Combined effects of simulated acidification and hypoxia on the harmful dinoflagellate Amphidinium carterae

Abstract

Hypoxia and acidification frequently co-occur in coastal marine ecosystems, and will likely become more intense and persistent with anthropogenic climate change. Although the separate effects of these stressors have previously been described, their combined effects on marine phytoplankton are currently unknown. In this novel study, multi-stressor incubation experiments using the harmful dinoflagellate, Amphidinium carterae, examined the effects of acidification and hypoxia both individually and in combination. Long-term (7 days) and short-term (6 h) experiments under controlled carbon dioxide (CO2) and oxygen (O2) conditions examined the interactive effects of the stressors and the physiological mechanisms driving their interaction. In the long-term experiment, synergistically negative effects were observed for A. carterae growth, photosynthesis, carbon fixation, nitrate uptake, and photosynthetic efficiency (Fv/Fm) under combined high CO2 (low pH) and low O2 conditions. In the short-term experiment, delayed recovery of photosystem II (PSII) reaction centers was observed following photoinhibition, suggesting that high CO2 and low O2 conditions negatively affect photosynthesis in A. carterae even after relatively short exposures. Although high CO2, low O2 conditions should decrease photorespiration and favor carbon fixation by the key photosynthetic enzyme ribulose-1,5-bisphosphate-carboxylase/oxygenase (RuBisCO), these findings demonstrate that the affinity of RuBisCO for CO2 relative to O2 alone does not predict phytoplankton responses to CO2 and O2 conditions in vivo, complicating predictions of phytoplankton community responses to hypoxia and acidification. Results of these experiments suggest that the combination of low pH and O2 concentrations may negatively impact the growth of some harmful dinoflagellates in coastal marine ecosystems.

This is a preview of subscription content, access via your institution.

Fig. 1
Fig. 2
Fig. 3
Fig. 4
Fig. 5
Fig. 6

References

  1. Azcón-Bieto J, Gonzàlez-Meler MA, Doherty W, Drake BG (1994) Acclimation of respiratory O2 uptake in green tissues of field-grown native species after long-term exposure to elevated atmospheric CO2. Plant Physiol 106(3):1163–1168. https://doi.org/10.1104/pp.106.3.1163

    Article  PubMed  PubMed Central  Google Scholar 

  2. Badger MR, Andrews TJ, Whitney SM, Ludwig M et al (1998) The diversity and coevolution of RuBisCO, plastids, pyrenoids, and chloroplast-based CO2-concentrating mechanisms in algae. Can J Bot 76(6):1052–1071. https://doi.org/10.1139/cjb-76-6-1052

    CAS  Article  Google Scholar 

  3. Bagby SC, Chisholm SW (2015) Response of Prochlorococcus to varying CO2:O2 ratios. Int Soc Microb Ecol 9(10):2232–2245. https://doi.org/10.1038/ismej.2015.36

    CAS  Article  Google Scholar 

  4. Baumann H (2016) Combined effects of ocean acidification, warming, and hypoxia on marine organisms. Limnol Oceanogr e-Lect 6(1):1–43. https://doi.org/10.1002/loe2.10002

    Article  Google Scholar 

  5. Bausch AR, Boatta F, Morton PL, McKee KT et al (2017) Elevated toxic effect of sediments on growth of the harmful dinoflagellate Cochlodinium polykrikoides under high CO2. Aquat Microb Ecol 80(2):139–152. https://doi.org/10.3354/ame01848

    Article  Google Scholar 

  6. Bauwe H, Hagemann M, Fernie AR (2010) Photorespiration: players, partners and origin. Trends Plant Sci 15(6):330–336. https://doi.org/10.1016/j.tplants.2010.03.006

    CAS  Article  Google Scholar 

  7. Bauwe H, Hagemann M, Kern R, Timm S (2012) Photorespiration has a dual origin and manifold links to central metabolism. Curr Opin Plant Biol 15(3):269–275. https://doi.org/10.1016/j.pbi.2012.01.008

    CAS  Article  Google Scholar 

  8. Behrenfeld MJ, Halsey KH, Milligan AJ (2008) Evolved physiological responses of phytoplankton to their integrated growth environment. Phil Trans R Soc B 363:2687–2703. https://doi.org/10.1098/rstb.2008.0019

    CAS  Article  Google Scholar 

  9. Birmingham BC, Coleman JR, Colman B (1982) Measurement of photorespiration in algae. Plant Physiol 69(1):259–262. https://doi.org/10.1104/pp.69.1.259

    CAS  Article  PubMed  PubMed Central  Google Scholar 

  10. Bowes G, Ogren WL, Hageman RH (1971) Phosphoglycolate production catalyzed by ribulose diphosphate carboxylase. Biochem Biophys Res Commun 45(3):716–722. https://doi.org/10.1016/0006-291X(71)90475-X

    CAS  Article  Google Scholar 

  11. Breitburg DL, Salisbury J, Bernhard JM, Cai W-J et al (2015) And on top of all that… Coping with ocean acidification in the midst of many stressors. Oceanogr 28(2):48–61. https://doi.org/10.5670/oceanog.2015.31

    Article  Google Scholar 

  12. Brooks MD, Niyogi KK (2011) Use of a pulse-amplitude modulated chlorophyll fluorometer to study the efficiency of photosynthesis in Arabidopsis plants. In: Jarvis RP (ed) Chloroplast research in Arabidopsis: methods and protocols. Springer, New York, pp 299–310

    Google Scholar 

  13. Bunt JS (1971) Levels of dissolved oxygen and carbon fixation by marine microalgae. Limnol Oceanogr 16(3):564–566. https://doi.org/10.4319/lo.1971.16.3.0564

    Article  Google Scholar 

  14. Burns BD, Beardall J (1987) Utilization of inorganic carbon by marine microalgae. J Exp Mar Biol Ecol 107(1):75–86. https://doi.org/10.1016/0022-0981(87)90125-0

    CAS  Article  Google Scholar 

  15. Cai W-J, Hu X, Huang W-J, Murrell MC et al (2011) Acidification of subsurface coastal waters enhanced by eutrophication. Nat Geosci 4(11):766–770. https://doi.org/10.1038/ngeo1297

    CAS  Article  Google Scholar 

  16. Caldeira K, Wickett ME (2003) Anthropogenic carbon and ocean pH. Nature 425(6956):365. https://doi.org/10.1038/425365a

    CAS  Article  Google Scholar 

  17. Caldeira K, Wickett ME (2005) Ocean model predictions of chemistry changes from carbon dioxide emissions to the atmosphere and ocean. J Geophys Res 110:1–12. https://doi.org/10.1029/2004JC002671

    CAS  Article  Google Scholar 

  18. Cao C, Sun S, Wang X, Liu W, Liang Y (2011) Effects of manganese on the growth, photosystem II and SOD activity of the dinoflagellate Amphidinium sp. J Appl Phycol 23(6):1039–1043. https://doi.org/10.1007/s10811-010-9637-0

    CAS  Article  Google Scholar 

  19. Cardol P, Forti G, Finazzi G (2011) Regulation of electron transport in microalgae. Biochim Biophys Acta 1807:912–918. https://doi.org/10.1016/j.bbabio.2010.12.004

    CAS  Article  Google Scholar 

  20. Cornwall CE, Hurd CL (2016) Experimental design in ocean acidification research: problems and solutions. ICES J Mar Sci 73(3):572–581. https://doi.org/10.1093/icesjms/fsv118

    Article  Google Scholar 

  21. Crafts-Brandner SJ, Salvucci ME (2000) RuBisCO activase constrains the photosynthetic potential of leaves at high temperature and CO2. Proc Natl Acad Sci 97(24):13430–13435. https://doi.org/10.1073/pnas.230451497

    CAS  Article  Google Scholar 

  22. Crawley A, Kline DI, Dunn S, Anthony K, Dove S (2010) The effect of ocean acidification on symbiont photorespiration and productivity in Acropora formosa. Glob Change Biol 16(2):851–863. https://doi.org/10.1111/j.1365-2486.2009.01943.x

    Article  Google Scholar 

  23. Dason JS, Huertas IE, Colman B (2004) Source of inorganic carbon for photosynthesis in two marine dinoflagellates. J Phycol 40(2):285–292. https://doi.org/10.1111/j.1529-8817.2004.03123.x

    CAS  Article  Google Scholar 

  24. DePasquale E, Baumann H, Gobler CJ (2015) Vulnerability of early life stage Northwest Atlantic forage fish to ocean acidification and low oxygen. Mar Ecol Prog Ser 523:145–156. https://doi.org/10.3354/meps11142

    CAS  Article  Google Scholar 

  25. Devos N, Ingouff M, Loppes R, Matagne RF (1998) RuBisCO adaptation to low temperatures: a comparative study in psychrophilic and mesophilic unicellular algae. J Phycol 34(4):655–660. https://doi.org/10.1046/j.1529-8817.1998.340655.x

    CAS  Article  Google Scholar 

  26. Diaz RJ, Rosenberg R (2008) Spreading dead zones and consequences for marine ecosystems. Science 321(5891):926–929. https://doi.org/10.1126/science.1156401

    CAS  Article  Google Scholar 

  27. Dickson AG, Millero FJ (1987) A comparison of the equilibrium constants for the dissociation of carbonic acid in seawater media. Deep-Sea Res Part A Oceanogr Res Pap 34(10):1733–1743. https://doi.org/10.1016/0198-0149(87)90021-5

    CAS  Article  Google Scholar 

  28. Dickson AG, Sabine CL, Christian JR (2007) Guide to best practices for ocean CO2 measurements. PICES Spec Publ 3(8):1–191. https://doi.org/10.1159/000331784

    Article  Google Scholar 

  29. Dixon GK, Syrett PJ (1988) The growth of dinoflagellates in laboratory cultures. New Phytol 109(3):297–302. https://doi.org/10.1111/j.1469-8137.1988.tb04198.x

    Article  Google Scholar 

  30. Doney SC, Fabry VJ, Feely RA, Kleypas JA (2009) Ocean acidification: the other CO2 problem. Ann Rev Mar Sci 1(1):169–192. https://doi.org/10.1146/annurev.marine.010908.163834

    Article  PubMed  PubMed Central  Google Scholar 

  31. Eberlein T, Van de Waal DB, Rost B (2014) Differential effects of ocean acidification on carbon acquisition in two bloom-forming dinoflagellate species. Physiol Plant 151(4):468–479. https://doi.org/10.1111/ppl.12137

    CAS  Article  PubMed  PubMed Central  Google Scholar 

  32. Echigoya R, Rhodes L, Oshima Y, Satake M (2005) The structures of five new antifungal and hemolytic amphidinol analogs from Amphidinium carterae collected in New Zealand. Harmful Algae 4(2):383–389. https://doi.org/10.1016/j.hal.2004.07.004

    CAS  Article  Google Scholar 

  33. Finazzi G, Furia A, Barbagallo RP, Forti G (1999) State transitions, cyclic and linear electron transport and photophosphorylation in Chlamydomonas reinhardtii. Biochim Biophys Acta 1413:117–129. https://doi.org/10.1016/S0005-2728(99)00089-4

    CAS  Article  PubMed  PubMed Central  Google Scholar 

  34. Finazzi G, Moreau H, Bowler C (2010) Genomic insights into photosynthesis in eukaryotic phytoplankton. Trends Plant Sci 15(10):565–572. https://doi.org/10.1016/j.tplants.2010.07.004

    CAS  Article  PubMed  PubMed Central  Google Scholar 

  35. Foyer CH, Noctor G (2000) Tansley review No. 112. Oxygen processing in photosynthesis: regulation and signaling. New Phytol 146(3):359–388. https://doi.org/10.1046/j.1469-8137.2000.00667.x

    CAS  Article  Google Scholar 

  36. Fu FX, Zhang Y, Warner ME, Feng Y, Sun J, Hutchins DA (2008) A comparison of future increased CO2 and temperature effects on sympatric Heterosigma akashiwo and Prorocentrum minimum. Harmful Algae 7(1):76–90. https://doi.org/10.1016/j.hal.2007.05.006

    CAS  Article  Google Scholar 

  37. Fu FX, Tatters AO, Hutchins DA (2012) Global change and the future of harmful algal blooms in the ocean. Mar Ecol Prog Ser 470:207–233. https://doi.org/10.3354/meps10047

    CAS  Article  Google Scholar 

  38. Gobler CJ, Baumann H (2016) Hypoxia and acidification in ocean ecosystems: coupled dynamics and effects of marine life. Biol Lett 12(5):20150976. https://doi.org/10.1098/rsbl.2015.0976

    CAS  Article  PubMed  PubMed Central  Google Scholar 

  39. Gobler CJ, DePasquale EL, Griffith AW, Baumann H (2014) Hypoxia and acidification have additive and synergistic negative effects on the growth, survival, and metamorphosis of early life stage bivalves. PLoS One 9(1):1–10. https://doi.org/10.1371/journal.pone.0083648

    CAS  Article  Google Scholar 

  40. Godaux D, Bailleul B, Berne N, Cardol P (2015) Induction of photosynthetic carbon fixation in anoxia relies on hydrogenase activity and proton-gradient regulation-like-mediated cyclic electron flow in Chlamydomonas reinhardtii. Plant Physiol 168(2):648–658. https://doi.org/10.1104/pp.15.00105

    CAS  Article  PubMed  PubMed Central  Google Scholar 

  41. Goldman JAL, Bender ML, Morel FMM (2017) The effects of pH and pCO2 on photosynthesis and respiration in the diatom Thalassiosira weissflogii. Photosynth Res 132(1):83–93. https://doi.org/10.1007/s11120-016-0330-2

    CAS  Article  PubMed  PubMed Central  Google Scholar 

  42. Gonzàlez-Meler MA, Ribas-Carbó M, Siedow JN, Drake BG (1996) Direct inhibition of plant mitochondrial respiration by elevated CO2. Plant Physiol 112(3):1349–1355. https://doi.org/10.1104/pp.112.3.1349

    Article  PubMed  PubMed Central  Google Scholar 

  43. Gruber N (2011) Warming up, turning sour, losing breath: ocean biogeochemistry under global change. Phil Trans R Soc 369:1980–1996. https://doi.org/10.1098/rsta.2011.0003

    CAS  Article  Google Scholar 

  44. Gruber RK, Lowe RJ, Falter JL (2017) Metabolism of a tide-dominated reef platform subject to extreme diel temperature and oxygen variations. Limnol Oceanogr 62(4):1701–1717. https://doi.org/10.1002/lno.10527

    CAS  Article  Google Scholar 

  45. Guillard RRL, Hargraves PE (1993) Stichochrysis immobilis is a diatom, not a chrysophyte. Phycologia 32(3):234–236. https://doi.org/10.2216/i0031-8884-32-3-234.1

    Article  Google Scholar 

  46. Guinotte JM, Fabry VJ (2008) Ocean acidification and its potential effects on marine ecosystems. Ann N Y Acad Sci 1134(1):320–342. https://doi.org/10.1196/annals.1439.013

    CAS  Article  PubMed  PubMed Central  Google Scholar 

  47. Hackenberg C, Engelhardt A, Matthijs HCP, Wittink F et al (2009) Photorespiratory 2-phosphoglycolate metabolism and photoreduction of O2 cooperate in high-light acclimation of Synechocystis sp. strain PCC 6803. Planta 230(4):625–637. https://doi.org/10.1007/s00425-009-0972-9

    CAS  Article  PubMed  PubMed Central  Google Scholar 

  48. Hargraves PE, Maranda L (2002) Potentially toxic or harmful microalgae from the northeast coast. Northeast Nat 9(1):81–120. https://doi.org/10.2307/3858576

    Article  Google Scholar 

  49. Hattenrath-Lehmann TK, Smith JL, Wallace RB, Merlo LR et al (2015) The effects of elevated CO2 on the growth and toxicity of field populations and cultures of the saxitoxin-producing dinoflagellate Alexandrium fundyense. Limnol Oceanogr 60(1):198–214. https://doi.org/10.1002/lno.10012

    CAS  Article  PubMed  PubMed Central  Google Scholar 

  50. Hennon GMM, Hernández Limón MD, Haley ST, Juhl AR, Dyhrman ST (2017) Diverse CO2-induced responses in physiology and gene expression among eukaryotic phytoplankton. Front Microbiol 8:1–14. https://doi.org/10.3389/fmicb.2017.02547

    Article  Google Scholar 

  51. Huang S-J, Kuo C-M, Lin Y-C, Chen Y-M, Lu C-K (2009) Carteraeol E, a potent polyhydroxyl ichthyotoxin from the dinoflagellate Amphidinium carterae. Tetrahedron Lett 50(21):2512–2515. https://doi.org/10.1016/j.tetlet.2009.03.065

    CAS  Article  Google Scholar 

  52. Hulburt EM (1957) The taxonomy of unarmored Dinophyceae of shallow embayments on Cape Cod, Massachusetts. Biol Bull 112(2):196–219. https://doi.org/10.2307/1539198

    Article  Google Scholar 

  53. IPCC (2013) Long-term climate change: projections, commitments and irreversibility. In: Stocker TF, Qin D, Plattner GK, Tignor M et al (eds) Climate change 2013: the physical science basis. Contribution of Working Group I to the Fifth Assessment Report of the Intergovernmental Panel on Climate Change. Cambridge University Press, Cambridge, pp 1029–1136

    Google Scholar 

  54. Jampeetong A, Brix H (2009) Oxygen stress in Salvinia natans: interactive effects of oxygen availability and nitrogen source. Envir Exp Bot 66(2):153–159. https://doi.org/10.1016/j.envexpbot.2009.01.006

    CAS  Article  Google Scholar 

  55. Jenks A, Gibbs SP (2000) Immunolocalization and distribution of Form II RuBisCO in the pyrenoid and chloroplast stroma of Amphidinium carterae and Form I RuBisCO in the symbiont-derived plastics of Peridinium foliaceum (Dinophyceae). J Phycol 36(1):127–138. https://doi.org/10.1046/j.1529-8817.2000.99114.x

    CAS  Article  Google Scholar 

  56. Jones RJ, Hoegh-Guldberg O (2001) Diurnal changes in the photochemical efficiency of the symbiotic dinoflagellates (Dinophyceae) of corals: photoprotection, photoinactivation and the relationship to coral bleaching. Plant Cell Environ 24:89–99. https://doi.org/10.1046/j.1365-3040.2001.00648.x

    CAS  Article  Google Scholar 

  57. Juhl AR, Latz MI (2002) Mechanisms of fluid shear-induced inhibition of population growth in a red-tide dinoflagellate. J Phycol 38(4):683–694. https://doi.org/10.1046/j.1529-8817.2002.00165.x

    Article  Google Scholar 

  58. Keeling RF, Körtzinger A, Gruber N (2010) Ocean deoxygenation in a warming world. Annu Rev Mar Sci 2(1):199–229. https://doi.org/10.1146/annurev.marine.010908.163855

    Article  Google Scholar 

  59. Kitaya Y, Xiao L, Masuda A, Ozawa T, Tsuda M, Omasa K (2008) Effects of temperature, photosynthetic photon flux density, photoperiod and O2 and CO2 concentrations on growth rates of the symbiotic dinoflagellate, Amphidinium sp. J Appl Phycol 20(5):737–742. https://doi.org/10.1007/s10811-008-9331-7

    CAS  Article  Google Scholar 

  60. Kroeker KJ, Kordas RL, Crim R, Hendriks IE et al (2013) Impacts of ocean acidification on marine organisms: quantifying sensitivities and interaction with warming. Glob Change Biol 19(6):1884–1896. https://doi.org/10.1111/gcb.12179

    Article  Google Scholar 

  61. Laws EA, Bidigare RR, Popp BN (1997) Effect of growth rate and CO2 concentration on carbon isotopic fractionation by the marine diatom Phaeodactylum tricornutum. Limnol Oceanogr 42(7):1552–1560. https://doi.org/10.4319/lo.1997.42.7.1552

    CAS  Article  Google Scholar 

  62. Leggat W, Badger MR, Yellowlees D (1999) Evidence for an inorganic carbon-concentrating mechanism in the symbiotic dinoflagellate Symbiodinium sp. Plant Physiol 121:1247–1255. https://doi.org/10.1104/pp.121.4.1247

    CAS  Article  PubMed  PubMed Central  Google Scholar 

  63. Li G, Campbell DA (2017) Interactive effects of nitrogen and light on growth rates and RuBisCO content of small and large centric diatoms. Photosynth Res 131(1):93–103. https://doi.org/10.1007/s11120-016-0301-7

    CAS  Article  PubMed  PubMed Central  Google Scholar 

  64. Liu N, Beardall J, Gao K (2017) Elevated CO2 and associated seawater chemistry do not benefit a model diatom grown with increased availability of light. Aquat Microb Ecol 79(2):137–147. https://doi.org/10.3354/ame01820

    Article  Google Scholar 

  65. Loganathan N, Tsai Y-CC, Mueller-Cajar O (2016) Characterization of the heterooligomeric red-type RuBisCO activase from red algae. Proc Natl Acad Sci 113(49):14019–14024. https://doi.org/10.1073/pnas.1610758113

    CAS  Article  PubMed  PubMed Central  Google Scholar 

  66. Losh JL, Young JN, Morel FMM (2013) RuBisCO is a small fraction of total protein in marine phytoplankton. New Phytol 198(1):52–58. https://doi.org/10.1111/nph.12143

    CAS  Article  PubMed  PubMed Central  Google Scholar 

  67. Mehrbach C, Culberson CH, Hawley JE, Pytkowicx RM (1973) Measurement of the apparent dissociation constants of carbonic acid in seawater at atmospheric pressure. Limnol Oceanogr 18(6):897–907. https://doi.org/10.4319/lo.1973.18.6.0897

    CAS  Article  Google Scholar 

  68. Melzner F, Thomsen J, Koeve W, Oschlies A et al (2013) Future ocean acidification will be amplified by hypoxia in coastal habitats. Mar Biol 160(8):1875–1888. https://doi.org/10.1007/s00227-012-1954-1

    CAS  Article  Google Scholar 

  69. Murray SA, Garby T, Hoppenrath M, Neilan BA (2012) Genetic diversity, morphological uniformity and polyketide production in dinoflagellates (Amphidinium, Dinoflagellata). PLoS One 7(6):1–14. https://doi.org/10.1371/journal.pone.0038253

    CAS  Article  Google Scholar 

  70. Parry MAJ, Keys AJ, Madgwick PJ, Carmo-Silva AE, Andralojc PJ (2008) RuBisCO regulation: a role for inhibitors. J Exp Bot 59(7):1569–1580. https://doi.org/10.1093/jxb/ern084

    CAS  Article  Google Scholar 

  71. Peckol P, Rivers JS (1995) Physiological responses of the opportunistic macroalgae Cladophora vagabunda (L.) van den Hoek and Gracilaria tikvahiae (McLachlan) to environmental disturbances associated with eutrophication. J Exp Mar Biol Ecol 190(1):1–16. https://doi.org/10.1016/0022-0981(95)00026-n

    Article  Google Scholar 

  72. Peltier G, Thibault P (1983) Ammonia exchange and photorespiration in Chlamydomonas. Plant Physiol 71(4):888–892. https://doi.org/10.1104/pp.71.4.888

    CAS  Article  PubMed  PubMed Central  Google Scholar 

  73. Peñuelas J, Llusià J (2002) Linking photorespiration, monoterpenes and thermotolerance in Quercus. New Phytol 155(2):227–237. https://doi.org/10.1046/j.1469-8137.2002.00457.x

    Article  Google Scholar 

  74. Peterhansel C, Horst I, Niessen M, Blume C et al (2010) Photorespirations. Arabidopsis Book 8(e0130):1–24. https://doi.org/10.1199/tab.0130

    Article  Google Scholar 

  75. Pierangelini M, Raven JA, Giordano M (2017) The relative availability of inorganic carbon and inorganic nitrogen influences the response of the dinoflagellate Protoceratium reticulatum to elevated CO2. J Phycol 53:298–307. https://doi.org/10.1111/jpy.12463

    CAS  Article  Google Scholar 

  76. Pope DH (1975) Effects of light intensity, oxygen concentration, and carbon dioxide concentration on photosynthesis in algae. Microb Ecol 2(1):1–16. https://doi.org/10.1007/BF02010377

    CAS  Article  Google Scholar 

  77. Possmayer M, Berardi G, Beall BFN, Trick CG, Hüner NPA, Maxwell DP (2011) Plasticity of the psychrophilic green alga Chlamydomonas raudensis (UWO 241) (Chlorophyta) to supraoptimal temperature stress. J Phycol 47(5):1098–1109. https://doi.org/10.1111/j.1529-8817.2011.01047.x

    CAS  Article  PubMed  PubMed Central  Google Scholar 

  78. Rabalais NN, Díaz RJ, Levin LA, Turner RE, Gilbert D, Zhang J (2010) Dynamics and distribution of natural and human-caused hypoxia. Biogeosciences 7(2):585–619. https://doi.org/10.5194/bg-7-585-2010

    CAS  Article  Google Scholar 

  79. Ratti S, Giordano M, Morse D (2007) CO2-concentrating mechanisms of the potentially toxic dinoflagellate Protoceratium reticulatum (Dinophyceae, Gonyaulacales). J Phycol 43:693–701. https://doi.org/10.1111/j.1529-8817.2007.00368.x

    CAS  Article  Google Scholar 

  80. Raven JA (2013) RuBisCO: still the most abundant protein of Earth? New Phytol 198:1–3. https://doi.org/10.1111/nph.12197

    CAS  Article  Google Scholar 

  81. Raven JA, Cockell CS, De La Rocha CL (2008) The evolution of inorganic carbon concentrating mechanisms in photosynthesis. Phil Trans R Soc B 363:2641–2650. https://doi.org/10.1098/rstb.2008.0020

    CAS  Article  Google Scholar 

  82. Riebesell U, Fabry VJ, Hansson L, Gattuso J-P (2011) Guide to best practices for ocean acidification research and data reporting. European Commission, Luxembourg, pp 1–258. https://doi.org/10.2777/66906

    Book  Google Scholar 

  83. Robbins LL, Hansen ME, Kleypas JA, Meylan SC (2010) CO2calc: a user-friendly seawater carbon calculator for Windows, Max OS X, and iOS (iPhone). US Geol Surv, pp 1–17

  84. 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 204:81–91. https://doi.org/10.1111/nph.12903

    CAS  Article  Google Scholar 

  85. Schreiber U, Vidaver W (1974) Chlorophyll fluorescence induction in anaerobic Scenedesmus obliquus. Biochim Biophys Acta 368(1):97–112. https://doi.org/10.1016/0005-2728(74)90100-5

    CAS  Article  Google Scholar 

  86. Schreiber U, Neubauer C, Schliwa U (1993) PAM fluorometer based on medium-frequency pulsed Xe-flash measuring light: a highly sensitive new tool in basic and applied photosynthesis research. Photosynth Res 36(1):65–72. https://doi.org/10.1007/BF00018076

    CAS  Article  Google Scholar 

  87. Sobrino C, Ward ML, Neale PJ (2008) Acclimation to elevated carbon dioxide and ultraviolet radiation in the diatom Thalassiosira pseudonana: effects on growth, photosynthesis, and spectral sensitivity of photoinhibition. Limnol Oceanogr 53(2):494–505. https://doi.org/10.4319/lo.2008.53.2.0494

    CAS  Article  Google Scholar 

  88. Steidinger KA, Jangen K (1996) Dinoflagellates. In: Tomas CR (ed) Identifying marine phytoplankton. Academic Press, New York, pp 387–589

    Google Scholar 

  89. Strickland JDH, Parsons TR (1972) A practical handbook of seawater analysis, 2nd edn. Fisheries Research Board of Canada Bulletin, Ottawa, pp 1–310. https://doi.org/10.1002/iroh.19700550118

    Book  Google Scholar 

  90. Sunda WG, Cai W-J (2012) Eutrophication induced CO2-acidification of subsurface coastal waters: interactive effects of temperature, salinity, and atmospheric pCO2. Envir Sci Tech 46(19):10651–10659. https://doi.org/10.1021/es300626f

    CAS  Article  Google Scholar 

  91. Tabita FR, Hanson TE, Li H, Satagopan S, Singh J, Chan S (2007) Function, structure, and evolution of the RuBisCO-like proteins and their RuBisCO homologs. Microbiol Mol Biol R 71(4):576–599. https://doi.org/10.1128/MMBR.00015-07

    CAS  Article  Google Scholar 

  92. Takahashi S, Bauwe H, Badger M (2007) Impairment of the photorespiratory pathway accelerates photoinhibition of photosystem II by suppression of repair but not acceleration of damage processes in Arabidopsis. Plant Physiol 144(1):487–494. https://doi.org/10.1104/pp.107.097253

    CAS  Article  PubMed  PubMed Central  Google Scholar 

  93. Takeba G, Kozaki A (1998) Photorespiration is an essential mechanism for the protection of C3 plants from photooxidation. In: Satoh K, Murata N (eds) stress responses of photosynthetic organisms. Elsevier, Amsterdam, pp 15–36

    Google Scholar 

  94. Tcherkez G, Bligny R, Gout E, Mahé A, Hodges M, Cornic G (2008) Respiratory metabolism of illuminated leaves depends on CO2 and O2 conditions. Proc Natl Acad Sci 105(2):797–802. https://doi.org/10.1073/pnas.0708947105

    Article  Google Scholar 

  95. Tortell PD (2000) Evolutionary and ecological perspectives on carbon acquisition in phytoplankton. Limnol Oceanogr 45(3):744–750. https://doi.org/10.4319/lo.2000.45.3.0744

    CAS  Article  Google Scholar 

  96. Ulstrup KE, Hill R, Ralph PJ (2005) Photosynthetic impact of hypoxia on in hospite zooxanthellae in the scleractinian coral Pocillopora damicornis. Mar Ecol Prog Ser 286:125–132. https://doi.org/10.3354/meps286125

    Article  Google Scholar 

  97. Vaquer-Sunyer R, Duarte CM (2008) Thresholds of hypoxia for marine biodiversity. Proc Natl Acad Sci 105(40):15452–15457. https://doi.org/10.1073/pnas.0803833105

    Article  Google Scholar 

  98. Wallace RB, Baumann H, Grear JS, Aller RC, Gobler CJ (2014) Coastal ocean acidification: the other eutrophication problem. Estuar Coast Shelf Sci 148:1–13. https://doi.org/10.1016/j.ecss.2014.05.027

    CAS  Article  Google Scholar 

  99. Whitney SM, Andrews TJ (1998) The CO2/O2 specificity of single-subunit ribulose-bisphosphate carboxylase from the dinoflagellate, Amphidinium carterae. Aust J Plant Physiol 25:131–138. https://doi.org/10.1071/PP97167

    CAS  Article  Google Scholar 

  100. Wu Y, Gao K, Riebesell U (2010) CO2-induced seawater acidification affects physiological performance of the marine diatom Phaeodactylum tricornutum. Biogeosciences 7(9):2915–2923. https://doi.org/10.5194/bg-7-2915-2010

    CAS  Article  Google Scholar 

  101. Wu RSS, Wo KT, Chiu JMY (2012) Effects of hypoxia on growth of the diatom Skeletonema costatum. J Exp Mar Biol Ecol 420–421:65–68. https://doi.org/10.1016/j.jembe.2012.04.003

    CAS  Article  Google Scholar 

  102. Young JN, Goldman JAL, Kranz SA, Tortell PD, Morel FMM (2015a) Slow carboxylation of RuBisCO constrains the rate of carbon fixation during Antarctic phytoplankton blooms. New Phytol 205(1):172–181. https://doi.org/10.1111/nph.13021

    CAS  Article  Google Scholar 

  103. Young JN, Kranz SA, Goldman JAL, Tortell PD, Morel FMM (2015b) Antarctic phytoplankton down-regulate their carbon-concentrating mechanisms under high CO2 with no change in growth rates. Mar Ecol Prog Ser 532:13–28. https://doi.org/10.3354/meps11336

    CAS  Article  Google Scholar 

  104. Young JN, Heureux AMC, Sharwood RE, Rickaby REM, Morel FMM, Whitney SM (2016) Large variation in the RuBisCO kinetics of diatoms reveals diversity among their carbon-concentrating mechanisms. J Exp Bot 67(11):3445–3456. https://doi.org/10.1093/jxb/erw163

    CAS  Article  PubMed  PubMed Central  Google Scholar 

Download references

Acknowledgements

The authors would like to thank Sonya Dyhrman and Sheean Haley at Lamont-Doherty Earth Observatory (LDEO) for providing laboratory space and logistical support; Hugh Ducklow, Robert Anderson, Kevin Griffin, and Gwenn Hennon at LDEO, Christopher Hayes at the University of Southern Mississippi, and the Editor and Reviewer for providing feedback on the manuscript; Wei Huang at LDEO for performing the isotopic analyses; Jerry Frank at the Chesapeake Biological Laboratory for performing the nutrient analyses; Andrew Dickson at Scripps Institution of Oceanography for providing the CO2 seawater reference materials; and Naomi Shelton and Clara Chang at LDEO for providing laboratory assistance. This is contribution #8317 from Lamont–Doherty Earth Observatory.

Funding

This work was partly supported by NASA Headquarters under the NASA Earth and Space Science Fellowship Program grant 15-EARTH15R-5. Funding was also provided by the Natural Sciences and Engineering Research Council of Canada and the Chevron Student Initiative Fund from the Department of Earth and Environmental Sciences at Columbia University.

Author information

Affiliations

Authors

Corresponding author

Correspondence to Alexandra R. Bausch.

Ethics declarations

Conflict of interest

The authors Alexandra Bausch, Andrew Juhl, and Natalie Donaher declare no conflicts of interest. The author Amanda Cockshutt declares a potential financial interest as part owner of Environmental Proteomics NB Inc., an Agrisera business partner.

Human and animal rights statement

All authors have agreed to the submitted version of this manuscript. This manuscript does not contain any studies with humans or animals performed by any of the authors.

Additional information

Publisher's Note

Springer Nature remains neutral with regard to jurisdictional claims in published maps and institutional affiliations.

Reviewed by P. Cardol.

Responsible Editor: S. Shumway.

Electronic supplementary material

Below is the link to the electronic supplementary material.

Supplementary material 1 (PDF 208 kb)

Rights and permissions

Reprints and Permissions

About this article

Verify currency and authenticity via CrossMark

Cite this article

Bausch, A.R., Juhl, A.R., Donaher, N.A. et al. Combined effects of simulated acidification and hypoxia on the harmful dinoflagellate Amphidinium carterae. Mar Biol 166, 80 (2019). https://doi.org/10.1007/s00227-019-3528-y

Download citation