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      Iron Limitation Modulates Ocean Acidification Effects on Southern Ocean Phytoplankton Communities

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          Abstract

          The potential interactive effects of iron (Fe) limitation and Ocean Acidification in the Southern Ocean (SO) are largely unknown. Here we present results of a long-term incubation experiment investigating the combined effects of CO 2 and Fe availability on natural phytoplankton assemblages from the Weddell Sea, Antarctica. Active Chl a fluorescence measurements revealed that we successfully cultured phytoplankton under both Fe-depleted and Fe-enriched conditions. Fe treatments had significant effects on photosynthetic efficiency (F v/F m; 0.3 for Fe-depleted and 0.5 for Fe-enriched conditions), non-photochemical quenching (NPQ), and relative electron transport rates (rETR). pCO 2 treatments significantly affected NPQ and rETR, but had no effect on F v/F m. Under Fe limitation, increased pCO 2 had no influence on C fixation whereas under Fe enrichment, primary production increased with increasing pCO 2 levels. These CO 2-dependent changes in productivity under Fe-enriched conditions were accompanied by a pronounced taxonomic shift from weakly to heavily silicified diatoms (i.e. from Pseudo-nitzschia sp. to Fragilariopsis sp.). Under Fe-depleted conditions, this functional shift was absent and thinly silicified species dominated all pCO 2 treatments ( Pseudo-nitzschia sp. and Synedropsis sp. for low and high pCO 2, respectively). Our results suggest that Ocean Acidification could increase primary productivity and the abundance of heavily silicified, fast sinking diatoms in Fe-enriched areas, both potentially leading to a stimulation of the biological pump. Over much of the SO, however, Fe limitation could restrict this possible CO 2 fertilization effect.

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          Enhanced biological carbon consumption in a high CO2 ocean.

          The oceans have absorbed nearly half of the fossil-fuel carbon dioxide (CO2) emitted into the atmosphere since pre-industrial times, causing a measurable reduction in seawater pH and carbonate saturation. If CO2 emissions continue to rise at current rates, upper-ocean pH will decrease to levels lower than have existed for tens of millions of years and, critically, at a rate of change 100 times greater than at any time over this period. Recent studies have shown effects of ocean acidification on a variety of marine life forms, in particular calcifying organisms. Consequences at the community to ecosystem level, in contrast, are largely unknown. Here we show that dissolved inorganic carbon consumption of a natural plankton community maintained in mesocosm enclosures at initial CO2 partial pressures of 350, 700 and 1,050 microatm increases with rising CO2. The community consumed up to 39% more dissolved inorganic carbon at increased CO2 partial pressures compared to present levels, whereas nutrient uptake remained the same. The stoichiometry of carbon to nitrogen drawdown increased from 6.0 at low CO2 to 8.0 at high CO2, thus exceeding the Redfield carbon:nitrogen ratio of 6.6 in today's ocean. This excess carbon consumption was associated with higher loss of organic carbon from the upper layer of the stratified mesocosms. If applicable to the natural environment, the observed responses have implications for a variety of marine biological and biogeochemical processes, and underscore the importance of biologically driven feedbacks in the ocean to global change.
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            The biogeochemical cycles of trace metals in the oceans.

            Planktonic uptake of some essential metals results in extraordinarily low concentrations in surface seawater. To sequester or take up these micronutrients, various microorganisms apparently release strong complexing agents and catalyze redox reactions that modify the bioavailability of trace metals and promote their rapid cycling in the upper water column. In turn, the low availability of some metals controls the rate of photosynthesis in parts of the oceans and the transformation and uptake of major nutrients such as nitrogen. The extremely low concentrations of several essential metals are both the cause and the result of ultraefficient uptake systems in the plankton and of widespread replacement of metals by one another for various biochemical functions.
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              Effect of ocean acidification on iron availability to marine phytoplankton.

              The acidification caused by the dissolution of anthropogenic carbon dioxide (CO2) in the ocean changes the chemistry and hence the bioavailability of iron (Fe), a limiting nutrient in large oceanic regions. Here, we show that the bioavailability of dissolved Fe may decline because of ocean acidification. Acidification of media containing various Fe compounds decreases the Fe uptake rate of diatoms and coccolithophores to an extent predicted by the changes in Fe chemistry. A slower Fe uptake by a model diatom with decreasing pH is also seen in experiments with Atlantic surface water. The Fe requirement of model phytoplankton remains unchanged with increasing CO2. The ongoing acidification of seawater is likely to increase the Fe stress of phytoplankton populations in some areas of the ocean.
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                Author and article information

                Contributors
                Role: Editor
                Journal
                PLoS One
                PLoS ONE
                plos
                plosone
                PLoS ONE
                Public Library of Science (San Francisco, USA )
                1932-6203
                2013
                20 November 2013
                : 8
                : 11
                : e79890
                Affiliations
                [1 ]Alfred Wegener Institute Helmholtz Centre for Polar and Marine Research, Bremerhaven, Germany
                [2 ]University of Technology Sydney, Plant Functional Biology and Climate Chance Cluster, New South Wales, Australia
                [3 ]University of British Columbia, Vancouver, British Columbia, Canada
                The Evergreen State College, United States of America
                Author notes

                Competing Interests: The authors have declared that no competing interests exist.

                Conceived and designed the experiments: CJMH ST BR CH PDT. Performed the experiments: CJMH ST CDP. Analyzed the data: CJMH ST CH CDP. Contributed reagents/materials/analysis tools: CJMH ST BR CH PDT CDP. Wrote the paper: CJMH ST BR CH PDT. Wrote the revised manuscript: CJMH ST BR CH PDT. Wrote the response to the reviewers: CJMH ST BR CH PDT.

                [¤]

                Current address: University of Geneva, Institute F. A. Forel, Versoix, Switzerland

                Article
                PONE-D-13-26603
                10.1371/journal.pone.0079890
                3835797
                24278207
                ee544b48-ae7f-471f-89c2-ec245c9f642f
                Copyright @ 2013

                This is an open-access article distributed under the terms of the Creative Commons Attribution License, which permits unrestricted use, distribution, and reproduction in any medium, provided the original author and source are credited.

                History
                : 27 June 2013
                : 7 October 2013
                Page count
                Pages: 9
                Funding
                S.T. was funded by the German Science Foundation (DFG; www.dfg.de), project TR 899/2. B.R. and C.J.M.H. were funded by the European Research Council (ERC; erc.europa.eu) under the European Community's Seventh Framework Programme (FP7/2007-2013), ERC grant agreement no. 205150. C.H. was funded by the Australian Research Council ( www.arc.gov.au; DP1092892) and a UTS Chancellor Fellowship ( www.uts.edu.au). P.D.T. was funded by an Alexander von Humboldt research fellowship ( http://www.humboldt-foundation.de)and grants from the Natural Sciences and Engineering Research Council of Canada ( www.nserc-crsng.gc.ca). The funders had no role in study design, data collection and analysis, decision to publish, or preparation of the manuscript.
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