Responses of globally important phytoplankton species to olivine dissolution products and implications for carbon dioxide removal via ocean alkalinity enhancement

Anthropogenic greenhouse gas emissions are leading to global temperature increases, ocean acidification, and significant ecosystem impacts. Given current emissions trajectories, the IPCC reports indicate that rapid abatement of CO2 emissions and development of carbon dioxide removal (CDR) strategies are needed to address legacy and difficult to abate emissions sources. These CDR methods must efficiently and safely sequester gigatons of atmospheric CO2. Coastal Enhanced Weathering (CEW) via the addition of the common mineral olivine to coastal waters is one promising approach to enhance ocean alkalinity for large-scale CDR. As olivine weathers, it releases several biologically active dissolution products, including alkalinity, trace metals, and the nutrient silicate. Released trace metals can serve as micronutrients but may also be toxic at high concentrations to marine biota including phytoplankton that lie at the base of marine food webs. We grew six species representing several globally important phytoplankton species under elevated concentrations of olivine dissolution products via a synthetic olivine leachate (OL) based on olivine elemental composition. We monitored their physiological and biogeochemical responses, which allowed us to determine physiological impacts and thresholds at elevated olivine leachate concentrations, in addition to individual effects of specific constituents. We found both positive and neutral responses but no evident toxic effects for two silicifying diatoms, a calcifying coccolithophore, and three cyanobacteria. In both single and competitive co-cultures, silicifiers and calcifiers benefited from olivine dissolution products like iron and silicate or enhanced alkalinity, respectively. The non-N2-fixing picocyanobacterium could use synthetic olivine-derived iron for growth, while N2-fixing cyanobacteria could not. However, other trace metals like nickel and cobalt supported cyanobacterial growth across both groups. Growth benefits to phytoplankton groups in situ will depend on species-specific responses and ambient concentrations of other required nutrients. Results suggest olivine dissolution products appear unlikely to cause negative physiological effects for any of the phytoplankton examined, even at high concentrations, and may support growth of particular taxa under some conditions. Future studies can shed light on long-term eco-evolutionary responses to olivine exposure and on the potential effects that marine microbes may in turn have on olivine dissolution rates and regional biogeochemistry.

[1]  J. Vink,et al.  Size-Fractionated Weathering of Olivine, Its CO2-Sequestration Rate, and Ecotoxicological Risk Assessment of Nickel Release , 2023, Minerals.

[2]  M. Tyka,et al.  Limits and CO2 equilibration of near-coast alkalinity enhancement , 2023, Biogeosciences.

[3]  Fei-xue Fu,et al.  The biogeochemical balance of oceanic nickel cycling , 2022, Nature Geoscience.

[4]  Fei-xue Fu,et al.  Molecular mechanisms underlying iron and phosphorus co-limitation responses in the nitrogen-fixing cyanobacterium Crocosphaera , 2022, The ISME Journal.

[5]  R. Strzepek,et al.  Investigating the effect of nickel concentration on phytoplankton growth to assess potential side-effects of ocean alkalinity enhancement , 2022, Biogeosciences.

[6]  Fei-xue Fu,et al.  Temperature variability interacts with mean temperature to influence the predictability of microbial phenotypes , 2022, Global change biology.

[7]  M. Grosso,et al.  The Availability of Limestone and Other Raw Materials for Ocean Alkalinity Enhancement , 2022, Global Biogeochemical Cycles.

[8]  R. Blust,et al.  Deriving Nickel (Ni(II)) and Chromium (Cr(III)) Based Environmentally Safe Olivine Guidelines for Coastal Enhanced Silicate Weathering. , 2021, Environmental science & technology.

[9]  D. Hutchins,et al.  The Enzymology of Ocean Global Change. , 2021, Annual review of marine science.

[10]  C. Dupont,et al.  Petrobactin, a siderophore produced by Alteromonas, mediates community iron acquisition in the global ocean , 2021, The ISME Journal.

[11]  Joshua D. Kling,et al.  Irradiance modulates thermal niche in a previously undescribed low-light and cold-adapted nano-diatom , 2020, bioRxiv.

[12]  M. Lomas,et al.  Potential for large-scale CO2 removal via enhanced rock weathering with croplands , 2020, Nature.

[13]  M. Saito,et al.  Minimal cobalt metabolism in the marine cyanobacterium Prochlorococcus , 2020, Proceedings of the National Academy of Sciences.

[14]  P. Renforth,et al.  CO2 Removal With Enhanced Weathering and Ocean Alkalinity Enhancement: Potential Risks and Co-benefits for Marine Pelagic Ecosystems , 2019, Front. Clim..

[15]  P. Renforth,et al.  The potential environmental response to increasing ocean alkalinity for negative emissions , 2018, Mitigation and Adaptation Strategies for Global Change.

[16]  Fei-xue Fu,et al.  Ocean warming alleviates iron limitation of marine nitrogen fixation , 2018, Nature Climate Change.

[17]  France Lam,et al.  Endocytosis-mediated siderophore uptake as a strategy for Fe acquisition in diatoms , 2018, Science Advances.

[18]  Tomoko Hasegawa,et al.  Scenarios towards limiting global mean temperature increase below 1.5 °C , 2018, Nature Climate Change.

[19]  K. Panneerselvam,et al.  Toxicity of Nickel on the Selected Species of Marine Diatoms and Copepods , 2018, Bulletin of Environmental Contamination and Toxicology.

[20]  Noelle A. Held,et al.  Transcriptional Activities of the Microbial Consortium Living with the Marine Nitrogen-Fixing Cyanobacterium Trichodesmium Reveal Potential Roles in Community-Level Nitrogen Cycling , 2017, Applied and Environmental Microbiology.

[21]  P. Renforth,et al.  Assessing ocean alkalinity for carbon sequestration , 2017 .

[22]  F. Meysman,et al.  Negative CO2 emissions via enhanced silicate weathering in coastal environments , 2017, Biology Letters.

[23]  P. Boyd,et al.  Marine phytoplankton and the changing ocean iron cycle , 2016 .

[24]  B. Kiran,et al.  Environmental toxicity: Exposure and impact of chromium on cyanobacterial species , 2016 .

[25]  Jana K. Maclaren,et al.  Reversal of ocean acidification enhances net coral reef calcification , 2016, Nature.

[26]  Mark R. Lomas,et al.  Enhanced weathering strategies for stabilizing climate and averting ocean acidification , 2015 .

[27]  Mary Ann Moran,et al.  The global ocean microbiome , 2015, Science.

[28]  D. Hutchins,et al.  Microbial biogeochemistry of coastal upwelling regimes in a changing ocean , 2013 .

[29]  P. Renforth,et al.  Enhanced chemical weathering as a geoengineering strategy to reduce atmospheric carbon dioxide, supply nutrients, and mitigate ocean acidification , 2013 .

[30]  J. Rimstidt,et al.  Systematic review of forsterite dissolution rate data , 2012 .

[31]  J. Moffett,et al.  The flux of iron and iron isotopes from San Pedro Basin sediments , 2012 .

[32]  Ruben E. Valas,et al.  Influence of cobalamin scarcity on diatom molecular physiology and identification of a cobalamin acquisition protein , 2012, Proceedings of the National Academy of Sciences.

[33]  C. Bowler,et al.  Iron Utilization in Marine Cyanobacteria and Eukaryotic Algae , 2011, Front. Microbio..

[34]  I. Berman‐Frank,et al.  Dust- and mineral-iron utilization by the marine dinitrogen-fixer Trichodesmium , 2011 .

[35]  Jonathan P Zehr,et al.  Genome-wide analysis of diel gene expression in the unicellular N2-fixing cyanobacterium Crocosphaera watsonii WH 8501 , 2010, The ISME Journal.

[36]  Fei-xue Fu,et al.  Interactions between changing pCO2, N2 fixation, and Fe limitation in the marine unicellular cyanobacterium Crocosphaera , 2008 .

[37]  C. Dupont,et al.  Ni Uptake and Limitation in Marine Synechococcus Strains , 2007, Applied and Environmental Microbiology.

[38]  Fei-xue Fu,et al.  CO2 control of Trichodesmium N2 fixation, photosynthesis, growth rates, and elemental ratios: Implications for past, present, and future ocean biogeochemistry , 2007 .

[39]  Y. Isoda,et al.  Effect of aging time on the availability of freshly precipitated ferric hydroxide to coastal marine diatoms , 2006 .

[40]  Fei-xue Fu,et al.  PHOSPHATE UPTAKE AND GROWTH KINETICS OF TRICHODESMIUM (CYANOBACTERIA) ISOLATES FROM THE NORTH ATLANTIC OCEAN AND THE GREAT BARRIER REEF, AUSTRALIA 1 , 2005 .

[41]  D. Hutchins,et al.  A trace metal clean reagent to remove surface-bound iron from marine phytoplankton , 2003 .

[42]  J. Randerson,et al.  Primary production of the biosphere: integrating terrestrial and oceanic components , 1998, Science.

[43]  E. Paasche,et al.  Growth and calcification in the coccolithophorid Emiliania huxleyi (Haptophyceae) at low salinities , 1996 .

[44]  W. Sunda,et al.  Cobalt and zinc interreplacement in marine phytoplankton: Biological and geochemical implications , 1995 .

[45]  N. Welschmeyer.  Fluorometric analysis of chlorophyll a in the presence of chlorophyll b and pheopigments , 1994 .

[46]  F. Millero,et al.  Chromium (III) interactions in seawater through its oxidation kinetics , 1991 .

[47]  F. Millero,et al.  The oxidation kinetics of Fe(II) in seawater , 1987 .

[48]  M. Brzezinski,et al.  THE Si:C:N RATIO OF MARINE DIATOMS: INTERSPECIFIC VARIABILITY AND THE EFFECT OF SOME ENVIRONMENTAL VARIABLES 1 , 1985 .

[49]  B. Frey,et al.  Sensitivity of estuarine phytoplankton to hexavalent chromium , 1983 .

[50]  C. H. V. D. Weijden,et al.  Chromium(III) -- chromium(VI) interconversions in seawater , 1982 .

[51]  S. R. Marigoudar,et al.  Toxicity assessment of cobalt and selenium on marine diatoms and copepods , 2019, Environmental Chemistry and Ecotoxicology.

[52]  M. Gehlen,et al.  Influence of diatom diversity on the ocean biological carbon pump , 2017, Nature Geoscience.

[53]  PeterKöhler JudithHauck,et al.  Iron fertilisation and century-scale effects of open ocean dissolution of olivine in a simulated CO 2 removal experiment , 2016 .

[54]  O. Matsuda,et al.  Phytoremediation of shallow organically enriched marine sediments using benthic microalgae. , 2008, Marine pollution bulletin.

[55]  F. Morel,et al.  Trace metal ion buffers and their use in culture studies , 2005 .

[56]  C. Wild,et al.  In situ measurements of advective solute transport in permeable shelf sands , 2004 .