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Insights on the genetic repertoire of the coral Mussismilia braziliensis endosymbiont Symbiodinium

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Abstract

Reef-building corals form a symbiotic association with photosynthetic dinoflagellates of the family Symbiodiniaceae. This symbiosis is crucial for the maintenance of coral reefs. In this work, we evaluate the effect of light conditions on the transcriptomic response of Symbiodinium CCMR0100 (ITS2 type A4), isolated from the Southwestern Atlantic Ocean endemic Mussismilia braziliensis. We obtained a total of 36,224 transcripts (N50 = 1007 bases, mean GC = 55.7%; ~25 Gb of assembled bases). We observed ecologically relevant transcripts encoding i. the complete antioxidant enzymatic system, ii. the recently described algal dimethylsulfoniopropionate (DMSP) lyase, and iii. The Mycosporine-like aminoacids (MAA) biosynthesis pathway. Cultures maintained in dark and light conditions yielded different transcriptomic profiles, and 48 transcripts were differentially expressed between these treatments. Expression of cytochrome P450 was inhibited by light, suggesting that endoplasmic reticulum monooxygenase activity might play a role in light-independent coral bleaching. Light conditions also triggered the induction of transcripts associated to chromatin condensation and mitosis, consistent with the light dependent progression of Symbiodiniaceae cell cycle. The repression of transcripts associated to the phosphatidylinositol (PI) signaling pathwaysuggests this pathway shall be related to light-induced morphological changes in Symbiodiniaceae cell.

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References

  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(6242):1466–1469

  2. Alexa A, Rahnenfuhrer J (2010) topGO: enrichment analysis for gene ontology. R package version, 2(0)

  3. Aranda M et al (2016) Genomes of coral dinoflagellate symbionts highlight evolutionary adaptations conducive to a symbiotic lifestyle. Sci Rep 6:39734

  4. Baker AC (2001) Reef corals bleach to survive change. Nature. 411(6839):765–766

  5. Baker AC (2003) Flexibility and specificity in coral-algal symbiosis: diversity, ecology, and biogeography of Symbiodinium. Annu Rev Ecol Evol Syst 34:661–689

  6. Balla T (2013) Phosphoinositides: tiny lipids with giant impact on cell regulation. Physiol Rev 93:1019–1137

  7. Banaszak AT, LaJeunesse TC, Trench RK (2000) The synthesis of mycosporine-like amino acids (MAAs) by cultured, symbiotic dinoflagellates. J Exp Mar Biol Ecol 249:219–233

  8. Barbrook AC, Voolstra CR, Howe CJ (2014) The chloroplast genome of a Symbiodinium sp. clade C3 isolate. Protist 165(1):1–13

  9. Baumgarten S et al (2013) Integrating microRNA and mRNA expression profiling in Symbiodinium microadriaticum, a dinoflagellate symbiont of reef-building corals. BMC Genomics 14:1

  10. Bayer T, Aranda M, Sunagawa S, Yum LK, Desalvo MK, Lindquist E, Coffroth MA, Voolstra CR, Medina M (2012) Symbiodinium transcriptomes: genome insights into the dinoflagellate symbionts of reef-building corals. PLoS One 7(4):e35269

  11. Carpenter KE, Abrar M, Aeby G, Aronson RB, Banks S, Bruckner A, Chiriboga A, Cortés J, Delbeek JC, Devantier L, Edgar GJ, Edwards AJ, Fenner D, Guzmán HM, Hoeksema BW, Hodgson G, Johan O, Licuanan WY, Livingstone SR, Lovell ER, Moore JA, Obura DO, Ochavillo D, Polidoro BA, Precht WF, Quibilan MC, Reboton C, Richards ZT, Rogers AD, Sanciangco J, Sheppard A, Sheppard C, Smith J, Stuart S, Turak E, Veron JE, Wallace C, Weil E, Wood E (2008) One-third of reef-building corals face elevated extinction risk from climate change and local impacts. Science 321(5888):560–563

  12. Decelle J et al (2018) Worldwide occurrence and activity of the reef-building coral Symbiont Symbiodinium in the Open Ocean. Curr Biol 28(22):3625–3633

  13. Díaz-Almeyda E, Thomé PE, El Hafidi M, Iglesias-Prieto R (2011) Differential stability of photosynthetic membranes and fatty acid composition at elevated temperature in Symbiodinium. Coral Reefs 30(1):217–225

  14. Díaz-Almeyda EM et al (2017) Intraspecific and interspecific variation in thermotolerance and photoacclimation in Symbiodinium dinoflagellates. Proc R Soc B 284(1868):20171767

  15. Dubousquet V, Gros E, Berteaux-Lecellier V, Viguier B, Raharivelomanana P, Bertrand C, Lecellier GJ (2016) Changes in fatty acid composition in the giant clam Tridacna maxima in response to thermal stress. Biol Open 5(10):1400–1407

  16. Dunlap WC, Yamamoto Y (1995) Small-molecule antioxidants in marine organisms: antioxidant activity of mycosporine-glycine. Comp Biochem Physiol B: Biochem Mol Biol 112(1):105–114

  17. Eddy S (2003) HMMER User’s guide. Biological sequence analysis using profile hidden Markov models

  18. Fitt WK, Trench RK (1983) The relation of diel patterns of cell division to diel patterns of motility in the symbiotic dinoflagellate Symbiodinium microadriaticum Freudenthal in culture. New Phytol 94(3):421–432

  19. Fu L, Niu B, Zhu Z, Wu S, Li W (2012) CD-HIT: accelerated for clustering the next generation sequencing data. Bioinformatics 28(23):3150–3152. https://doi.org/10.1093/bioinformatics/bts565

  20. Fujise L, Nitschke MR, Frommlet JC, Serôdio J, Woodcock S, Ralph PJ, Suggett DJ (2018) Cell cycle dynamics of cultured coral endosymbiotic microalgae (Symbiodinium) across different types (species) under alternate light and temperature conditions. J Eukaryot Microbiol 65(4):505–517

  21. Gao Q, Garcia-Pichel F (2011) Microbial ultraviolet sunscreens. Nat Rev Microbiol 9(11):791–802

  22. Garcia GD, Santos Ede O, Sousa GV, Zingali RB, Thompson CC, Thompson FL (2016) Metaproteomics reveals metabolic transitions between healthy and diseased stony coral Mussismilia braziliensis. Mol Ecol 25:4632–4644

  23. Gierz SL, Forêt S, Leggat W (2017) Transcriptomic analysis of thermally stressed Symbiodinium reveals differential expression of stress and metabolism genes. Front Plant Sci 28(8):271

  24. González-Pech RA, Ragan MA, Chan CX (2017) Signatures of adaptation and symbiosis in genomes and transcriptomes of Symbiodinium. Sci Rep 7(1):15021

  25. Gornik SG, Ford KL, Mulhern TD, Bacic A, McFadden G, Waller RF (2012) Loss of nucleosomal DNA condensation coincides with appearance of a novel nuclear protein in dinoflagellates. Curr Biol 22(24):2303–2312

  26. Grabherr MG et al (2011) Trinity: reconstructing a full-length transcriptome without a genome from RNA-Seq data. Nat Biotechnol 29(7):644

  27. Grottoli AG et al (2014) The cumulative impact of annual coral bleaching can turn some coral species winners into losers. Glob Chang Biol 20(12):3823–3833

  28. Hansen G, Daugbjerg N (2009) Symbiodinium natans sp. nov.: a “free living” dinoflagellate from Tenerife (Northeast Atlantic Ocean). J Phycol 45(1):251–263

  29. Hill R, Ulstrup KE, Ralph PJ (2009) Temperature induced changes in thylakoid membrane thermostability of cultured, freshly isolated, and expelled zooxanthellae from scleractinian corals. Bull Mar Sci 85(3):223–244

  30. Keller MD, Selvin RC, Claus W, Guillard RRL (1987) Media for the culture of oceanic ultraphytoplankton. J Phycol 23:633–638

  31. LaJeunesse TC (2001) Investigating the biodiversity, ecology, and phylogeny of endosymbiotic dinoflagellates in the genus Symbiodinium using the ITS region: in search of a “species” level marker. J Phycol 37(5):866–880

  32. LaJeunesse TC et al (2015) Symbiodinium necroappetens sp. nov. (Dinophyceae): an opportunist ‘zooxanthella’ found in bleached and diseased tissues of Caribbean reef corals. Eur J Phycol 50(2):223–238

  33. LaJeunesse TC, Parkinson JE, Gabrielson PW, Jeong HJ, Reimer JD, Voolstra CR, Santos SR (2018) Systematic revision of Symbiodiniaceae highlights the antiquity and diversity of coral endosymbionts. Curr Biol 28(16):2570–2580

  34. Langmead B, Salzberg S (2012) Fast gapped-read alignment with bowtie 2. Nat Methods 9:357–359

  35. Leggat W, Hoegh-Guldberg O, Dove S, Yellowlees D (2007) Analysis of an EST library from the dinoflagellate (Symbiodinium sp.) symbiont of reef building corals. J Phycol 43(5):1010–1021

  36. Lesser MP (2006) Oxidative stress in marine environments: biochemistry and physiological ecology. Annu Rev Physiol 68:253–278

  37. Levin RA et al. (2016) Sex, scavengers, and chaperones: transcriptome secrets of divergent Symbiodinium thermal tolerances. Mol Biol Evol 33(9):2201–2215

  38. Li B, Dewey CN (2011) RSEM: accurate transcript quantification from RNA-Seq data with or without a reference genome. BMC Bioinf 12(1):1

  39. Lin S, Cheng S, Song B, Zhong X, Lin X, Li W, Li L, Zhang Y, Zhang H, Ji Z, Cai M, Zhuang Y, Shi X, Lin L, Wang L, Wang Z, Liu X, Yu S, Zeng P, Hao H, Zou Q, Chen C, Li Y, Wang Y, Xu C, Meng S, Xu X, Wang J, Yang H, Campbell DA, Sturm NR, Dagenais-Bellefeuille S, Morse D (2015) The Symbiodinium kawagutii genome illuminates dinoflagellate gene expression and coral symbiosis. Science 350(6261):691–694

  40. Liu H et al (2018) Symbiodinium genomes reveal adaptive evolution of functions related to coral-dinoflagellate symbiosis. Commun Biol 1(1):95

  41. Martin M (2011) Cutadapt removes adapter sequences from high-throughput sequencing reads. EMBnet J 17(1):10

  42. McGinley MP, Suggett DJ, Warner ME (2013) Transcript patterns of chloroplast encoded genes in cultured Symbiodinium spp.(Dinophyceae): testing the influence of a light shift and diel periodicity. J Phycol 49(4):709–718

  43. McGinty ES, Pieczonka J, Mydlarz LD (2012) Variations in reactive oxygen release and antioxidant activity in multiple Symbiodinium types in response to elevated temperature. Microb Ecol 64(4):1000–1007

  44. McLenon AL, DiTullio GR (2012) Effects of increased temperature on dimethylsulfoniopropionate (DMSP) concentration and methionine synthase activity in Symbiodinium microadriaticum. Biogeochemistry 110(1–3):17–29

  45. Muller-Parker G, D’elia CF, Cook CB (2015) Interactions between corals and their symbiotic algae. InCoral reefs in the Anthropocene (pp. 99-116). Springer, Dordrecht.

  46. Mungpakdee S, Shinzato C, Takeuchi T, Kawashima T, Koyanagi R, Hisata K, Tanaka M, Goto H, Fujie M, Lin S, Satoh N, Shoguchi E (2014) Massive gene transfer and extensive RNA editing of a symbiotic dinoflagellate plastid genome. Genome Biol Evol 6(6):1408–1422

  47. Nunes F, Norris RD, Knowlton N (2009) Implications of isolation and low genetic diversity in peripheral populations of an amphi-Atlantic coral. Mol Ecol 18(20):4283–4297

  48. Oren A, Gunde-Cimerman N (2007) Mycosporines and mycosporine-like amino acids: UV protectants or multipurpose secondary metabolites? FEMS Microbiol Lett 269(1): 1–0, 10

  49. Parkinson JE, Baumgarten S, Michell CT, Baums IB, LaJeunesse T, Voolstra CR (2016) Gene expression variation resolves species and individual strains among coral-associated dinoflagellates within the genus Symbiodinium. Genome Biol Evol 8(3):665–680

  50. Picciani N et al (2016) Geographic patterns of Symbiodinium diversity associated with the coral Mussismilia hispida (Cnidaria, Scleractinia) correlate with major reef regions in the southwestern Atlantic Ocean. Mar Biol 163(11):236

  51. Polne-Fuller M (1991) A novel technique for preparation of axenic cultures of Symbiodinium (Pyrrophyta) through selective digestion by amoebae. J Phycol 27(4):552–554

  52. Quast C et al (2013) The SILVA ribosomal RNA gene database project: improved data processing and web-based tools. Nucleic Acids Res 41(D1):D590–D596

  53. R Core Team (2016) R: A language and environment for statistical computing

  54. Reynolds JM, Bruns BU, Fit WK, Schmidt GW (2008) Enhanced photoprotection pathways in symbiotic dinoflagellates of shallow-water corals and other cnidarians. PNAS 105(36):13674–13678

  55. Ritchie ME et al (2015) Limma powers differential expression analyses for RNA-sequencing and microarray studies. Nucleic Acids Res 43(7):e47. https://doi.org/10.1093/nar/gkv007

  56. Roberty S, Bailleul B, Berne N, Franck F, Cardol P (2014) PSI Mehler reaction is the main alternative photosynthetic electron pathway in Symbiodinium sp., symbiotic dinoflagellates of cnidarians. New Phytol 204(1):81–91

  57. Roberty S, Furla P, Plumier JC (2016) Differential antioxidant response between two Symbiodinium species from contrasting environments. Plant Cell Environ 39(12):2713–2724

  58. Robinson MD, McCarthy DJ, Smyth GK (2010) edgeR: a bioconductor package for differential expression analysis of digital gene expression data. Bioinformatics 26(1):139–140

  59. Rosic NN (2019) Mycosporine-like amino acids: making the foundation for organic personalised sunscreens. Marine Drugs 17(11):638

  60. Rosic NN, Dove S (2011) Mycosporine-like amino acids from coral dinoflagellates. Appl Environ Microbiol 77(24):8478–8486

  61. Rosic NN, Pernice M, Dunn S, Dove S, Hoegh-Guldberg O (2010) Differential regulation by heat stress of novel cytochrome P450 genes from the dinoflagellate symbionts of reef-building corals. Appl Environ Microbiol 76(9):2823–2829

  62. Rosic NN et al (2015) Unfolding the secrets of coral–algal symbiosis. ISME 9(4):844

  63. Rowan R, Knowlton N, Baker A, Jara J (1997) Landscape ecology of algal symbionts creates variation in episodes of coral bleaching. Nature 388(6639):265–269

  64. Ryu T, Mavromatis C, Bayer T, Voolstra C, Ravasi T (2011) Unexpected complexity of the reef-building coral Acropora millepora transcription factor network. BMC Syst Biol 5:58–58

  65. Santos SR, LaJeunesse TC (2006) Searchable database of Symbiodinium diversity - geographic and ecological diversity (SD2-GED). http://www.auburn.edu/~santosr/sd2_ged.htm. Auburn University, Auburn

  66. Santos SR, Taylor DJ, Coffroth MA (2001) Genetic comparisons of freshly isolated versus cultured symbiotic dinoflagellates: implications for extrapolating to the intact symbiosis. J Phycol 37:900–912

  67. Saragosti E, Tchernov D, Katsir A, Shaked Y (2010) Extracellular production and degradation of superoxide in the coral Stylophora pistillata and cultured Symbiodinium. PLoS One 5(9):e12508

  68. Schmieder R, Edwards R (2011) Quality control and preprocessing of metagenomic datasets. Bioinformatics 27(6):863–864

  69. Shoguchi E, Shinzato C, Kawashima T, Gyoja F, Mungpakdee S, Koyanagi R, Takeuchi T, Hisata K, Tanaka M, Fujiwara M, Hamada M, Seidi A, Fujie M, Usami T, Goto H, Yamasaki S, Arakaki N, Suzuki Y, Sugano S, Toyoda A, Kuroki Y, Fujiyama A, Medina M, Coffroth MA, Bhattacharya D, Satoh N (2013) Draft assembly of the Symbiodinium minutum nuclear genome reveals dinoflagellate gene structure. Curr Biol 23(15):1399–1408

  70. Shoguchi E, Shinzato C, Hisata K, Satoh N, Mungpakdee S (2015) The large mitochondrial genome of Symbiodinium minutum reveals conserved noncoding sequences between dinoflagellates and apicomplexans. Genome Biol Evol 7(8):2237–2244

  71. Shoguchi E, Beedessee G, Tada I, Hisata K, Kawashima T, Takeuchi T, Arakaki N, Fujie M, Koyanagi R, Roy MC, Kawachi M, Hidaka M, Satoh N, Shinzato C (2018) Two divergent Symbiodinium genomes reveal conservation of a gene cluster for sunscreen biosynthesis and recently lost genes. BMC Genomics 19(1):458

  72. Silva-Lima AW, Walter JM, Garcia GD, Ramires N, Ank G, Meirelles PM, Nobrega AF, Siva-Neto ID, Moura RL, Salomon PS, Thompson CC, Thompson FL (2015) Multiple Symbiodinium strains are hosted by the Brazilian endemic corals Mussismilia spp. Microb Ecol 70(2):301–310

  73. Silveira CB et al (2017) Bacterial community associated with the reef coral Mussismilia braziliensis's momentum boundary layer over a diel cycle. Front Microbiol 8:784

  74. Simão FA, Waterhouse RM, Ioannidis P, Kriventseva EV, Zdobnov EM (2015) BUSCO: assessing genome assembly and annotation completeness with single-copy orthologs. Bioinformatics 31(19):3210–3212

  75. Simpson MF et al (2008) Integrative analysis of RUNX1 downstream pathways and target genes. BMC Genomics 9(1):363

  76. Sorek M, Díaz-Almeyda EM, Medina M, Levy O (2004) Circadian clocks in symbiotic corals: the duet between Symbiodinium algae and their coral host. Mar Genomics 14:47–57

  77. Suggett DJ, Warner ME, Smith DJ, Davey P, Hennige S, Baker NR (2008) Photosynthesis and production of hydrogen peroxide by Symbiodinium (Pyrrhophyta) phylotypes with different thermal tolerances. J Phycol 44(4):948–956

  78. Suggett DJ et al (2012) Photobiology of corals from Brazil’s near-shore marginal reefs of Abrolhos. Mar Biol 159(7):1461–1473

  79. Sunda WK, Kieber DJ, Kiene R, Huntsman S (2002) An antioxidant function for DMSP and DMS in marine algae. Nature 418(6895):317–320

  80. Takahashi S, Yoshioka-Nishimura M, Nanba D, Badger MR (2013) Thermal acclimation of the symbiotic alga Symbiodinium spp. alleviates photobleaching under heat stress. Plant Physiol 161(1):477–485

  81. Tchernov D, Gorbunov MY, de Vargas C, Narayan Yadav S, Milligan AJ, Häggblom M, Falkowski PG (2004) Membrane lipids of symbiotic algae are diagnostic of sensitivity to thermal bleaching in corals. PNAS 101(37):13531–13535

  82. Teixeira CD et al (2019) Sustained mass coral bleaching (2016–2017) in Brazilian turbid-zone reefs: taxonomic, cross-shelf and habitat-related trends. Coral Reefs 38(4):801–813

  83. Tolleter D, Seneca FO, DeNofrio J, Krediet CJ, Palumbi SR, Pringle JR, Grossman AR (2013) Coral bleaching independent of photosynthetic activity. Curr Biol 23(18):1782–1786

  84. Villanueva MA, Barnay-Verdier S, Priouzeau F, Furla P (2015) Chloroplast and oxygen evolution changes in Symbiodinium sp. as a response to latrunculin and butanedione monoxime treatments under various light conditions. Photosynth Res 124(3):305–313

  85. Voolstra CR et al (2009) Evolutionary analysis of orthologous cDNA sequences from cultured and symbiotic dinoflagellate symbionts of reef-building corals (Dinophyceae: Symbiodinium). Comp Biochem Phys D 4(2):67–74

  86. Waller RF, Slamovits CH, Keeling PJ (2006) Lateral gene transfer of a multigene region from cyanobacteria to dinoflagellates resulting in a novel plastid-targeted fusion protein. Mol Biol Evol 23:1437–1443

  87. Wang LH et al (2008) Cell cycle propagation is driven by light–dark stimulation in a cultured symbiotic dinoflagellate isolated from corals. Coral Reefs 27(4):823

  88. Warner ME, Fitt WK, Schmidt GW (1999) Damage to photosystem II in symbiotic dinoflagellates: a determinant of coral bleaching. PNAS 96(14):8007–8012

  89. Weis VM (2008) Cellular mechanisms of cnidarian bleaching: stress causes the collapse of symbiosis. J Exp Biol 211(19):3059–3066

  90. Weston AJ et al. (2015) Proteomics links the redox state to calcium signalling during bleaching of the scleractinian coral Acropora microphthalma on exposure to high solar irradiance and thermal stress. Mol Cell Proteomics 14(3):585–595

  91. Xiang T, Nelson W, Rodriguez J, Tolleter D, Grossman AR (2015) Symbiodinium transcriptome and global responses of cells to immediate changes in light intensity when grown under autotrophic or mixotrophic conditions. Plant J 82(1):67–80

  92. Yakovleva I, Bhagooli R, Takemura A, Hidaka M (2004) Differential susceptibility to oxidative stress of two scleractinian corals: antioxidant functioning of mycosporine-glycine. Comp Biochem Physiol B: Biochem Mol Biol 139(4):721–730

  93. Yamashita H, Koike K (2013) Genetic identity of free living Symbiodinium obtained over a broad latitudinal range in the Japanese coast. Phycol Res 61(1):68–80

  94. Zhang J, Kobert K, Flouri T, Stamatakis A (2014) PEAR: a fast and accurate Illumina paired-end reAd mergeR. Bioinformatics 30(5):614–620

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Funding

This work was supported by CNPq, CAPES, and FAPERJ. AWSL acknowledges the financial support from Science Without Borders program from CNPQ, process 232399/2014–0. MM was supported by NSF OCE 1442206 and OCE 1642311.

Author information

AWSL conceived the study design, RNA extractions, the bioinformatic analysis and drafted the manuscript.

LSO and LL performed the transcriptome sequencing and prepared the MiSeq sequencing libraries.

JT participated in the discussion of the results and the draft manuscript, and the acquisition of funding.

MM, TV, and CLT participated in the discussion of the results and the draft manuscript.

FLT participated in the acquisition of funding, conceived the study design, discussion of the results and draft of the manuscript.

All authors read and approved the final manuscript.

Correspondence to Arthur W. Silva Lima or Fabiano L. Thompson.

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Silva Lima, A.W., Leomil, L., Oliveira, L. et al. Insights on the genetic repertoire of the coral Mussismilia braziliensis endosymbiont Symbiodinium. Symbiosis (2020). https://doi.org/10.1007/s13199-020-00664-1

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Keywords

  • Symbiodiniaceae
  • Symbiodinium
  • Transcriptome
  • Mycosporine-like aminoacids (MAA)
  • Differential expression