Ocean acidification research in the 'post-genomic' era: Roadmaps from the purple sea urchin Strongylocentrotus purpuratus

Comparative Biochemistry and Physiology -Part A : Molecular and Integrative Physiology

Volumn 185, Issue , 2015, Pages 33-42

  Evans, Tyler G ^a   Padilla Gamiño, Jacqueline L ^b   Kelly, Morgan W ^c   Pespeni, Melissa H ^d   Chan, Francis ^e   Menge, Bruce A ^e   Gaylord, Brian ^f   Hill, Tessa M ^f   Russell, Ann D ^g   Palumbi, Stephen R ^h   Sanford, Eric ^f   Hofmann, Gretchen E ⁱ  

^a CALIFORNIA STATE UNIVERSITY   (United States)

^b CALIFORNIA STATE UNIVERSITY   (United States)

^c LOUISIANA STATE UNIVERSITY   (United States)

^d UNIVERSITY OF VERMONT   (United States)

^e OREGON STATE UNIVERSITY   (United States)

^f UNIVERSITY OF CALIFORNIA DAVIS   (United States)

^g UNIVERSITY OF CALIFORNIA   (United States)

^h STANFORD UNIVERSITY   (United States)

ⁱ UNIVERSITY OF CALIFORNIA   (United States)

Author keywords

Adaptation; Climate change; Gene expression; Genomics; Ocean acidification; RNA seq; Strongylocentrotus purpuratus; Transcriptomics; Urchin

Indexed keywords

SEA WATER; CARBON DIOXIDE;

ACIDIFICATION; ECOSYSTEM; ENVIRONMENTAL FACTOR; GENE IDENTIFICATION; GENOMICS; HOMEOSTASIS; MARINE SPECIES; NONHUMAN; PH; REVIEW; SEA; STRONGYLOCENTROTUS PURPURATUS; SURVIVAL; TRANSCRIPTOMICS; ADAPTIVE BEHAVIOR; ANIMAL; CHEMISTRY; CLIMATE CHANGE; GENETICS; HUMAN; PHYSIOLOGY;

ECHINOIDEA; STRONGYLOCENTROTUS PURPURATUS;

ADAPTATION, PSYCHOLOGICAL; ANIMALS; CARBON DIOXIDE; CLIMATE CHANGE; GENOMICS; HUMANS; HYDROGEN-ION CONCENTRATION; SEAWATER; STRONGYLOCENTROTUS PURPURATUS;

EID: 84925605857     PISSN: 10956433     EISSN: 15314332     Source Type: Journal    
DOI: 10.1016/j.cbpa.2015.03.007     Document Type: Review

References (120)

1. Andersson A.J., Mackenzie F.T. Revisiting four scientific debates in ocean acidification research. Biogeosciences 2012, 9:893-905.
2. Barth J.A., Menge B.A., Lubchenco J., Chan F., Bane J.M., Kirincich A.R., McManus M.A., Nielsen K.J., Pierce S.D., Washburn L. Delayed upwelling alters nearshore coastal ocean ecosystems in the northern California current. Proc. Natl. Acad. Sci. U. S. A. 2007, 104:3719-3724.
3. Bell J.T., Spector T.D. A twin approach to unraveling epigenetics. Trends Genet. 2011, 27:116-125.
4. 2. Philos. Trans. R. Soc. Lond. B Biol. Sci. 2013, 368:20130049.
5. Boley N., Stoiber M.H., Booth B.W., Wan K.H., Hoskins R.A., Bickel P.J., Celniker S.E., Brown J.B. Genome-guided transcript assembly by integrative analysis of RNA sequence data. Nat. Biotechnol. 2014, 32:341-346.
6. Boyd P.W. Beyond ocean acidification. Nat. Geosci. 2011, 4:273-274.
7. Byrne M., Ho M., Wong E., Soars M.A., Selvakumaraswamy P., Shepard-Brennard H., Dworjanyn S.A., Davis A.R. Unshelled abalone and corrupted urchins: development of marine calcifiers in a changing ocean. Proc. R. Soc. B 2011, 278:2376-2383.
8. 2 ocean on calcification and development in sea urchin larvae, a synthesis from the tropics to the poles. Proc. R. Soc. B 2013, 368:20120439.
9. Caldeira K., Wickett M.E. Oceanography: anthropogenic carbon and ocean pH. Nature 2003, 425:365-365.
10. Carter H.A., Ceballos-Osuna L., Miller N.A., Stillman J.H. Impact of ocean acidification on metabolism and energetics during early life stages of the intertidal porcelain crab Petrolisthes cinctipes. J. Exp. Biol. 2013, 216:1412-1422.
11. Collard M., Dery A., Dehairs F., Dubois P. Euechinoidea and Cidaroidea respond differently to ocean acidification. Comp. Biochem. Physiol. A 2014, 174:45-55.
12. Collins S., Rost B., Rynearson T.A. Evolutionary potential of marine phytoplankton under ocean acidification. Evol. Appl. 2014, 7:140-155.
13. Cossins A., Fraser J., Hughes M., Gracey A. Post-genomic approaches to understanding the mechanisms of environmentally induced phenotypic plasticity. J. Exp. Biol. 2006, 209:2328-2336.
14. Crain C.M., Kroeker K., Halpern B.S. Interactive and cumulative effects of multiple human stressors in marine systems. Ecol. Lett. 2008, 11:1304-1315.
15. Crawford D.L., Oleksiak M.F. The biological importance of measuring individual variation. J. Exp. Biol. 2007, 210:1613-1621.
16. De Wit P., Palumbi S.R. Transcriptome-wide polymorphisms of red abalone (Haliotis rufscens) reveal patterns of gene flow and local adaptation. Mol. Ecol. 2012, 22:2884-2897.
17. De Wit P., Pespeni M.H., Ladner J.T., Barshis D.J., Seneca F., Jaris H., Therkildsen N.O., Morikawa M., Palumbi S.R. The simple fool's guide to population genomics via RNA-Seq: an introduction to high-throughput sequencing data analysis. Mol. Ecol. Resour. 2012, 12:1058-1067.
18. Doney S.C., Schimel D.S. Carbon and climate system coupling on timescales from the precambrian to the anthropocene. Annu. Rev. Environ. Resour. 2007, 32:31-66.
19. 2 problem. Annu. Rev. Mar. Sci. 2009, 1:169-192.
20. Doney S.C., Ruckelshaus M., Emmett Duffy J., Barry J.P., Chan F., English C.A., Galindo H.M., Grebmeier J.M., Hollowed A.B., Knowlton N., Polovina J., Rabalais N.N., Sydeman W.J., Talley L.D. Climate change impacts on marine ecosystems. Annu. Rev. Mar. Sci. 2011, 4:11-37.
21. Dow J.A.T. Integrative physiology, functional genomics and the phenotype gap: a guide for comparative physiologists. J. Exp. Biol. 2007, 210:1632-1640.
22. Dupont S., Ortega-Martínez O., Thorndyke M. Impact of near-future ocean acidification on echinoderms. Ecotoxicology 2010, 19(3):449-462.
23. Dupont S., Dorey N., Stumpp M., Melzner F., Thorndyke M. Long-term and trans-life-cycle effects of exposure to ocean acidification in the green sea urchin Strongylocentrotus droebachiensis. Mar. Biol. 2013, 160:1835-1843.
24. 14carbon. Fish. Bull. 2003, 101(915):922.
25. 2 world: Synergistic effects of elevated temperature and carbon dioxide on the metabolic rates of Antarctic notothenioids. Comp. Biochem. Physiol. A 2013, 164:154-161.
26. Evans T.G. Considerations for the use of transcriptomics in identifying the 'genes that matter' for environmental adaptation. J. Exp. Biol. 2015, (in press).
27. Evans T.G., Hofmann G.E. Defining the limits of physiological plasticity: how gene expression can assess and predict the consequences of ocean change. Philos. Trans. R. Soc. Lond. B Biol. Sci. 2012, 367:1733-1745.
28. Evans T.G., Watson-Wynn P. Effects of seawater acidification on gene expression: resolving broader-scale trends in sea urchins. Biol. Bull. 2014, 226:237-254.
29. Evans T.G., Chan F., Menge B.A., Hofmann G.E. Transcriptomic responses to ocean acidification in larval sea urchins from a naturally variable pH environment. Mol. Ecol. 2013, 22:1609-1625.
30. Fabry V.J., Seibel B.A., Feely R.A., Orr J.C. Impacts of ocean acidification on marine fauna and ecosystem processes. ICES J. Mar. Sci. 2008, 65:414-432.
31. Fassbender A.J., Sabine C.L., Feely R.A., Langdon C., Mordy C.W. Inorganic carbon dynamics during northern California coastal upwelling. Cont. Shelf Res. 2011, 31:1180-1192.
32. Feely R.A., Sabine C.L., Hernandez-Ayon J.M., Ianson D., Hales B. Evidence for upwelling of corrosive "acidified" water onto the continental shelf. Science 2008, 320:1490-1492.
33. Field D.B., Baumgartner T.R., Charles C.D., Ferreira-Bartrina V., Ohman M.D. Planktonic foraminifera of the California Current reflect 20th-century warming. Science 2006, 311:63-66.
34. Garcia-Reyes M., Largier J. Observations of increased wind-driven coastal upwelling off central California. J. Geophys. Res. 2010, 115:C04011.
35. Grabherr M.G., Haas B.J., Levin J.Z., Thompson D.A., Amit I., Adiconis X., Fan L., Raychowdhury R., Zeng Q., Chen Z., Mauceli E., Hacohen N., Gnirke A., Rhind N., di Palma F., Birren B.W., Nusbaum C., Lindblad-Toh K., Friedman N., Regev A. Full-length transcriptome assembly from RNA-Seq data without a reference genome. Nat. Biotechnol. 2011, 29:644-652.
36. Gruber N. Warming up, turning sour, losing breath: ocean biogeochemistry under global change. Philos. Trans. R. Soc. A 2011, 369:1980-1996.
37. Gruber N., Hauri C., Lachkar Z., Loher D., Frölicher T.L., Plattner G.-K. Rapid progression of ocean acidification in the California Current System. Science 2012, 337:220-223.
38. Hall-Spencer J.M., Rodolfo-Metalpa R., Martin S., Ransome E., Fine M., Turner S.M., Rowley S.J., Tedesco D., Buia M.-C. Volcanic carbon dioxide vents show ecosystem effects of ocean acidification. Nature 2008, 454:96-99.
39. Hauri C., Gruber N., Plattner G.-K., Alin S., Feely R.A., Hales B., Wheeler P.A. Ocean acidification in the California Current System. Oceanography 2009, 22:60-71.
40. Hauri C., Gruber N., Vogt M., Doney S.C., Feely R.A., Lachkar Z., Leinweber A., McDonnell A.M.P., Munnich M., Plattner G.K. Spatiotemporal variability and long-term trends of ocean acidification in the California Current System. Biogeosciences 2013, 10:193-216.
41. Hermisson J., Pennings P.S. Soft sweeps: molecular population genetics of adaptation from standing genetic variation. Genetics 2005, 169:2335-2352.
42. Hoegh-Guldberg O., Bruno J.F. The impact of climate change on the world's marine ecosystems. Science 2010, 328:1523-1528.
43. Hoegh-Guldberg O., Cai R., Poloczanska E.S., Brewer P.G., Sundby S., Hilmi K., Fabry V.J., Jung S. The Ocean. Climate Change 2014: Impacts, Adaptation, and Vulnerability. Part B: Regional Aspects. Contribution of Working Group II to the Fifth Assessment Report of the Intergovernmental Panel on Climate Change 2014, 1655-1731. Cambridge University Press, Cambridge, United Kingdom and New York, NY, USA. V.R. Barros, C.B. Field, D.J. Dokken, M.D. Mastrandrea, K.J. Mach, T.E. Bilir, M. Chatterjee, K.L. Ebi, Y.O. Estrada, R.C. Genova, B. Girma, E.S. Kissel, A.N. Levy, S. MacCracken, P.R. Mastrandrea, L.L. White (Eds.).
44. Hofmann G.E., Todgham A.E. Living in the now: physiological mechanisms to tolerate a rapidly changing environment. Annu. Rev. Physiol. 2010, 72:127-145.
45. Hofmann G.E., Barry J.P., Edmunds P.J., Gates R.D., Hutchins D.A., Klinger T., Sewell M.A. The effect of ocean acidification on calcifying organisms in marine ecosystems: an organism-to-ecosystem perspective. Annu. Rev. Ecol. Evol. Syst. 2010, 41:127-147.
46. Hofmann G.E., Smith J.E., Johnson K.S., Send U., Levin L.A., Micheli F., Paytan A., Price N.N., Peterson B., Takeshita Y., Matson P.G., Crook E.D., Kroeker K.J., Gambi M.C., Rivest E.B., Frieder C.A., Yu P.C., Martz T.R. High-frequency dynamics of ocean pH: a multi-ecosystem comparison. PLoS One 2011, 6:e28983.
47. Hofmann G.E., Evans T.G., Kelly M.W., Padilla-Gamiño J.L., Blanchette C.A., Washburn L., Chan F., McManus M.A., Menge B.A., Gaylord B., Hill T.M., Sanford E., LaVigne M., Rose J.M., Kapsenberg L., Dutton J.M. Exploring local adaptation and the ocean acidification seascape-studies in the California Current Large Marine Ecosystem. Biogeosciences 2014, 11:1053-1064.
48. Holcomb M., McCorkle D.C., Cohen A.L. Long-term effects of nutrient and CO2 enrichment on the temperate coral Astrangia poculata (Ellis and Solander, 1786). J. Exp. Mar. Biol. Ecol. 2010, 386:27-33.
49. Hönisch B., Ridgwell A., Schmidt D.N., Thomas E., Gibbs S.J., Sluijs A., Zeebe R., Kump L., Martindale R.C., Greene S.E., Kiessling W., Ries J., Zachos J.C., Royer D.L., Barker S., Marchitto T.M., Moyer R., Pelejero C., Ziveri P., Foster G.L., Williams B. The geological record of ocean acidification. Science 2012, 335:1058-1063.
50. Hwang S.-P.L., Lennarz W.J. Studies on the cellular pathway involved in assembly of the embryonic sea urchin spicule. Exp. Cell Res. 1993, 205:383-387.
51. 2 levels on energy metabolism and biomineralization of marine bivalves Crassostrea virginica and Mercenaria mercenaria. Comp. Biochem. Physiol. A 2013, 166:101-111.
52. Jacobs D.K., Haney T.A., Louie K.D. Genes, diversity and geologic processes on the Pacific Coast. Annu. Rev. Earth Planet. Sci. 2004, 32:601-652.
53. Jasny B.R., Purnell B.A. The glorious sea urchin. Science 2006, 314:938.
54. Johnstone J.A., Mantua N.J. Atmospheric controls on northeast Pacific temperature variability and change, 1900-2012. Proc. Natl. Acad. Sci. U. S. A. 2014, 111:14360-14365.
55. Katada S., Imhof A., Sassone-Corsi P. Connecting threads: epigenetics and metabolism. Cell 2012, 148:24-28.
56. Kelly M.W., Hofmann G.E. Adaptation and the physiology of ocean acidification. Funct. Ecol. 2013, 27:980-990.
57. Kelly M.W., Padilla-Gamiño J.L., Hofmann G.E. Natural variation and the capacity to adapt to ocean acidification in the keystone sea urchin Strongylocentrotus purpuratus. Glob. Chang. Biol. 2013, 19:2536-2546.
58. King J.R., Agostini V.N., Harvey C.J., McFarlane G.A., Foreman M.G.G., Overland J.E., Di Lorenzo E., Bond N.A., Aydin K.Y. Climate forcing and the California Current ecosystem. ICES J. Mar. Sci. 2011, 68:1199-1216.
59. Kirkpatrick M., Barton N.H. Evolution of a species' range. Am. Nat. 1997, 150:1-23.
60. Kouzarides T. Chromatin modifications and their function. Cell 2007, 128:693-705.
61. Kroeker K.J., Kordas R.L., Crim R.N., Singh G.G. Meta-analysis reveals negative yet variable effects of ocean acidification on marine organisms. Ecol. Lett. 2010, 13:1419-1434.
62. Kroeker K.J., Micheli F., Gambi M.C., Martz T.R. Divergent ecosystem responses within a benthic marine community to ocean acidification. Proc. Natl. Acad. Sci. U. S. A. 2011, 108:14515-14520.
63. 2 ocean. Proc. Natl. Acad. Sci. U. S. A. 2013, 110:12721-12726.
64. Kroeker K.J., Micheli F., Gambi M.C. Ocean acidification causes ecosystem shifts via altered competitive interactions. Nat. Clim. Chang. 2013, 3:156-159.
65. Kroeker K.J., Kordas R.L., Crim R., Hendriks I.E., Ramajo L., Singh G.S., Duarte C.M., Gattuso J.-P. Impacts of ocean acidification on marine organisms: quantifying sensitivities and interaction with warming. Glob. Chang. Biol. 2013, 19:1884-1896.
66. Lande R., Shannon S. The role of genetic variation in adaptation and population persistence in a changing environment. Evolution 1996, 50:434-437.
67. Langer G., Nehrke G., Probert I., Ly J., Ziveri P. Strain-specific responses of Emiliania huxleyi to changing seawater carbonate chemistry. Biogeosciences 2009, 6:2637-2646.
68. +-ATPase activity during sea urchin development. J. Exp. Biol. 1997, 200:2881-2892.
69. Lüthi D., Le Floch M., Bereiter B., Blunier T., Barnola J.-M., Siegenthaler U., Raynaud D., Jouzel J., Fischer H., Kawamura K., Stocker T.F. High-resolution carbon dioxide concentration record 650,000-800,000years before present. Nature 2008, 453:379-382.
70. Martz T.R., Connery J.G., Johnson K.S. Testing the Honeywell Durafet® for seawater pH applications. Limnol. Oceanogr. Methods 2010, 8:172-184.
71. Marzluff W.F., Duronio R.J. Histone mRNA expression: multiple levels of cell cycle regulation and important developmental consequences. Curr. Opin. Cell Biol. 2002, 14:692-699.
72. 2 tolerance in marine ectothermic animals: pre-adaptation through lifestyle and ontogeny?. Biogeosciences 2009, 6:2313-2331.
73. Michaelidis B., Ouzounis C., Paleras A., Portner H.O. Effects of long-term moderate hypercapnia on acid-base balance and growth rate in marine mussels Mytilus galloprovincialis. Mar. Ecol. Prog. Ser. 2005, 293:109-118.
74. Mitsunaga K., Makihara R., Fujino Y., Yasumasu I. Inhibitory effects of ethacrynic acid, furosemide, and nifedipine on the calcification of spicules in cultures of micromeres isolated from sea-urchin eggs. Differentiation 1986, 30:197-204.
75. Munday P.L. Transgenerational acclimation of fishes to climate change and ocean acidification. F1000Prime Rep. 2014, 6:99.
76. Nakamura M., Ohki S., Suzuki A., Sakai K. Coral larvae under ocean acidification: survival, metabolism, and metamorphosis. PLoS One 2011, 6:e14521.
77. National Research Council America's Climate Choices: Panel on Adapting to the Impacts of Climate Change 2010, The National Academies Press, Washington DC, (325pp.).
78. Nilsson G.E., Dixson D.L., Domenici P., McCormick M.I., Sorensen C., Watson S.-A., Munday P.L. Near-future carbon dioxide levels alter fish behaviour by interfering with neurotransmitter function. Nat. Clim. Chang. 2012, 2:201-204.
79. Orr J.C., Fabry V.J., Aumont O., Bopp L., Doney S.C., Feely R.A., Gnanadesikan A., Gruber N., Ishida A., Joos F., Key R.M., Lindsay K., Maier-Reimer E., Matear R., Monfray P., Mouchet A., Najjar R.G., Plattner G.-K., Rodgers K.B., Sabine C.L., Sarmiento J.L., Schlitzer R., Slater R.D., Totterdell I.J., Weirig M.-F., Yamanaka Y., Yool A. Anthropogenic ocean acidification over the twenty-first century and its impact on calcifying organisms. Nature 2005, 437:681-686.
80. 2 additively regulate physiology, morphology and genomic responses of larval sea urchins, Strongylocentrotus purpuratus. Proc. R. Soc. B 2013, 280:20130155.
81. Pansch C., Schaub I., Havenhand J., Wahl M. Habitat traits and food availability determine the response of marine invertebrates to ocean acidification. Glob. Chang. Biol. 2014, 20:765-777.
82. Parker L.M., Ross P.M., O'connor W.A., Borysko L., Raftos D.A., Pörtner H.O. Adult exposure influences offspring response to ocean acidification in oysters. Glob. Chang. Biol. 2012, 18:82-92.
83. Pelejero C., Calvo E., Hoegh-Guldberg O. Paleo-perspectives on ocean acidification. Trends Ecol. Evol. 2010, 25:332-344.
84. Pespeni M.H., Barney B.T., Palumbi S.R. Differences in the regulation of growth and biomineralization genes revealed through long-term common-garden acclimation and experimental genomics in the purple sea urchin. Evolution 2013, 67:1901-1914.
85. Pespeni M.H., Chan F., Menge B.A., Palumbi S.R. Signs of adaptation to local pH conditions across an environmental mosaic in the California Current Ecosystem. Integr. Comp. Biol. 2013, 53:857-870.
86. Pespeni M.H., Sanford E., Gaylord B., Hill T.M., Hosfelt J.D., Jaris H.K., LaVigne M., Lenz E.A., Russell A.D., Young M.K., Palumbi S.R. Evolutionary change during experimental ocean acidification. Proc. Natl. Acad. Sci. U. S. A. 2013, 110:6937-6942.
87. Pistevos J.C.A., Calosi P., Widdicombe S., Bishop J.D.D. Will variation among genetic individuals influence species responses to global climate change?. Oikos 2011, 120:675-689.
88. Pörtner H.O. Ecosystem effects of ocean acidification in times of ocean warming: a physiologist's view. Mar. Ecol. Prog. Ser. 2008, 373:203-217.
89. Raven J., Caldeira K., Elderfield H., Hoegh-Guldberg O., Liss P., Riebesell U., Shepherd J., Turley C., Watson A. Ocean acidification due to increasing atmospheric carbon dioxide 2005, The Royal Society.
90. Reipschläger A., Pörtner H.O. Metabolic depression during environmental stress: the role of extracellular versus intracellular pH in Sipunculus nudus. J. Exp. Biol. 1996, 199:1801-1807.
91. Ridgwell A., Schmidt D.N. Past constraints on the vulnerability of marine calcifiers to massive carbon dioxide release. Nat. Geosci. 2010, 3:196-200.
92. Ries J.B., Cohen A.L., McCorkle D.C. Marine calcifiers exhibit mixed responses to CO2-induced ocean acidification. Geology 2009, 37:1131-1134.
93. Roberts A., Pimentel H., Trapnell C., Pachter L. Identification of novel transcripts in annotated genomes using RNA-Seq. Bioinformatics 2011, 27:2325-2329.
94. 2. Science 2004, 305:367-371.
95. Schalkhausser B., Bock C., Stemmer K., Brey T., Pörtner H.-O., Lannig G. Impact of ocean acidification on escape performance of the king scallop, Pecten maximus, from Norway. Mar. Biol. 2012, 160:1995-2006.
96. Sodergren E., Weinstock G.M., Davidson E.H., Cameron R.A., Gibbs R.A., Angerer R.C., Angerer L.M., Arnone M.I., Burgess D.R., Burke R.D., Coffman J.A., Dean M., Elphick M.R., Ettensohn C.A., Foltz K.R., Hamdoun A., Hynes R.O., Klein W.H., Marzluff W., McClay D.R., Morris R.L., Mushegian A., Rast J.P., Smith L.C., Thorndyke M.C., Vacquier V.D., Wessel G.M., Wray G., Zhang L., Elsik C.G., Ermolaeva O., Hlavina W., Hofmann G., Kitts P., Landrum M.J., Mackey A.J., Maglott D., Panopoulou G., Poustka A.J., Pruitt K., Sapojnikov V., Song X., Souvorov A., Solovyev V., Wei Z., Whittaker C.A., Worley K., Durbin K.J., Shen Y., Fedrigo O., Garfield D., Haygood R., Primus A., Satija R., Severson T., Gonzalez-Garay M.L., Jackson A.R., Milosavljevic A., Tong M., Killian C.E., Livingston B.T., Wilt F.H., Adams N., Bellé R., Carbonneau S., Cheung R., Cormier P., Cosson B., Croce J., Fernandez-Guerra A., Genevière A.-M., Goel M., Kelkar H., Morales J., Mulner-Lorillon O., Robertson A.J., Goldstone J.V., Cole B., Epel D., Gold B., Hahn M.E., Howard-Ashby M., Scally M., Stegeman J.J., Allgood E.L., Cool J., Judkins K.M., McCafferty S.S., Musante A.M., Obar R.A., Rawson A.P., Rossetti B.J., Gibbons I.R., Hoffman M.P., Leone A., Istrail S., Materna S.C., Samanta M.P., Stolc V., Tongprasit W., Tu Q., Bergeron K.-F., Brandhorst B.P., Whittle J., Berney K., Bottjer D.J., Calestani C., Peterson K., Chow E., Yuan Q.A., Elhaik E., Graur D., Reese J.T., Bosdet I., Heesun S., Marra M.A., Schein J., Anderson M.K., Brockton V., Buckley K.M., Cohen A.H., Fugmann S.D., Hibino T., Loza-Coll M., Majeske A.J., Messier C., Nair S.V., Pancer Z., Terwilliger D.P., Agca C., Arboleda E., Chen N., Churcher A.M., Hallböök F., Humphrey G.W., Idris M.M., Kiyama T., Liang S., Mellott D., Mu X., Murray G., Olinski R.P., Raible F., Rowe M., Taylor J.S., Tessmar-Raible K., Wang D., Wilson K.H., Yaguchi S., Gaasterland T., Galindo B.E., Gunaratne H.J., Juliano C., Kinukawa M., Moy G.W., Neill A.T., Nomura M., Raisch M., Reade A., Roux M.M., Song J.L., Su Y.-H., Townley I.K., Voronina E., Wong J.L., Amore G., Branno M., Brown E.R., Cavalieri V., Duboc V., Duloquin L., Flytzanis C., Gache C., Lapraz F., Lepage T., Locascio A., Martinez P., Matassi G., Matranga V., Range R., Rizzo F., Röttinger E., Beane W., Bradham C., Byrum C., Glenn T., Hussain S., Manning G., Miranda E., Thomason R., Walton K., Wikramanayke A., Wu S.-Y., Xu R., Brown C.T., Chen L., Gray R.F., Lee P.Y., Nam J., Oliveri P., Smith J., Muzny D., Bell S., Chacko J., Cree A., Curry S., Davis C., Dinh H., Dugan-Rocha S., Fowler J., Gill R., Hamilton C., Hernandez J., Hines S., Hume J., Jackson L., Jolivet A., Kovar C., Lee S., Lewis L., Miner G., Morgan M., Nazareth L.V., Okwuonu G., Parker D., Pu L.-L., Thorn R., Wright R. The genome of the sea urchin Strongylocentrotus purpuratus. Science 2006, 314:941-952. Sea Urchin Genome Sequencing Consortium.
97. Shinzato C., Shoguchi E., Kawashima T., Hamada M., Hisata K., Tanaka M., Fujie M., Fujiwara M., Koyanagi R., Ikuta T., Fujiyama A., Miller D.J., Satoh N. Using the Acropora digitifera genome to understand coral responses to environmental change. Nature 2011, 476:320-323.
98. Stillman J.H. Acclimation capacity underlies susceptibility to climate change. Science 2003, 301:65.
99. Stockwell C.A., Hendry A.P., Kinnison M.T. Contemporary evolution meets conservation biology. Trends Ecol. Evol. 2003, 18:94-101.
100. Strange K. Revisiting the Krogh Principle in the post-genome era: Caenorhabditis elegans as a model system for integrative physiology research. J. Exp. Biol. 2007, 210:1622-1631.
101. Stumpp M., Hu M.Y., Melzner F., Gutowska M.A., Dorey N., Himmerkus N., Holtmann W.C., Dupont S.T., Thorndyke M.C., Bleich M. Acidified seawater impacts sea urchin larvae pH regulatory systems relevant for calcification. Proc. Natl. Acad. Sci. U. S. A. 2012, 109:18192-18197.
102. Su C., Gao G., Schneider S., Helt C., Weiss C., O'Reilly M.A., Bohmann D., Zhao J. DNA damage induces downregulation of histone gene expression through the G1 checkpoint pathway. EMBO J. 2004, 23:1133-1143.
103. Sunday J.M., Calosi P., Dupont S., Munday P.L., Stillman J.H., Reusch T.B.H. Evolution in an acidifying ocean. Trends Ecol. Evol. 2014, 29:117-125.
104. Tegner M.J. The ecology of Strogylocentrotus franciscanus and Strogylocentrotus purpuratus. Edible Sea Urchins: Biology and Ecology 2001, 307-331. Elsevier, New York. J.M. Lawrence (Ed.).
105. Thomsen J., Gutowska M.A., Saphörster J., Heinemann A., Trübenbach K., Fietzke J., Hiebenthal C., Eisenhauer A., Körtzinger A., Wahl M., Melzner F. Calcifying invertebrates succeed in a naturally CO2-rich coastal habitat but are threatened by high levels of future acidification. Biogeosciences 2010, 7:3879-3891.
106. Thomsen J., Casties I., Pansch C., Körtzinger A., Melzner F. Food availability outweighs ocean acidification effects in juvenile Mytilus edulis: laboratory and field experiments. Glob. Chang. Biol. 2013, 19:1017-1027.
107. 2-driven seawater acidification. J. Exp. Biol. 2009, 212:2579-2594.
108. Tomanek L. The importance of physiological limits in determining biogeographical range shifts due to global climate change: the heat-shock response. Physiol. Biochem. Zool. 2008, 81:709-717.
109. Vermeij G.J. Geographical restriction as a guide to the causes of extinction: the case of the cold northern oceans during the Neogene. Paleobiology 1989, 15:335-356.
110. 2-driven pH decrease in corals: new insights from transcriptome analysis. PLoS One 2013, 8:e58652.
111. Wang Z., Gerstein M., Snyder M. RNA-Seq: a revolutionary tool for transcriptomics. Nat. Rev. Genet. 2009, 10:57-63.
112. Wernberg T., Smale D.A., Thomsen M.S. A decade of climate change experiments on marine organisms: procedures, patterns and problems. Glob. Chang. Biol. 2012, 18:1491-1498.
113. Whitehead A. Comparative genomics in ecological physiology: toward a more nuanced understanding of acclimation and adaptation. J. Exp. Biol. 2012, 215:884-891.
114. Whitehead A., Crawford D.L. Variation within and among species in gene expression: raw material for evolution. Mol. Ecol. 2006, 15:1197-1211.
115. Whitehead A., Pilcher W., Champlin D., Nacci D. Common mechanism underlies repeated evolution of extreme pollution tolerance. Proc. Biol. Sci. 2012, 279:427-433.
116. Wilt F.H. Biomineralization of the spicules of sea urchin embryos. Zool. Sci. 2002, 19:253-261.
117. Wood H.L., Spicer J.I., Widdicombe S. Ocean acidification may increase calcification rates, but at a cost. Proc. R. Soc. B 2008, 275:1767-1773.
118. Wootton J.T., Pfister C.A. Carbon system measurements and potential climatic drivers at a site of rapidly declining ocean pH. PLoS One 2012, 7:e53396.
119. 2/pH. J. Exp. Mar. Biol. Ecol. 2011, 400:288-295.
120. Zhang G., Fang X., Guo X., Li L., Luo R., Xu F., Yang P., Zhang L., Wang X., Qi H., Xiong Z., Que H., Xie Y., Holland P.W.H., Paps J., Zhu Y., Wu F., Chen Y., Wang J., Peng C., Meng J., Yang L., Liu J., Wen B., Zhang N., Huang Z., Zhu Q., Feng Y., Mount A., Hedgecock D., Xu Z., Liu Y., Domazet-Loso T., Du Y., Sun X., Zhang S., Liu B., Cheng P., Jiang X., Li J., Fan D., Wang W., Fu W., Wang T., Wang B., Zhang J., Peng Z., Li Y., Li N., Wang J., Chen M., He Y., Tan F., Song X., Zheng Q., Huang R., Yang H., Du X., Chen L., Yang M., Gaffney P.M., Wang S., Luo L., She Z., Ming Y., Huang W., Zhang S., Huang B., Zhang Y., Qu T., Ni P., Miao G., Wang J., Wang Q., Steinberg C.E.W., Wang H., Li N., Qian L., Zhang G., Li Y., Yang H., Liu X., Wang J., Yin Y., Wang J. The oyster genome reveals stress adaptation and complexity of shell formation. Nature 2012, 490:49-54.