Adaptations to Endosymbiosis in a Cnidarian-Dinoflagellate Association: Differential Gene Expression and Specific Gene Duplications
Trophic endosymbiosis between anthozoans and photosynthetic dinoflagellates forms the key foundation of reef ecosystems. Dysfunction and collapse of symbiosis lead to bleaching (symbiont expulsion), which is responsible for the severe worldwide decline of coral reefs. Molecular signals are central to the stability of this partnership and are therefore closely related to coral health. To decipher inter-partner signaling, we developed genomic resources (cDNA library and microarrays) from the symbiotic sea anemone Anemonia viridis. Here we describe differential expression between symbiotic (also called zooxanthellate anemones) or aposymbiotic (also called bleached) A. viridis specimens, using microarray hybridizations and qPCR experiments. We mapped, for the first time, transcript abundance separately in the epidermal cell layer and the gastrodermal cells that host photosynthetic symbionts. Transcriptomic profiles showed large inter-individual variability, indicating that aposymbiosis could be induced by different pathways. We defined a restricted subset of 39 common genes that are characteristic of the symbiotic or aposymbiotic states. We demonstrated that transcription of many genes belonging to this set is specifically enhanced in the symbiotic cells (gastroderm). A model is proposed where the aposymbiotic and therefore heterotrophic state triggers vesicular trafficking, whereas the symbiotic and therefore autotrophic state favors metabolic exchanges between host and symbiont. Several genetic pathways were investigated in more detail: i) a key vitamin K–dependant process involved in the dinoflagellate-cnidarian recognition; ii) two cnidarian tissue-specific carbonic anhydrases involved in the carbon transfer from the environment to the intracellular symbionts; iii) host collagen synthesis, mostly supported by the symbiotic tissue. Further, we identified specific gene duplications and showed that the cnidarian-specific isoform was also up-regulated both in the symbiotic state and in the gastroderm. Our results thus offer new insight into the inter-partner signaling required for the physiological mechanisms of the symbiosis that is crucial for coral health.
Vyšlo v časopise:
Adaptations to Endosymbiosis in a Cnidarian-Dinoflagellate Association: Differential Gene Expression and Specific Gene Duplications. PLoS Genet 7(7): e32767. doi:10.1371/journal.pgen.1002187
Kategorie:
Research Article
prolekare.web.journal.doi_sk:
https://doi.org/10.1371/journal.pgen.1002187
Souhrn
Trophic endosymbiosis between anthozoans and photosynthetic dinoflagellates forms the key foundation of reef ecosystems. Dysfunction and collapse of symbiosis lead to bleaching (symbiont expulsion), which is responsible for the severe worldwide decline of coral reefs. Molecular signals are central to the stability of this partnership and are therefore closely related to coral health. To decipher inter-partner signaling, we developed genomic resources (cDNA library and microarrays) from the symbiotic sea anemone Anemonia viridis. Here we describe differential expression between symbiotic (also called zooxanthellate anemones) or aposymbiotic (also called bleached) A. viridis specimens, using microarray hybridizations and qPCR experiments. We mapped, for the first time, transcript abundance separately in the epidermal cell layer and the gastrodermal cells that host photosynthetic symbionts. Transcriptomic profiles showed large inter-individual variability, indicating that aposymbiosis could be induced by different pathways. We defined a restricted subset of 39 common genes that are characteristic of the symbiotic or aposymbiotic states. We demonstrated that transcription of many genes belonging to this set is specifically enhanced in the symbiotic cells (gastroderm). A model is proposed where the aposymbiotic and therefore heterotrophic state triggers vesicular trafficking, whereas the symbiotic and therefore autotrophic state favors metabolic exchanges between host and symbiont. Several genetic pathways were investigated in more detail: i) a key vitamin K–dependant process involved in the dinoflagellate-cnidarian recognition; ii) two cnidarian tissue-specific carbonic anhydrases involved in the carbon transfer from the environment to the intracellular symbionts; iii) host collagen synthesis, mostly supported by the symbiotic tissue. Further, we identified specific gene duplications and showed that the cnidarian-specific isoform was also up-regulated both in the symbiotic state and in the gastroderm. Our results thus offer new insight into the inter-partner signaling required for the physiological mechanisms of the symbiosis that is crucial for coral health.
Zdroje
1. TechnauUSteeleRE 2011 Evolutionary crossroads in developmental biology: Cnidaria. Development 138 1447 1458
2. VennAALoramJEDouglasAE 2008 Photosynthetic symbioses in animals. J Exp Bot 59 1069 1080
3. FurlaPAllemandDShickJMFerrier-PagesCRichierS 2005 The Symbiotic Anthozoan: A Physiological Chimera between Alga and Animal. Integr Comp Biol 45 595 604
4. YellowleesDReesTALeggatW 2008 Metabolic interactions between algal symbionts and invertebrate hosts. Plant Cell Environ 31 679 694
5. FurlaPAllemandDOrsenigoMN 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. WeisVM 1991 The induction of carbonic anhydrase in the symbiotic sea anemone Aiptasia pulchella. Biol Bull 180 496 504
7. MerleP-LSabouraultCRichierSAllemandDFurlaP 2007 Catalase characterization and implication in bleaching of a symbiotic sea anemone. Free Rad Biol Med 42 236 246
8. RichierSFurlaPPlantivauxAMerleP-LAllemandD 2005 Symbiosis-induced adaptation to oxidative stress. J Exp Biol 208 277 285
9. RichierSSabouraultCCourtiadeJZucchiniNAllemandD 2006 Oxidative stress and apoptotic events during thermal stress in the symbiotic sea anemone, Anemonia viridis. Febs J 273 4186 4198
10. BertucciATambuttéSSupuranCAllemandDZoccolaD 2011 A New Coral Carbonic Anhydrase in Stylophora pistillata. Marine Biotechnology 1 11
11. WeisVM 2008 Cellular mechanisms of Cnidarian bleaching: stress causes the collapse of symbiosis. J Exp Biol 211 3059 3066
12. MoyaATambuttéSBertucciATambuttéELottoS 2008 Carbonic Anhydrase in the Scleractinian Coral Stylophora pistillata. J Biol Chem 283 25475 25484
13. SchwarzJAWeisVM 2003 Localization of a symbiosis-related protein, Sym32, in the Anthopleura elegantissima-Symbiodinium muscatinei Association. Biol Bull 205 339 350
14. WeisVMAllemandD 2009 Physiology. What determines coral health? Science 324 1153 1155
15. BayLKNielsenHBJarmerHSenecaFvanOppenMJH 2009 Transcriptomic variation in a coral reveals pathways of clonal organisation. Marine Genomics 2 119 125
16. Rodriguez-LanettyMPhillipsWSWeisVM 2006 Transcriptome analysis of a cnidarian-dinoflagellate mutualism reveals complex modulation of host gene expression. BMC Genomics 7 23
17. VoolstraCRSchwarzJASchnetzerJSunagawaSDesalvoMK 2009 The host transcriptome remains unaltered during the establishment of coral-algal symbioses. Mol Ecol 18 1823 1833
18. DeSalvoMKVoolstraCRSunagawaSSchwarzJAStillmanJH 2008 Differential gene expression during thermal stress and bleaching in the Caribbean coral Montastraea faveolata. Mol Ecol 17 3952 3971
19. Rodriguez-LanettyMHariiSHoegh-GuldbergO 2009 Early molecular responses of coral larvae to hyperthermal stress. Mol Ecol 18 5101 5114
20. SabouraultCGanotPDeleuryEAllemandDFurlaP 2009 Comprehensive EST analysis of the symbiotic sea anemone, Anemonia viridis. BMC Genomics 10 333
21. BachvaroffTRPlaceAR 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. SlamovitsCHKeelingPJ 2008 Widespread recycling of processed cDNAs in dinoflagellates. Current Biology 18 R550 R552
23. WettenhallJMSmythGK 2004 limmaGUI: A graphical user interface for linear modeling of microarray data. Bioinformatics 20 3705 3706
24. ExpositoJYLarrouxCCluzelCValcourtULethiasC 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. MyllyharjuJKivirikkoKI 2004 Collagens, modifying enzymes and their mutations in humans, flies and worms. Trends Genet 20 33 43
26. HonoreB 2009 The rapidly expanding CREC protein family: members, localization, function, and role in disease. Bioessays 31 262 277
27. DouglasAE 1994 Symbiotic Interactions New York Oxford University Press Inc
28. SacherMKimYGLavieAOhBHSegevN 2008 The TRAPP complex: insights into its architecture and function. Traffic 9 2032 2042
29. ZwangYYardenY 2009 Systems Biology of Growth Factor-Induced Receptor Endocytosis. Traffic 10 349 363
30. CapassoMDecourseyTEDyerMJ 2010 pH regulation and beyond: unanticipated functions for the voltage-gated proton channel, HVCN1. Trends Cell Biol
31. Falcon-PerezJMDell'AngelicaEC 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. BarrFLambrightDG 2010 Rab GEFs and GAPs. Curr Opin Cell Biol 22 461 470
33. ChenMCChengYMSungPJKuoCEFangLS 2003 Molecular identification of Rab7 (ApRab7) in Aiptasia pulchella and its exclusion from phagosomes harboring zooxanthellae. Biochem Biophys Res Commun 308 586 595
34. ChenM-CHongM-CHuangY-SLiuM-CChengY-M 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. StamblerNDubinskyZ 1987 Energy relationships between Anemonia sulcata and its endosymbiotic zooxanthellae. Symbiosis 3 233 248
36. HansonRW 2005 Metabolism in the era of molecular biology. J Biol Chem 280 1705 1715
37. FoulonVAntonenkovVDCroesKWaelkensEMannaertsGP 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. KuoJLiangZ-CLinC-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. IkonenE 2008 Cellular cholesterol trafficking and compartmentalization. Nat Rev Mol Cell Biol 9 125 138
40. LiscumLSturleySL 2004 Intracellular trafficking of Niemann-Pick C proteins 1 and 2: obligate components of subcellular lipid transport. Biochim Biophys Acta 1685 22 27
41. VanceJE 2010 Transfer of cholesterol by the NPC team. Cell Metab 12 105 106
42. KimuraASakaguchiENonakaM 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. NonakaMKimuraA 2006 Genomic view of the evolution of the complement system. Immunogenetics 58 701 713
44. KvenneforsECLeggatWKerrCCAinsworthTDHoegh-GuldbergO 2010 Analysis of evolutionarily conserved innate immune components in coral links immunity and symbiosis. Dev Comp Immunol 34 1219 1229
45. RaykhelIAlanenHSaloKJurvansuuJNguyenVD 2007 A molecular specificity code for the three mammalian KDEL receptors. J Cell Biol 179 1193 1204
46. WallinRHutsonSM 2004 Warfarin and the vitamin K-dependent gamma-carboxylation system. Trends Mol Med 10 299 302
47. BandyopadhyayPK 2008 Vitamin K-dependent gamma-glutamylcarboxylation: an ancient posttranslational modification. Vitam Horm 78 157 184
48. OldenburgJMarinovaMMuller-ReibleCWatzkaM 2008 The vitamin K cycle. Vitam Horm 78 35 62
49. CoutuDLWuJHMonetteARivardGEBlosteinMD 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. WeisVMLevineRP 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. ReynoldsWSSchwarzJAWeisVM 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. NishimotoSKPricePA 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. HuangMRigbyACMorelliXGrantMAHuangG 2003 Structural basis of membrane binding by Gla domains of vitamin K-dependent proteins. Nat Struct Biol 10 751 756
54. AllemandDFurlaPBénazet-TambuttéS 1998 Mechanisms of carbon acquisition for endosymbiont photosynthesis in Anthozoa. Can J Bot 76 925 941
55. CookCMLanarasTColmanB 1986 Evidence for bicarbonate transport in species of red and brown macrophytic marine algae. J Exp Bot 37 977 984
56. KerbyNWRavenJA 1985 Transport and fixation of inorganic carbon by marine algae. Adv Bot Res 11 71 123
57. FurlaPGalganiIDurandIAllemandD 2000 Sources and mechanisms of inorganic carbon transport for coral calcification and photosynthesis. J Exp Biol 203 3445 3457
58. LeggatWMarendyEMBaillieBWhitneySMLudwigM 2002 Dinoflagellate symbioses: strategies and adaptations for the acquisition and fixation of inorganic carbon. Funct Plant Biol 29 309 322
59. WeisVM 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-MoghrabiSGoiranCAllemandDSpezialeNJaubertJ 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. WeisVMReynoldsWS 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-AzizRJiangLChenL-MBeharKBoronW 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. SoupeneEInwoodWKustuS 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. UehleinNLovisoloCSiefritzFKaldenhoffR 2003 The tobacco aquaporin NtAQP1 is a membrane CO2 pore with physiological functions. Nature 425 734 737
65. EndewardVMusa-AzizRCooperGJChenLMPelletierMF 2006 Evidence that aquaporin 1 is a major pathway for CO2 transport across the human erythrocyte membrane. The FASEB Journal 20 1974 1981
66. SalomaoMZhangXYangYLeeSHartwigJH 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 AkkerESatchwellTJWilliamsonRCToyeAM 2010 Band 3 multiprotein complexes in the red cell membrane; of mice and men. Blood Cells, Molecules, and Diseases 45 1 8
68. GroverRMaguerJ-FReynaud-VaganaySFerrier-PagèsC 2002 Uptake of ammonium by the scleractinian coral Stylophora pistillata: Effect of feeding, light, and ammonium concentrations. Limnology and Oceanography 47 782 790
69. CsászárNBMSenecaFOvanOppenMJH 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. ColesSLBrownBE 2003 Coral Bleaching - Capacity for Acclimatization and Adaptation. Advances in Marine Biology 46 183 223
71. Vega ThurberRWillner-HallDRodriguez-MuellerBDesnuesCEdwardsRA 2009 Metagenomic analysis of stressed coral holobionts. Environmental Microbiology 11 1752 1766
72. RitchieMESilverJOshlackAHolmesMDiyagamaD 2007 A comparison of background correction methods for two-colour microarrays. Bioinformatics 23 2700 2707
73. de HoonMJImotoSNolanJMiyanoS 2004 Open source clustering software. Bioinformatics 20 1453 1454
74. RozenSSkaletskyH 2000 Primer3 on the WWW for general users and for biologist programmers. Methods in Molecular Biology 132 365 386
75. VandesompeleJDe PreterKPattynFPoppeBVan RoyN 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. BlüthgenNBrandKCajavecBSwatMHerzelH 2005 Biological Profiling of Gene Groups utilizing Gene Ontology. Genome Informatics 16 106 115
77. CorpetF 1988 Multiple sequence alignment with hierarchical clustering. Nucl Acids Res 16 10881 10890
78. AbascalFZardoyaRPosadaD 2005 ProtTest: selection of best-fit models of protein evolution. Bioinformatics 21 2104 2105
79. GuindonSGascuelO 2003 A simple, fast, and accurate algorithm to estimate large phylogenies by maximum likelihood. Syst Biol 52 696 704
Štítky
Genetika Reprodukčná medicínaČlánok vyšiel v časopise
PLOS Genetics
2011 Číslo 7
- Je „freeze-all“ pro všechny? Odborníci na fertilitu diskutovali na virtuálním summitu
- Gynekologové a odborníci na reprodukční medicínu se sejdou na prvním virtuálním summitu
Najčítanejšie v tomto čísle
- Genome-Wide Association Study Identifies Novel Restless Legs Syndrome Susceptibility Loci on 2p14 and 16q12.1
- Loss of the BMP Antagonist, SMOC-1, Causes Ophthalmo-Acromelic (Waardenburg Anophthalmia) Syndrome in Humans and Mice
- Gene-Based Tests of Association
- Genome-Wide Association Study Identifies as a Susceptibility Gene for Pediatric Asthma in Asian Populations