Lineage-specific transcriptional profiles of Symbiodinium spp. Unaltered by heat stress in a coral host

Molecular Biology and Evolution

Volumn 31, Issue 6, 2014, Pages 1343-1352

  Barshis, Daniel J ^a,b   Ladner, Jason T ^a   Oliver, Thomas A ^a   Palumbi, Stephen R ^a  

^a STANFORD UNIVERSITY   (United States)

^b OLD DOMINION UNIVERSITY   (United States)

Author keywords

coral; Symbiodinium; thermal stress; transcriptomics

Indexed keywords

HEAT SHOCK PROTEIN; INTERNAL TRANSCRIBED SPACER 2; TRANSCRIPTOME; PROTOZOAL RNA;

ACROPORA; ACROPORA HYACINTHUS; ARTICLE; BLEACHING; CARBON FIXATION; CHLOROPLAST; CHLOROPLAST MEMBRANE COMPONENT; CLADISTICS; CORAL REEF; DINOFLAGELLATE; ENDOSYMBIONT; GENE EXPRESSION; GENE LOCUS; GENE ONTOLOGY; HEAT STRESS; HEAT TOLERANCE; MEMBRANE COMPONENT; MICROCLIMATE; NONHUMAN; ORTHOLOGY; PHOTOSYNTHESIS; RNA SEQUENCE; SYMBIODINIUM; SYMBIOSIS; THERMAL EXPOSURE; THERMOSTABILITY; THYLAKOID MEMBRANE; ANIMAL; CLASSIFICATION; GENE; GENE EXPRESSION PROFILING; GENE EXPRESSION REGULATION; GENETICS; HEAT; PHYLOGENY; PHYSIOLOGICAL STRESS; SEQUENCE ANALYSIS; SPECIES DIFFERENCE;

ANIMALS; CORAL REEFS; DINOFLAGELLIDA; GENE EXPRESSION PROFILING; GENE EXPRESSION REGULATION; GENES, PROTOZOAN; HOT TEMPERATURE; PHYLOGENY; RNA, PROTOZOAN; SEQUENCE ANALYSIS, RNA; SPECIES SPECIFICITY; STRESS, PHYSIOLOGICAL; SYMBIOSIS; TRANSCRIPTOME;

EID: 84901457589     PISSN: 07374038     EISSN: 15371719     Source Type: Journal    
DOI: 10.1093/molbev/msu107     Document Type: Article

References (71)

1. Abrego D, Ulstrup KE, Willis BL, van Oppen MJH. 2008. Species-specific interactions between algal endosymbionts and coral hosts define their bleaching response to heat and light stress. Proc R Soc Lond Ser B Biol Sci. 275:2273-2282.
2. Abreu RD, Penalva LO, Marcotte EM, Vogel C. 2009. Global signatures of protein and mRNA expression levels. Mol Biosyst. 5:1512-1526.
3. Anders S, Huber W. 2010. Differential expression analysis for sequence count data. Genome Biol. 11:R106.
4. Baker AC, Starger CJ, McClanahan TR, Glynn PW. 2004. Corals' adaptive response to climate change. Nature 430:741-741.
5. Barshis D, Ladner J, Oliver TA, Seneca F, Traylor-Knowles N, Palumbi SR. 2013. Genomic basis for coral resilience to climate change. Proc Natl Acad Sci USA. 110:1387-1392.
6. Barshis DJ, Stillman JH, Gates RD, Toonen RJ, Smith LW, Birkeland C. 2010. Protein expression and genetic structure of the coral Porites lobata in an environmentally extreme Samoan back reef: does host genotype limit phenotypic plasticity? Mol Ecol. 19:1705-1720.
7. Baskett ML, Gaines SD, Nisbet RM. 2009. Symbiont diversity may help coral reefs survive moderate climate change. Ecol Appl. 19:3-17.
8. Baumgarten S, Bayer T, Aranda M, Liew YJ, Carr A, Micklem G, Voolstra CR. 2013. Integrating microRNA and mRNA expression profiling in Symbiodinium microadriaticum, a dinoflagellate symbiont of reefbuilding corals. BMC Genomics 14:704.
9. Bayer T, Aranda M, Sunagawa S, Yum L, DeSalvo M, Lindquist E, Coffroth MA, Voolstra CR, Medina M. 2012. Symbiodinium transcriptomes: genome insights into the dinoflagellate symbionts of reef-building corals. PLoS One 7:e35269.
10. Beck A, Weng Z, Witten D, Zhu S, Foley J, Lacroute P, Smith C, Tibshirani R, van de Rijn M, Sidow A, et al. 2010. 3'-End sequencing for expression quantification (3SEQ) from archival tumor samples. PLoS One 5: 1-11.
11. Bellantuono AJ, Granados-Cifuentes C, Miller DJ, Hoegh-Guldberg O, Rodriguez-Lanetty M. 2012. Coral thermal tolerance: tuning gene expression to resist thermal stress. PLoS One 7:e50685.
12. Bellantuono AJ, Hoegh-Guldberg O, Rodriguez-Lanetty M. 2012. Resistance to thermal stress in corals without changes in symbiont composition. Proc R Soc Lond Ser B Biol Sci. 279:1100-1107.
13. Benjamini Y, Hochberg Y. 1995. Controlling the false discovery rate: a practical and powerful approach to multiple testing. J Roy Stat Soc Ser B. 57:289-300.
14. Berkelmans R, van Oppen MJH. 2006. The role of zooxanthellae in the thermal tolerance of corals: a 'nugget of hope' for coral reefs in an era of climate change. Proc R Soc Lond Ser B Biol Sci. 273:2305-2312.
15. Buddemeier RW, Fautin DG. 1993. Coral bleaching as an adaptive mechanism. A testable hypothesis. Bioscience 43:320-325.
16. Cantin N, van Oppen MJH, Willis BL, Mieog JC, Negri A. 2009. Juvenile corals can acquire more carbon from high-performance algal symbionts. Coral Reefs 28:405-414.
17. Carpenter KE, Abrar M, Aeby G, Aronson RB, Banks S, Bruckner A, Chiriboga A, Cortes J, Delbeek JC, DeVantier L, et al. 2008. Onethird of reef-building corals face elevated extinction risk from climate change and local impacts. Science 321:560-563.
18. Cheviron ZA, Whitehead A, Brumfield RT. 2008. Transcriptomic variation and plasticity in rufous-collared sparrows (Zonotrichia capensis) along an altitudinal gradient. Mol Ecol. 17:4556-4569.
19. Craig P, Birkeland C, Belliveau S. 2001. High temperatures tolerated by a diverse assemblage of shallow-water corals in American Samoa. Coral Reefs 20:185-189.
20. De Wit P, Pespeni MH, Ladner JT, Barshis DJ, Seneca F, Jaris H, Therkildsen NO, Morikawa M, Palumbi SR. 2012. The simple fool's guide to population genomics via RNA-Seq: an introduction to high-throughput sequencing data analysis. Mol Ecol Resour. 12: 1058-1067.
21. DeSalvo MK, Voolstra CR, Sunagawa S, Schwarz JA, Stillman JH, Coffroth MA, Szmant AM, Medina M. 2008. Differential gene expression during thermal stress and bleaching in the Caribbean coral Montastraea faveolata. Mol Ecol. 17:3952-3971.
22. Fabricius KE, Mieog JC, Colin PL, Idip D, van Oppen MJH. 2004. Identity and diversity of coral endosymbionts (zooxanthellae) from three Palauan reefs with contrasting bleaching, temperature and shading histories. Mol Ecol. 13:2445-2458.
23. Fagan T, Morse D, Hastings JW. 1999. Circadian synthesis of a nuclearencoded chloroplast glyceraldehyde-3-phosphate dehydrogenase in the dinoflagellate Gonyaulax polyedra is translationally controlled. Biochemistry 38:7689-7695.
24. Gasch AP, Spellman PT, Kao CM, Carmel-Harel O, Eisen MB, Storz G, Botstein D, Brown PO. 2000. Genomic expression programs in the response of yeast cells to environmental changes. Mol Biol Cell. 11: 4241-4257.
25. Gates RD, Baghdasarian G, Muscatine L. 1992. Temperature stress causes host cell detachment in symbiotic cnidarians implications for coral bleaching. Biol Bull. 182:324-332.
26. Guo R, Ki J-S. 2012. Differential transcription of heat shock protein 90 (HSP90) in the dinoflagellate Prorocentrum minimum by copper and endocrine-disrupting chemicals. Ecotoxicology 21: 1448-1457.
27. Hallock P. 1981. Algal symbiosis: a mathematical analysis. Mar Biol. 62: 249-255.
28. Hoegh-Guldberg O, Mumby PJ, Hooten AJ, Steneck RS, Greenfield P, Gomez E, Harvell CD, Sale PF, Edwards AJ, Caldeira K, et al. 2007. Coral reefs under rapid climate change and ocean acidification. Science 318:1737-1742.
29. Howells EJ, Beltran VH, Larsen NW, Bay LK, Willis BL, Van Oppen MJH. 2012. Coral thermal tolerance shaped by local adaptation of photosymbionts. Nat Climate Change. 2:116-120.
30. Hughes TP, Baird AH, Bellwood DR, Card M, Connolly SR, Folke C, Grosberg R, Hoegh-Guldberg O, Jackson JBC, Kleypas J, et al. 2003. Climate change, human impacts, and the resilience of coral reefs. Science 301:929-933.
31. Jones AM, Berkelmans R, van Oppen MJH, Mieog JC, SinclairW. 2008. A community change in the algal endosymbionts of a scleractinian coral following a natural bleaching event: field evidence of acclimatization. Proc R Soc Lond Ser B Biol Sci. 275:1359-1365.
32. Ladner JT, Barshis DJ, Palumbi SR. 2012. Protein evolution in two cooccurring types of Symbiodinium: an exploration into the genetic basis of thermal tolerance in Symbiodinium clade D. BMC Evol Biol. 12:217.
33. Ladner JT, Palumbi SR. 2012. Extensive sympatry, cryptic diversity and introgression throughout the geographic distribution of two coral species complexes. Mol Ecol. 21:2224-2238.
34. Leggat W, Seneca F, Wasmund K, Ukani L, Yellowlees D, Ainsworth T. 2011a. Differential responses of the coral host and their algal symbiont to thermal stress. PLoS One 6:e26687.
35. Leggat W, Yellowlees D, Medina M. 2011b. Recent progress in Symbiodinium transcriptomics. J Exp Mar Biol Ecol. 408:120-125.
36. Li H, Durbin R. 2009. Fast and accurate short read alignment with Burrows Wheeler transform. Bioinformatics 25:1754-1760.
37. Lien Y-T, Nakano Y, Plathong S, Fukami H, Wang J-T, Chen CA. 2007. Occurrence of the putatively heat-tolerant Symbiodinium phylotype D in high-latitudinal outlying coral communities. Coral Reefs 26: 35-44.
38. Little AF, van Oppen MJH, Willis BL. 2004. Flexibility in algal endosymbioses shapes growth in reef corals. Science 304: 1492-1494.
39. Lockwood BL, Sanders JG, Somero GN. 2010. Transcriptomic responses to heat stress in invasive and native blue mussels (genus Mytilus): molecular correlates of invasive success. J Exp Biol. 213:3548-3558.
40. Lu P, Vogel C, Wang R, Yao X, Marcotte EM. 2007. Absolute protein expression profiling estimates the relative contributions of transcriptional and translational regulation. Nat Biotechnol. 25:117-124.
41. Mancia A, Warr W, Chapman RW. 2008. A transcriptomic analysis of the stress induced by capture-release health assessment studies in wild dolphins (Tursiops truncatus). Mol Ecol. 17:2581-2589.
42. Marshall PA, Baird AH. 2000. Bleaching of corals on the Great Barrier Reef: differential susceptibilities among taxa. Coral Reefs 19: 155-163.
43. Meyer E, Aglyamova GV, Matz MV. 2011. Profiling gene expression responses of coral larvae (Acropora millepora) to elevated temperature and settlement inducers using a novel RNA-Seq procedure. Mol Ecol. 20:3599-3616.
44. Meyer E, Davies S, Wang S, Willis BL, Abrego D, Juenger TE, Matz MV. 2009. Genetic variation in responses to a settlement cue and elevated temperature in the reef-building coral Acropora millepora. Mar Ecol Prog Ser. 392:81-92.
45. Middlebrook R, Hoegh-Guldberg O, Leggat W. 2008. The effect of thermal history on the susceptibility of reef-building corals to thermal stress. J Exp Biol. 211:1050-1056.
46. Min XJ, Butler G, Storms R, Tsang A. 2005. OrfPredictor: predicting protein-coding regions in EST-derived sequences. Nucleic Acids Res. 33:W677-W680.
47. Mortazavi A,Williams BA,McCue K, Schaeffer L,Wold B. 2008. Mapping and quantifying mammalian transcriptomes by RNA-Seq. Nat Methods. 5:621-628.
48. Muscatine L, Porter J. 1977. Reef corals: mutualistic symbioses adapted to nutrient-poor environments. Bioscience 27:454-460.
49. Mustroph A, Lee SC, Oosumi T, Zanetti ME, Yang HJ, Ma K, Yaghoubi-Masihi A, FukaoT, Bailey-Serres J. 2010. Cross-kingdomcomparison of transcriptomic adjustments to low-oxygen stress highlights conserved and plant-specific responses. Plant Physiol. 152:1484-1500.
50. Nagalakshmi U, Wang Z, Waern K, Shou C, Raha D, Gerstein M, Snyder M. 2008. The transcriptional landscape of the yeast genome defined by RNA sequencing. Science 320:1344-1349.
51. Oliver TA, Palumbi SR. 2009. Distributions of stress-resistant coral symbionts match environmental patterns at local but not regional scales. Mar Ecol Prog Ser. 378:93-103.
52. Oliver TA, Palumbi SR. 2011. Many corals host thermally resistant symbionts in high-temperature habitat. Coral Reefs 30:241-250.
53. Pandolfi JM, Connolly SR, Marshall DJ, Cohen AL. 2011. Projecting coral reef futures under global warming and ocean acidification. Science 333:418-422.
54. Paradis E, Claude J, Strimmer K. 2004. APE: analyses of phylogenetics and evolution in R language. Bioinformatics 20:289-290.
55. Pochon X, Gates RD. 2010. A new Symbiodinium clade (Dinophyceae) from soritid foraminifera in Hawai'i. Mol Phylogenet Evol. 56:492-497.
56. Pochon X, Montoya-Burgos JI, Stadelmann B, Pawlowski J. 2006. Molecular phylogeny, evolutionary rates, and divergence timing of the symbiotic dinoflagellate genus Symbiodinium. Mol Phylogenet Evol. 38:20-30.
57. Podrabsky JE, Somero GN. 2004. Changes in gene expression associated with acclimation to constant temperatures and fluctuating daily temperatures in an annual killifish Austrofundulus limnaeus. J Exp Biol. 207:2237-2254.
58. Polato NR, Voolstra CR, Schnetzer J, DeSalvo MK, Randall CJ, Szmant AM, Medina M, Baums IB. 2010. Location-specific responses to thermal stress in larvae of the reef-building coral Montastraea faveolata. PLoS One 5:e11221.
59. Putnam HM, Mayfield AB, Fan TY, Chen CS, Gates RD. 2013. The physiological and molecular responses of larvae from the reef-building coral Pocillopora damicornis exposed to near-future increases in temperature and pCO2. Mar Biol. 160:2157-2173.
60. Remm M, Storm CE, Sonnhammer EL. 2001. Automatic clustering of orthologs and in-paralogs from pairwise species comparisons. J Mol Biol. 314:1041-1052.
61. Richier S, Furla P, Plantivaux A, Merle PL, Allemand D. 2005. Symbiosisinduced adaptation to oxidative stress. J Exp Biol. 208:277-285.
62. Rosic N, Pernice M, Dove S, Dunn S, Hoegh-Guldberg O. 2011. Gene expression profiles of cytosolic heat shock proteins Hsp70 and Hsp90 from symbiotic dinoflagellates in response to thermal stress: possible implications for coral bleaching. Cell Stress Chaperones. 16:69-80.
63. Rosic N, 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. 76:2823-2829.
64. Sotka EE, Thacker RW. 2005. Do some corals like it hot? Trends Ecol Evol. 20:59-62.
65. Stat M, Gates RD. 2011. Clade D Symbiodinium in scleractinian corals: a "nugget" of hope, a selfish opportunist, an ominous sign, or all of the above. J Mar Biol. 2011:1-9.
66. Stat M, Morris E, Gates RD. 2008. Functional diversity in coral-dinoflagellate symbiosis. Proc Natl Acad Sci USA. 105:9256-9261.
67. Suzuki R, Shimodaira H. 2006. Pvclust: an R package for assessing the uncertainty in hierarchical clustering. Bioinformatics 22:1540.
68. Tchernov D, Gorbunov M, de Vargas C, Yadav S, Milligan A, Haggblom M, Falkowski P. 2004. Membrane lipids of symbiotic algae are diagnostic of sensitivity to thermal bleaching in corals. Proc Natl Acad Sci USA. 101:13531-13535.
69. Teets NM, Peyton JT, Colinet H, Renault D, Kelley JL, Kawarasaki Y, Lee RE, Denlinger DL. 2012. Gene expression changes governing extreme dehydration tolerance in an Antarctic insect. Proc Natl Acad Sci USA. 109:20744-20749.
70. Teranishi KS, Stillman JH. 2007. A cDNA microarray analysis of the response to heat stress in hepatopancreas tissue of the porcelain crab Petrolisthes cinctipes. Comp Biochem Physiol D. 2: 53-62.
71. Zheng Q, Wang XJ. 2008. GOEAST: a web-based software toolkit for Gene Ontology enrichment analysis. Nucleic Acids Res. 36: W358-W363.