Combined effects of simulated acidification and hypoxia on the harmful dinoflagellate Amphidinium carterae
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.
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.
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.
Compliance with ethical standards
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.
- 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 CrossRefPubMedPubMedCentralGoogle Scholar
- 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 CrossRefGoogle Scholar
- 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 CrossRefPubMedPubMedCentralGoogle Scholar
- 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 CrossRefPubMedPubMedCentralGoogle Scholar
- 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 CrossRefPubMedPubMedCentralGoogle Scholar
- 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 CrossRefPubMedPubMedCentralGoogle Scholar
- 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 1029–1136Google Scholar
- 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 CrossRefGoogle Scholar
- 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 CrossRefGoogle Scholar
- 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 CrossRefGoogle Scholar
- 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 CrossRefGoogle Scholar
- 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 CrossRefGoogle Scholar
- 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 CrossRefPubMedPubMedCentralGoogle Scholar
- 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 1–17Google Scholar
- 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 CrossRefGoogle Scholar
- Steidinger KA, Jangen K (1996) Dinoflagellates. In: Tomas CR (ed) Identifying marine phytoplankton. Academic Press, New York, pp 387–589Google Scholar
- 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 CrossRefPubMedPubMedCentralGoogle Scholar