-occurring types of Symbiodinium: an exploration into the genetic basis of thermal tolerance in Symbiodinium clade D. BMC Evol. Biol., 12, 217.
41. Lees, J.F., Shneidman, P.S., Skuntz, S.F., Carden, M.J., and, Lazzarini, R.A., (1988) The structure and organization of the human heavy neurofilament subunit (NF-H) and the gene encoding it. EMBO J. 7, 1947-1955.
42. Lehnert, E.M., Burriesci, M.S., and, Pringle, J.R., (2012) Developing the anemone Aiptasia as a tractable model for cnidarian-dinoflagellate symbiosis: the transcriptome of aposymbiotic A. pallida. BMC Genom. 13, 271.
43. Lin, S., Zhang, H., Zhuang, Y., Tran, B., and, Gill, J., (2010) Spliced leader-based metatranscriptomic analyses lead to recognition of hidden genomic features in dinoflagellates. Proc. Natl Acad. Sci. USA, 107, 20033-20038.
44. Loeblich, A.R., and, Loeblich, L.A., (1985) Dinoflagellates: structure of the amphiesma and re-analysis of thecal plate patterns. Hydrobiologia, 123, 177-179.
45. Makde, R.D., England, J.R., Yennawar, H.P., and, Tan, S., (2010) Structure of RCC1 chromatin factor bound to the nucleosome core particle. Nature, 467, 562-566.
46. McGinley, M.P., Aschaffenburg, M.D., Pettay, D.T., Smith, R.T., LaJeunesse, T.C., and, Warner, M.E., (2012) Transcriptional response of two core photosystem genes in Symbiodinium spp. exposed to thermal stress. PLoS ONE, 7, e50439.
47. Moon, S.Y., and, Zheng, Y., (2003) Rho GTPase-activating proteins in cell regulation. Trends Cell Biol. 13, 13-22.
48. Mukohata, Y., Ihara, K., Tamura, T., and, Sugiyama, Y., (1999) Halobacterial rhodopsins. J. Biochem. 125, 649-657.
49. Ohtsubo, M., Kai, R., Furuno, N., et al. (1987) Isolation and characterization of the active cDNA of the human cell cycle gene (RCC1) involved in the regulation of onset of chromosome condensation. Genes Dev. 1, 585-593.
50. Pankov, R., and, Yamada, K.M., (2002) Fibronectin at a glance. J. Cell Sci. 115, 3861-3863.
51. Peers, G., Truong, T.B., Ostendorf, E., Elrad, D., Grossman, A.R., Hippler, M., and, Niyogi, K.K., (2009) An ancient light-harvesting protein is critical for the regulation of algal photosynthesis. Nature, 462, 518-521.
52. Polato, N.R., Voolstra, C.R., Schnetzer, J., DeSalvo, M.K., Randall, C.J., Szmant, A.M., Medina, M., and, Baums, I.B., (2010) Location-specific responses to thermal stress in larvae of the reef-building coral Montastraea faveolata. PLoS ONE, 5, e11221.
53. Reynolds, W.S., Schwarz, J.A., and, Weis, V.M., (2000) Symbiosis-enhanced gene expression in cnidarian-algal associations: cloning and characterization of a cDNA, sym32, encoding a possible cell adhesion protein. Comp. Biochem. Physiol. A Mol. Integr. Physiol. 126, 33-44.
54. Riazuddin, S., Khan, S.N., Ahmed, Z.M., et al. (2006) Mutations in TRIOBP, which encodes a putative cytoskeletal-organizing protein, are associated with nonsyndromic recessive deafness. Am. J. Hum. Genet. 78, 137-143.
55. Robison, J.D., and, Warner, M., (2006) Differential impacts of photoacclimation and thermal stress on the photobiology of four different phylotypes of Symbiodinium (Pyrrhophyta). J. Phycol. 42, 568-579.
56. Rosic, N., Ling, E.Y.S., Chan, C.-K.K., Lee, H.C., Kaniewska, P., Edwards, D., Dove, S., and, Hoegh-Guldberg, O., (2014) Unfolding the secrets of coral-algal symbiosis. ISME J. 15, 1052.
57. Rotin, D., and, Kumar, S., (2009) Physiological functions of the HECT family of ubiquitin ligases. Nat. Rev. Mol. Cell Biol. 10, 398-409.
58. Schwarz, J.A., and, Weis, V.M., (2003) Localization of a symbiosis-related protein, Sym32, in the Anthopleura elegantissima-Symbiodinium muscatinei association. Biol. Bull. 205, 339-350.
59. Sedlacek, K., Stark, K., Cunha, S.R., et al. (2008) Common genetic variants in ANK2 modulate QT interval: results from the KORA study. Circ. Cardiovasc. Genet. 1, 93-99.
60. Shefer, G., and, Benayahu, D., (2010) SVEP1 is a novel marker of activated pre-determined skeletal muscle satellite cells. Stem Cell Rev. 6, 42-49.
61. Shoguchi, E., Shinzato, C., Kawashima, T., et al. (2013) Draft assembly of the Symbiodinium minutum nuclear genome reveals dinoflagellate gene structure. Curr. Biol. 23, 1399-1408.
62. Slamovits, C.H., and, Keeling, P.J., (2008) Widespread recycling of processed cDNAs in dinoflagellates. Curr. Biol. 18, R550-R552.
63. Slamovits, C.H., Okamoto, N., Burri, L., James, E.R., and, Keeling, P.J., (2011) A bacterial proteorhodopsin proton pump in marine eukaryotes. Nat. Commun. 2, 138.
64. Sorek, M., Diaz-Almeyda, E., Medina, M., and, Levy, O., (2014) Circadian clocks in symbiotic corals: the duet between Symbiodinium algae and their coral host. Mar. Genomics, 14, 47-57.
65. Stoecker, D.K., (1999) Mixotrophy among dinoflagellates. J. Eukaryot. Microbiol. 46, 397-401.
66. Taylor, F.J.R., Hoppenrath, M., and, Saldarriaga, J.F., (2008) Dinoflagellate diversity and distribution. Biodivers. Conserv. 17, 407-418.
67. Tolleter, D., Seneca, F.O., Denofrio, J.C., Krediet, C.J., Palumbi, S.R., Pringle, J.R., and, Grossman, A.R., (2013) Coral bleaching independent of photosynthetic activity. Curr. Biol. 23, 1782-1786.
68. Voolstra, C.R., Schwarz, J.A., Schnetzer, J., Sunagawa, S., DeSalvo, M.K., Szmant, A.M., Coffroth, M.A., and, Medina, M., (2009) The host transcriptome remains unaltered during the establishment of coral-algal symbioses. Mol. Ecol. 18, 1823-1833.
69. Wang, Y., Jensen, L., Hojrup, P., and, Morse, D., (2005) Synthesis and degradation of dinoflagellate plastid-encoded psbA proteins are light-regulated, not circadian-regulated. Proc. Natl. Acad. Sci. USA, 102, 2844-2849.
70. Wang, F., Zhu, D., Huang, X., Li, S., Gong, Y., Yao, Q., Fu, X., Fan, L.M., and, Deng, X.W., (2009) Biochemical insights on degradation of Arabidopsis DELLA proteins gained from a cell-free assay system. Plant Cell, 21, 2378-2390.
71. Warner, M.E., Fitt, W.K., and, Schmidt, G.W., (1999) Damage to photosystem II in symbiotic dinoflagellates: a determinant of coral bleaching. Proc. Natl. Acad. Sci. USA, 96, 8007-8012.
72. Warner, M.E., Michael, P.L., and, Ralph, P.J., (2010) "Chlorophyll fluorescence in reef building corals." Chlorophyll a fluorescence in aquatic sciences: methods and applications. Springer Netherlands, 209-222.
73. Waschuk, S.A., Bezerra, A.G., Shi, L., and, Brown, L.S., (2005) Leptosphaeria rhodopsin: Bacteriorhodopsin-like proton pump from a eukaryote. Proc. Natl Acad. Sci. USA, 102, 6879-6883.
74. Weis, V.M., Davy, S.K., Hoegh-Guldberg, O., Rodriguez-Lanetty, M., and, Pringle, J.R., (2008) Cell biology in model systems as the key to understanding corals. Trends Ecol. Evol. 23, 369-376.
75. Wood-Charlson, E.M., Hollingsworth, L.L., Krupp, D.A., and, Weis, V.M., (2006) Lectin/glycan interactions play a role in recognition in a coral/dinoflagellate symbiosis. Cell. Microbiol. 8, 1985-1993.
76. Xiang, T., Hambleton, E., DeNofrio, J., Pringle, J., and, Grossman, A.R., (2013) Isolation of clonal axenic strains of the symbiotic dinoflagellate Symbiodinium and their growth and host specificity. J. Phycol. 49, 447-458.
77. Yonge, C.M., (1931) The significance of the relationship between corals and Zooxanthellæ. Nature, 128, 309-311.
78. Zhang, Z., Green, B.R., and, Cavalier-Smith, T., (1999) Single gene circles in dinoflagellate chloroplast genomes. Nature, 400, 155-159.
79. Zhang, H., Hou, Y., Miranda, L., Campbell, D.A., Sturm, N.R., Gaasterland, T., and, Lin, S., (2007) Spliced leader RNA trans-splicing in dinoflagellates. Proc. Natl. Acad. Sci. USA, 104, 4618-4623.
80. Zhang, H., Zhuang, Y., Gill, J., and, Lin, S., (2013) Proof that dinoflagellate spliced leader (DinoSL) is a useful hook for fishing dinoflagellate transcripts from mixed microbial samples: Symbiodinium kawagutii as a case study. Protist, 164, 510-527.