Single-species dinoflagellate cyst carbon isotope fractionation in core-top sediments: environmental controls, CO2 dependency and proxy potential

. Sedimentary bulk organic matter and various molecular organic components exhibit strong CO 2 -dependent carbon isotope fractionation relative to dissolved inorganic carbon sources. This fractionation ( e p ) has been employed as proxy for paleo- p CO 2 . Yet, culture experiments indicate this CO 2 -dependent e p is highly specific at genus and even species level, potentially hampering the use of bulk organic matter and non-species specific organic compounds. In recent years, significant progress has been made towards a CO 2 proxy using controlled growth experiments with dinoflagellate species, also showing 15 highly species-specific e p values. These values were, however, based on motile specimens and it remains unknown whether these relations also hold for the organic-walled resting cysts (dinocysts) produced by these dinoflagellate species in their natural environment. We here analyze dinocysts isolated from core-tops from the Atlantic Ocean and Mediterranean Sea, representing several species ( Spiniferites elongatus, S. (cf.) ramosus, S. mirabilis , Operculodinium centrocarpum sensu Wall & Dale (1966) (hereafter referred to as O. centrocarpum ) and Impagidinium aculeatum ) using Laser ablation – nano 20 Combustion – Gas Chromatography – Isotope Ratio Mass Spectrometry (LA/nC/GC-IRMS). We find that the dinocysts

[1]  G. Foster,et al.  Atmospheric CO2 over the Past 66 Million Years from Marine Archives , 2021 .

[2]  M. Badger Alkenone isotopes show evidence of active carbon concentrating mechanisms in coccolithophores as aqueous carbon dioxide concentrations fall below 7 µmolL-1 , 2020 .

[3]  A. Pearson,et al.  A general model for carbon isotopes in red-lineage phytoplankton: Interplay between unidirectional processes and fractionation by RubisCO , 2019, Geochimica et Cosmochimica Acta.

[4]  H. Dijkstra,et al.  Transport Bias by Ocean Currents in Sedimentary Microplankton Assemblages: Implications for Paleoceanographic Reconstructions , 2019, Paleoceanography and Paleoclimatology.

[5]  P. Ziveri,et al.  Upregulation of phytoplankton carbon concentrating mechanisms during low CO2 glacial periods and implications for the phytoplankton pCO2 proxy , 2019, Quaternary Science Reviews.

[6]  G. Kuhn,et al.  Postdepositional aerobic and anaerobic particulate organic matter degradation succession reflected by dinoflagellate cysts: The Madeira Abyssal Plain revisited , 2019, Marine Geology.

[7]  B. Blais,et al.  Molecular fossils from phytoplankton reveal secular Pco2 trend over the Phanerozoic , 2018, Science Advances.

[8]  A. Sluijs,et al.  Towards quantitative environmental reconstructions from ancient non-analogue microfossil assemblages: Ecological preferences of Paleocene – Eocene dinoflagellates , 2018, Earth-Science Reviews.

[9]  A. Pearson,et al.  Carbon isotope ratios of coccolith–associated polysaccharides of Emiliania huxleyi as a function of growth rate and CO2 concentration , 2018 .

[10]  G. Reichart,et al.  Single-species dinoflagellate cyst carbon isotope ecology across the Paleocene-Eocene Thermal Maximum , 2017 .

[11]  A. Pearson,et al.  CO 2 -dependent carbon isotope fractionation in the dinoflagellate Alexandrium tamarense , 2017 .

[12]  Michael B. Wunder,et al.  Using ocean models to predict spatial and temporal variation in marine carbon isotopes , 2017 .

[13]  Dedmer B. Van de Waal,et al.  CO2-dependent carbon isotope fractionation in dinoflagellates relates to their inorganic carbon fluxes , 2016, Journal of experimental marine biology and ecology.

[14]  E. Achterberg,et al.  Interactive effects of ocean acidification and nitrogen limitation on two bloom-forming dinoflagellate species , 2016 .

[15]  R. Pancost,et al.  Gradual and sustained carbon dioxide release during Aptian Oceanic Anoxic Event 1a , 2016 .

[16]  G. Reichart,et al.  Stable carbon isotope fractionation of organic cyst-forming dinoflagellates: Evaluating the potential for a CO2 proxy , 2015 .

[17]  K. Scott,et al.  Isotopic discrimination and kinetic parameters of RubisCO from the marine bloom‐forming diatom, Skeletonema costatum , 2015, Geobiology.

[18]  Taro Takahashi,et al.  Climatological distributions of pH, pCO2, total CO2, alkalinity, and CaCO3 saturation in the global surface ocean, and temporal changes at selected locations , 2014 .

[19]  Uwe John,et al.  Ocean Acidification Reduces Growth and Calcification in a Marine Dinoflagellate , 2013, PloS one.

[20]  A. Vernal,et al.  Atlas of modern dinoflagellate cyst distribution based on 2405 data points , 2013 .

[21]  A. Rochon,et al.  Infra red spectroscopy, flash pyrolysis, thermally assisted hydrolysis and methylation (THM) in the presence of tetramethylammonium hydroxide (TMAH) of cultured and sediment-derived Lingulodinium polyedrum (Dinoflagellata) cyst walls , 2012 .

[22]  C. Cavanaugh,et al.  Low stable carbon isotope fractionation by coccolithophore RubisCO , 2011 .

[23]  Stefan Schouten,et al.  Stable carbon isotope patterns of marine biomarker lipids in the Arctic Ocean during Eocene Thermal Maximum 2 , 2011 .

[24]  J. S. Sinninghe Damsté,et al.  Transient Middle Eocene Atmospheric CO2 and Temperature Variations , 2010, Science.

[25]  G. Lange,et al.  A natural exposure experiment on short-term species-selective aerobic degradation of dinoflagellate cysts , 2008 .

[26]  David Morse,et al.  An External δ-Carbonic Anhydrase in a Free-Living Marine Dinoflagellate May Circumvent Diffusion-Limited Carbon Acquisition1[W] , 2008, Plant Physiology.

[27]  C. Marshall,et al.  Macromolecular composition of the dinoflagellate cyst Thalassiphora pelagica (Oligocene, SW Germany) , 2007 .

[28]  M. Pagani,et al.  Refining ancient carbon dioxide estimates: Significance of coccolithophore cell size for alkenone-based pCO2 records , 2007 .

[29]  D. Morse,et al.  CO2‐CONCENTRATING MECHANISMS OF THE POTENTIALLY TOXIC DINOFLAGELLATE PROTOCERATIUM RETICULATUM (DINOPHYCEAE, GONYAULACALES) 1 , 2007 .

[30]  U. Riebesell,et al.  Inorganic carbon acquisition in red tide dinoflagellates. , 2006, Plant, cell & environment.

[31]  J. Raven,et al.  CO2 concentrating mechanisms in algae: mechanisms, environmental modulation, and evolution. , 2005, Annual review of plant biology.

[32]  R. Fensome,et al.  Southern Ocean and Global Dinoflagellate Cyst Events Compared: Index Events for the Late Cretaceous–Neogene , 2004 .

[33]  M. Badger,et al.  Evidence for an inorganic carbon-concentrating mechanism in the symbiotic dinoflagellate Symbiodinium sp. , 1999, Plant physiology.

[34]  U. Riebesell,et al.  Effects of growth rate, CO2 concentration, and cell size on the stable carbon isotope fractionation in marine phytoplankton , 1999 .

[35]  D. Etheridge,et al.  A 1000-year high precision record of δ 13 C in atmospheric CO 2 , 1999 .

[36]  K. Grice,et al.  Biosynthetic effects on the stable carbon isotopic compositions of algal lipids: implications for deciphering the carbon isotopic biomarker record , 1998 .

[37]  G. Lange,et al.  Preservation of organic-walled dinoflagellate cysts in different oxygen regimes: a 10,000 year natural experiment , 1997 .

[38]  G. Hallegraeff A review of harmful algal blooms and their apparent global increase , 1993 .

[39]  J. Hayes,et al.  Fractionation of carbon isotopes by phytoplankton and estimates of ancient CO2 levels. , 1992, Global biogeochemical cycles.

[40]  C. Lorius,et al.  Vostok ice core provides 160,000-year record of atmospheric CO2 , 1987, Nature.

[41]  W. R. Evitt Sporopollenin Dinoflagellate Cysts: Their Morphology and Interpretation , 1985 .

[42]  M. O'Leary,et al.  Carbon isotope effects on enzyme-catalyzed carboxylation of ribulose bisphosphate , 1984 .

[43]  W. G. Mook,et al.  CARBON ISOTOPE FRACTIONATION BETWEEN DISSOLVED BICARBONATE AND GASEOUS CARBON-DIOXIDE , 1974 .

[44]  B. Dale,et al.  “Living Fossils” in Western Atlantic Plankton , 1966, Nature.

[45]  M. Pagani 12.13 – Biomarker-Based Inferences of Past Climate: The Alkenone pCO2 Proxy , 2014 .

[46]  Zhonghui Liu,et al.  High Earth-system climate sensitivity determined from Pliocene carbon dioxide concentrations , 2010 .

[47]  R. Pancost,et al.  Controls on the Carbon Isotopic Compositions of Lipids in Marine Environments , 2006 .

[48]  M. Badger,et al.  The roles of carbonic anhydrases in photosynthetic CO2 concentrating mechanisms , 2004, Photosynthesis Research.

[49]  Klas Lackschewitz,et al.  Proceedings of the Ocean Drilling Program , 2002 .

[50]  K. Freeman Isotopic Biogeochemistry of Marine Organic Carbon , 2001 .

[51]  J. Hayes Fractionation of Carbon and Hydrogen Isotopes in Biosynthetic Processes , 2001 .