Adaptations to endosymbiosis in a Cnidarian-Dinoflagellate association: Differential gene expression and specific gene duplications

PLoS Genetics

Volumn 7, Issue 7, 2011, Pages

  Ganot, Philippe ^a,b,c,d   Moya, Aurélie ^a,b,c,d,g   Magnone, Virginie ^a,c,e   Allemand, Denis ^a,f   Furla, Paola ^a,b,c,d   Sabourault, Cécile ^a,b,c,d  

^a UNIVERSITÉ CÔTE D'AZUR   (France)

^b SORBONNE UNIVERSITÉ   (France)

^c CNRS   (France)

^d UMR7138 Systématique Adaptation Evolution ^*  (France)

^e INSTITUT DE PHARMACOLOGIE MOLÉCULAIRE ET CELLULAIRE   (France)

^f CENTRE SCIENTIFIQUE DE MONACO   (Monaco)

^g JAMES COOK UNIVERSITY   (Australia)

Author keywords

[No Author keywords available]

Indexed keywords

CARBON; CARBONATE DEHYDRATASE; MEMBRANE PROTEIN; SIGNAL PEPTIDE; VITAMIN K GROUP; CALCIUM BINDING PROTEIN; CELL ADHESION MOLECULE; TRANSCRIPTOME;

ANEMONIA VIRIDIS; ARTICLE; AUTOTROPH; CELL MIGRATION; CNIDARIA; COLLAGEN SYNTHESIS; CONTROLLED STUDY; DINOFLAGELLATE; ENDOSYMBIOSIS; EPIDERMIS CELL; EVOLUTIONARY ADAPTATION; FATTY ACID METABOLISM; GASTRODERM; GENE AMPLIFICATION; GENE DOSAGE; GENE DUPLICATION; GENE EXPRESSION REGULATION; GENE LOCUS; GERM LAYER; HETEROTROPH; MICROARRAY ANALYSIS; NONHUMAN; NUCLEOTIDE SEQUENCE; PHENOTYPE; PHOTOSYNTHESIS; PHYLOGENY; REAL TIME POLYMERASE CHAIN REACTION; SEA ANEMONE; SEQUENCE ALIGNMENT; SYMBIONT; TEMPERATURE STRESS; TISSUE SPECIFICITY; UPREGULATION; AMINO ACID SEQUENCE; ANIMAL; CLASSIFICATION; DNA MICROARRAY; FRANCE; GENE EXPRESSION PROFILING; GENETICS; GEOGRAPHY; HEAT; HOST PARASITE INTERACTION; MEDITERRANEAN SEA; MOLECULAR GENETICS; PARASITOLOGY; PHYSIOLOGY; REVERSE TRANSCRIPTION POLYMERASE CHAIN REACTION; SEQUENCE HOMOLOGY; SYMBIOSIS; TIME;

ACTINIARIA; ANEMONIA VIRIDIS; ANTHOZOA; DINOPHYCEAE;

AMINO ACID SEQUENCE; ANIMALS; CALCIUM-BINDING PROTEINS; CELL ADHESION MOLECULES; DINOFLAGELLIDA; FRANCE; GENE EXPRESSION PROFILING; GEOGRAPHY; HOST-PARASITE INTERACTIONS; HOT TEMPERATURE; MEDITERRANEAN SEA; MEMBRANE PROTEINS; MOLECULAR SEQUENCE DATA; OLIGONUCLEOTIDE ARRAY SEQUENCE ANALYSIS; PHYLOGENY; REVERSE TRANSCRIPTASE POLYMERASE CHAIN REACTION; SEA ANEMONES; SEQUENCE HOMOLOGY, AMINO ACID; SYMBIOSIS; TIME FACTORS; TRANSCRIPTOME;

EID: 79960949840     PISSN: 15537390     EISSN: 15537404     Source Type: Journal    
DOI: 10.1371/journal.pgen.1002187     Document Type: Article

References (79)

1. Technau U, Steele RE, (2011) Evolutionary crossroads in developmental biology: Cnidaria. Development 138: 1447-1458.
2. Venn AA, Loram JE, Douglas AE, (2008) Photosynthetic symbioses in animals. J Exp Bot 59: 1069-1080.
3. Furla P, Allemand D, Shick JM, Ferrier-Pages C, Richier S, et al. (2005) The Symbiotic Anthozoan: A Physiological Chimera between Alga and Animal. Integr Comp Biol 45: 595-604.
4. Yellowlees D, Rees TA, Leggat W, (2008) Metabolic interactions between algal symbionts and invertebrate hosts. Plant Cell Environ 31: 679-694.
5. Furla P, Allemand D, Orsenigo MN, (2000) Involvement of H+-ATPase and carbonic anhydrase in inorganic carbon uptake for endosymbiont photosynthesis. Amer J Physiol (Regul Integr Comp) 278: R870-R881.
6. Weis VM, (1991) The induction of carbonic anhydrase in the symbiotic sea anemone Aiptasia pulchella. Biol Bull 180: 496-504.
7. Merle P-L, Sabourault C, Richier S, Allemand D, Furla P, (2007) Catalase characterization and implication in bleaching of a symbiotic sea anemone. Free Rad Biol Med 42: 236-246.
8. Richier S, Furla P, Plantivaux A, Merle P-L, Allemand D, (2005) Symbiosis-induced adaptation to oxidative stress. J Exp Biol 208: 277-285.
9. Richier S, Sabourault C, Courtiade J, Zucchini N, Allemand D, et al. (2006) Oxidative stress and apoptotic events during thermal stress in the symbiotic sea anemone, Anemonia viridis. Febs J 273: 4186-4198.
10. Bertucci A, Tambutté S, Supuran C, Allemand D, Zoccola D, (2011) A New Coral Carbonic Anhydrase in Stylophora pistillata. Marine Biotechnology pp. 1-11.
11. Weis VM, (2008) Cellular mechanisms of Cnidarian bleaching: stress causes the collapse of symbiosis. J Exp Biol 211: 3059-3066.
12. Moya A, Tambutté S, Bertucci A, Tambutté E, Lotto S, et al. (2008) Carbonic Anhydrase in the Scleractinian Coral Stylophora pistillata. J Biol Chem 283: 25475-25484.
13. Schwarz JA, Weis VM, (2003) Localization of a symbiosis-related protein, Sym32, in the Anthopleura elegantissima-Symbiodinium muscatinei Association. Biol Bull 205: 339-350.
14. Weis VM, Allemand D, (2009) Physiology. What determines coral health? Science 324: 1153-1155.
15. Bay LK, Nielsen HB, Jarmer H, Seneca F, vanOppen MJH, (2009) Transcriptomic variation in a coral reveals pathways of clonal organisation. Marine Genomics 2: 119-125.
16. Rodriguez-Lanetty M, Phillips WS, Weis VM, (2006) Transcriptome analysis of a cnidarian-dinoflagellate mutualism reveals complex modulation of host gene expression. BMC Genomics 7: 23.
17. Voolstra CR, Schwarz JA, Schnetzer J, Sunagawa S, Desalvo MK, et al. (2009) The host transcriptome remains unaltered during the establishment of coral-algal symbioses. Mol Ecol 18: 1823-1833.
18. DeSalvo MK, Voolstra CR, Sunagawa S, Schwarz JA, Stillman JH, et al. (2008) Differential gene expression during thermal stress and bleaching in the Caribbean coral Montastraea faveolata. Mol Ecol 17: 3952-3971.
19. Rodriguez-Lanetty M, Harii S, Hoegh-Guldberg O, (2009) Early molecular responses of coral larvae to hyperthermal stress. Mol Ecol 18: 5101-5114.
20. Sabourault C, Ganot P, Deleury E, Allemand D, Furla P, (2009) Comprehensive EST analysis of the symbiotic sea anemone, Anemonia viridis. BMC Genomics 10: 333.
21. Bachvaroff TR, Place AR, (2008) From Stop to Start: Tandem Gene Arrangement, Copy Number and Trans-Splicing Sites in the Dinoflagellate Amphidinium carterae. PLoS ONE 3: e2929 doi:10.1371/journal.pone.0002929.
22. Slamovits CH, Keeling PJ, (2008) Widespread recycling of processed cDNAs in dinoflagellates. Current Biology 18: R550-R552.
23. Wettenhall JM, Smyth GK, (2004) limmaGUI: A graphical user interface for linear modeling of microarray data. Bioinformatics 20: 3705-3706.
24. Exposito JY, Larroux C, Cluzel C, Valcourt U, Lethias C, et al. (2008) Demosponge and sea anemone fibrillar collagen diversity reveals the early emergence of A/C clades and the maintenance of the modular structure of type V/XI collagens from sponge to human. J Biol Chem 283: 28226-28235.
25. Myllyharju J, Kivirikko KI, (2004) Collagens, modifying enzymes and their mutations in humans, flies and worms. Trends Genet 20: 33-43.
26. Honore B, (2009) The rapidly expanding CREC protein family: members, localization, function, and role in disease. Bioessays 31: 262-277.
27. Douglas AE, (1994) Symbiotic Interactions New York Oxford University Press Inc.
28. Sacher M, Kim YG, Lavie A, Oh BH, Segev N, (2008) The TRAPP complex: insights into its architecture and function. Traffic 9: 2032-2042.
29. Zwang Y, Yarden Y, (2009) Systems Biology of Growth Factor-Induced Receptor Endocytosis. Traffic 10: 349-363.
30. Capasso M, Decoursey TE, Dyer MJ, (2010) pH regulation and beyond: unanticipated functions for the voltage-gated proton channel, HVCN1. Trends Cell Biol.
31. Falcon-Perez JM, Dell'Angelica EC, (2007) Zinc transporter 2 (SLC30A2) can suppress the vesicular zinc defect of adaptor protein 3-depleted fibroblasts by promoting zinc accumulation in lysosomes. Exp Cell Res 313: 1473-1483.
32. Barr F, Lambright DG, (2010) Rab GEFs and GAPs. Curr Opin Cell Biol 22: 461-470.
33. Chen MC, Cheng YM, Sung PJ, Kuo CE, Fang LS, (2003) Molecular identification of Rab7 (ApRab7) in Aiptasia pulchella and its exclusion from phagosomes harboring zooxanthellae. Biochem Biophys Res Commun 308: 586-595.
34. Chen M-C, Hong M-C, Huang Y-S, Liu M-C, Cheng Y-M, et al. (2005) ApRab11, a cnidarian homologue of the recycling regulatory protein Rab11, is involved in the establishment and maintenance of the Aiptasia-Symbiodinium endosymbiosis. Biochemical and Biophysical Research Communications 338: 1607-1616.
35. Stambler N, Dubinsky Z, (1987) Energy relationships between Anemonia sulcata and its endosymbiotic zooxanthellae. Symbiosis 3: 233-248.
36. Hanson RW, (2005) Metabolism in the era of molecular biology. J Biol Chem 280: 1705-1715.
37. Foulon V, Antonenkov VD, Croes K, Waelkens E, Mannaerts GP, et al. (1999) Purification, molecular cloning, and expression of 2-hydroxyphytanoyl-CoA lyase, a peroxisomal thiamine pyrophosphate-dependent enzyme that catalyzes the carbon-carbon bond cleavage during alpha-oxidation of 3-methyl-branched fatty acids. Proc Natl Acad Sci U S A 96: 10039-10044.
38. Kuo J, Liang Z-C, Lin C-H, (2010) Suppression subtractive hybridization identifies genes correlated to symbiotic and aposymbiotic sea anemone associated with dinoflagellate. Journal of Experimental Marine Biology and Ecology 388: 11-19.
39. Ikonen E, (2008) Cellular cholesterol trafficking and compartmentalization. Nat Rev Mol Cell Biol 9: 125-138.
40. Liscum L, Sturley SL, (2004) Intracellular trafficking of Niemann-Pick C proteins 1 and 2: obligate components of subcellular lipid transport. Biochim Biophys Acta 1685: 22-27.
41. Vance JE, (2010) Transfer of cholesterol by the NPC team. Cell Metab 12: 105-106.
42. Kimura A, Sakaguchi E, Nonaka M, (2009) Multi-component complement system of Cnidaria: C3, Bf, and MASP genes expressed in the endodermal tissues of a sea anemone, Nematostella vectensis. Immunobiology 214: 165-178.
43. Nonaka M, Kimura A, (2006) Genomic view of the evolution of the complement system. Immunogenetics 58: 701-713.
44. Kvennefors EC, Leggat W, Kerr CC, Ainsworth TD, Hoegh-Guldberg O, et al. (2010) Analysis of evolutionarily conserved innate immune components in coral links immunity and symbiosis. Dev Comp Immunol 34: 1219-1229.
45. Raykhel I, Alanen H, Salo K, Jurvansuu J, Nguyen VD, et al. (2007) A molecular specificity code for the three mammalian KDEL receptors. J Cell Biol 179: 1193-1204.
46. Wallin R, Hutson SM, (2004) Warfarin and the vitamin K-dependent gamma-carboxylation system. Trends Mol Med 10: 299-302.
47. Bandyopadhyay PK, (2008) Vitamin K-dependent gamma-glutamylcarboxylation: an ancient posttranslational modification. Vitam Horm 78: 157-184.
48. Oldenburg J, Marinova M, Muller-Reible C, Watzka M, (2008) The vitamin K cycle. Vitam Horm 78: 35-62.
49. Coutu DL, Wu JH, Monette A, Rivard GE, Blostein MD, et al. (2008) Periostin, a member of a novel family of vitamin K-dependent proteins, is expressed by mesenchymal stromal cells. J Biol Chem 283: 17991-18001.
50. Weis VM, Levine RP, (1996) Differential protein profiles reflect the different lifestyles of symbiotic and aposymbiotic Anthopleura elegantissima, a sea anemone from temperate waters. J Exp Biol 199: 883-892.
51. Reynolds WS, Schwarz JA, Weis VM, (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.
52. Nishimoto SK, Price PA, (1985) The vitamin K-dependent bone protein is accumulated within cultured osteosarcoma cells in the presence of the vitamin K antagonist warfarin. J Biol Chem 260: 2832-2836.
53. Huang M, Rigby AC, Morelli X, Grant MA, Huang G, et al. (2003) Structural basis of membrane binding by Gla domains of vitamin K-dependent proteins. Nat Struct Biol 10: 751-756.
54. Allemand D, Furla P, Bénazet-Tambutté S, (1998) Mechanisms of carbon acquisition for endosymbiont photosynthesis in Anthozoa. Can J Bot 76: 925-941.
55. Cook CM, Lanaras T, Colman B, (1986) Evidence for bicarbonate transport in species of red and brown macrophytic marine algae. J Exp Bot 37: 977-984.
56. Kerby NW, Raven JA, (1985) Transport and fixation of inorganic carbon by marine algae. Adv Bot Res 11: 71-123.
57. Furla P, Galgani I, Durand I, Allemand D, (2000) Sources and mechanisms of inorganic carbon transport for coral calcification and photosynthesis. J Exp Biol 203: 3445-3457.
58. Leggat W, Marendy EM, Baillie B, Whitney SM, Ludwig M, et al. (2002) Dinoflagellate symbioses: strategies and adaptations for the acquisition and fixation of inorganic carbon. Funct Plant Biol 29: 309-322.
59. Weis VM, (1993) Effect of dissolved inorganic carbon concentration on the photosynthesis of the symbiotic sea anemone Aiptasia pulchella Carlgren: role of carbonic anhydrase. J Exp Mar Biol Ecol 174: 209-225.
60. Al-Moghrabi S, Goiran C, Allemand D, Speziale N, Jaubert J, (1996) Inorganic carbon uptake for photosynthesis by the symbiotic coral/dinoflagellate association. II. Mechanisms for bicarbonate uptake. J Exp Mar Biol Ecol 199: 227-248.
61. Weis VM, Reynolds WS, (1999) Carbonic Anhydrase Expression and Synthesis in the Sea Anemone Anthopleura elegantissima Are Enhanced by the Presence of Dinoflagellate Symbionts. Physiological and Biochemical Zoology 72: 307-316.
62. Musa-Aziz R, Jiang L, Chen L-M, Behar K, Boron W, (2009) Concentration-Dependent Effects on Intracellular and Surface pH of Exposing Xenopus oocytes to Solutions Containing NH3/NH4(+). Journal of Membrane Biology 228: 15-31.
63. Soupene E, Inwood W, Kustu S, (2004) Lack of the Rhesus protein Rh1 impairs growth of the green alga Chlamydomonas reinhardtii at high CO2. Proceedings of the National Academy of Sciences of the United States of America 101: 7787-7792.
64. Uehlein N, Lovisolo C, Siefritz F, Kaldenhoff R, (2003) The tobacco aquaporin NtAQP1 is a membrane CO2 pore with physiological functions. Nature 425: 734-737.
65. Endeward V, Musa-Aziz R, Cooper GJ, Chen LM, Pelletier MF, et al. (2006) Evidence that aquaporin 1 is a major pathway for CO2 transport across the human erythrocyte membrane. The FASEB Journal 20: 1974-1981.
66. Salomao M, Zhang X, Yang Y, Lee S, Hartwig JH, et al. (2008) Protein 4.1R-dependent multiprotein complex: New insights into the structural organization of the red blood cell membrane. 105: 8026-8031.
67. van den Akker E, Satchwell TJ, Williamson RC, Toye AM, (2010) Band 3 multiprotein complexes in the red cell membrane; of mice and men. Blood Cells, Molecules, and Diseases 45: 1-8.
68. Grover R, Maguer J-F, Reynaud-Vaganay S, Ferrier-Pagès C, (2002) Uptake of ammonium by the scleractinian coral Stylophora pistillata: Effect of feeding, light, and ammonium concentrations. Limnology and Oceanography 47: 782-790.
69. Császár NBM, Seneca FO, vanOppen MJH, (2009) Variation in antioxidant gene expression in the scleractinian coral Acropora millepora under laboratory thermal stress. Marine Ecology and Progress Series 392: 93-102.
70. Coles SL, Brown BE, (2003) Coral Bleaching- Capacity for Acclimatization and Adaptation. Advances in Marine Biology 46: 183-223.
71. Vega Thurber R, Willner-Hall D, Rodriguez-Mueller B, Desnues C, Edwards RA, et al. (2009) Metagenomic analysis of stressed coral holobionts. Environmental Microbiology 11: 1752-1766.
72. Ritchie ME, Silver J, Oshlack A, Holmes M, Diyagama D, et al. (2007) A comparison of background correction methods for two-colour microarrays. Bioinformatics 23: 2700-2707.
73. de Hoon MJ, Imoto S, Nolan J, Miyano S, (2004) Open source clustering software. Bioinformatics 20: 1453-1454.
74. Rozen S, Skaletsky H, (2000) Primer3 on the WWW for general users and for biologist programmers. Methods in Molecular Biology 132: 365-386.
75. Vandesompele J, De Preter K, Pattyn F, Poppe B, Van Roy N, et al. (2002) Accurate normalization of real-time quantitative RT-PCR data by geometric averaging of multiple internal control genes. Genome Biology 3: research0034.0031-research0034.0011.
76. Blüthgen N, Brand K, Cajavec B, Swat M, Herzel H, et al. (2005) Biological Profiling of Gene Groups utilizing Gene Ontology. Genome Informatics 16: 106-115.
77. Corpet F, (1988) Multiple sequence alignment with hierarchical clustering. Nucl Acids Res 16: 10881-10890.
78. Abascal F, Zardoya R, Posada D, (2005) ProtTest: selection of best-fit models of protein evolution. Bioinformatics 21: 2104-2105.
79. Guindon S, Gascuel O, (2003) A simple, fast, and accurate algorithm to estimate large phylogenies by maximum likelihood. Syst Biol 52: 696-704.