Björn Rost

Reduced calcification of marine plankton in response to increased atmospheric CO2.

The formation of calcareous skeletons by marine planktonic organisms and their subsequent sinking to depth generates a continuous rain of calcium carbonate to the deep ocean and underlying sediments. This is important in regulating marine carbon cycling and ocean–atmosphere CO2 exchange. The present rise in atmospheric CO2 levels causes significant changes in surface ocean pH and carbonate chemistry. Such changes have been shown to slow down calcification in corals and coralline macroalgae,, but the majority of marine calcification occurs in planktonic organisms. Here we report reduced calcite production at increased CO2 concentrations in monospecific cultures of two dominant marine calcifying phytoplankton species, the coccolithophorids Emiliania huxleyi and Gephyrocapsa oceanica . This was accompanied by an increased proportion of malformed coccoliths and incomplete coccospheres. Diminished calcification led to a reduction in the ratio of calcite precipitation to organic matter production. Similar results were obtained in incubations of natural plankton assemblages from the north Pacific ocean when exposed to experimentally elevated CO2 levels. We suggest that the progressive increase in atmospheric CO2 concentrations may therefore slow down the production of calcium carbonate in the surface ocean. As the process of calcification releases CO2 to the atmosphere, the response observed here could potentially act as a negative feedback on atmospheric CO2 levels.

Decreasing marine biogenic calcification: A negative feedback on rising atmospheric pCO2

In laboratory experiments with the coccolithophore species Emiliania huxleyi and Gephyrocapsa oceanica, the ratio of particulate inorganic carbon (PIC) to particulate organic carbon (POC) production decreased with increasing CO2 concentration ([CO2]). This was due to both reduced PIC and enhanced POC production at elevated [CO2]. Carbon dioxide concentrations covered a range from a preindustrial level to a value predicted for 2100 according to a “business as usual” anthropogenic CO2 emission scenario. The laboratory results were used to employ a model in which the immediate effect of a decrease in global marine calcification relative to POC production on the potential capacity for oceanic CO2 uptake was simulated. Assuming that overall marine biogenic calcification shows a similar response as obtained for E. huxleyi or G. oceanica in the present study, the model reveals a negative feedback on increasing atmospheric CO2 concentrations owing to a decrease in the PIC/POC ratio.

Effect of CO2 concentration on the PIC/POC ratio in the coccolithophore Emiliania huxleyi grown under light-limiting conditions and different daylengths.

We compared the effect of CO2 concentration ([CO2], ranging from ∼5 to ∼34 μmol l−1) at four different photon flux densities (PFD=15, 30, 80 and 150 μmol m−2 s−1) and two light/dark (L/D) cycles (16/8 and 24/0 h) on the coccolithophore Emiliania huxleyi. With increasing [CO2], a decrease in the particulate inorganic carbon to particulate organic carbon (PIC/POC) ratio was observed at all light intensities and L/D cycles tested. The individual response in cellular PIC and POC to [CO2] depended strongly on the PFD. POC production increased with rising [CO2], irrespective of the light intensity, and PIC production decreased with increasing [CO2] at a PFD of 150 μmol m−2 s−1, whereas below this light level it was unaffected by [CO2]. Cell growth rate decreased with decreasing PFD, but was largely independent of ambient [CO2]. The diurnal variation in PIC and POC content, monitored over a 38-h period (16/8 h L/D, PFD=150 μmol m−2 s−1), exceeded the difference in carbon content between cells grown at high (∼29 μmol l−1) and low (∼4 μmol l−1) [CO2]. However, consistent with the results described above, cellular POC content was higher and PIC content lower at high [CO2], compared to the values at low [CO2], and the offset was observed throughout the day. It is suggested that the observed sensitivity of POC production for ambient [CO2] may be of importance in regulating species-specific primary production and species composition.

Coccolithophores and the biological pump: responses to environmental changes

Summary Coccolithophores, which are considered to be the most productive calcifying organisms on earth, play an important role in the marine carbon cycle. The formation of calcite skeletons in the surface layer and their subsequent sinking to depth modifies upper-ocean alkalinity and directly affects air/sea CO2 exchange. Recent work indicates that the productivity and distribution of coccolithophores are sensitive to CO2-related changes in environmental conditions, both directly through acidification of surface seawater and indirectly through increasing upper-ocean thermal stratification. To assess possible responses of this group we examine the physiology and ecology of coccolithophores with regard to expected environmental changes. Potential feedbacks to atmospheric CO2 increase, as could arise from changes in photosynthesis and calcification as well as from a shift in the dominance of coccolithophores, may be crucial when trying to forecast future climate change.

Evolutionary potential of marine phytoplankton under ocean acidification

Marine phytoplankton have many obvious characters, such as rapid cell division rates and large population sizes, that give them the capacity to evolve in response to global change on timescales of weeks, months or decades. However, few studies directly investigate if this adaptive potential is likely to be realized. Because of this, evidence of to whether and how marine phytoplankton may evolve in response to global change is sparse. Here, we review studies that help predict evolutionary responses to global change in marine phytoplankton. We find limited support from experimental evolution that some taxa of marine phytoplankton may adapt to ocean acidification, and strong indications from studies of variation and structure in natural populations that selection on standing genetic variation is likely. Furthermore, we highlight the large body of literature on plastic responses to ocean acidification available, and evolutionary theory that may be used to link plastic and evolutionary responses. Because of the taxonomic breadth spanned by marine phytoplankton, and the diversity of roles they fill in ocean ecosystems and biogeochemical cycles, we stress the necessity of treating taxa or functional groups individually.

Combined Effects of CO2 and Light on the N2-Fixing Cyanobacterium Trichodesmium IMS101: Physiological Responses

Recent studies on the diazotrophic cyanobacterium Trichodesmium erythraeum (IMS101) showed that increasing CO2 partial pressure (pCO2) enhances N2 fixation and growth. Significant uncertainties remain as to the degree of the sensitivity to pCO2, its modification by other environmental factors, and underlying processes causing these responses. To address these questions, we examined the responses of Trichodesmium IMS101 grown under a matrix of low and high levels of pCO2 (150 and 900 μatm) and irradiance (50 and 200 μmol photons m−2 s−1). Growth rates as well as cellular carbon and nitrogen contents increased with increasing pCO2 and light levels in the cultures. The pCO2-dependent stimulation in organic carbon and nitrogen production was highest under low light. High pCO2 stimulated rates of N2 fixation and prolonged the duration, while high light affected maximum rates only. Gross photosynthesis increased with light but did not change with pCO2. HCO3− was identified as the predominant carbon source taken up in all treatments. Inorganic carbon uptake increased with light, but only gross CO2 uptake was enhanced under high pCO2. A comparison between carbon fluxes in vivo and those derived from 13C fractionation indicates high internal carbon cycling, especially in the low-pCO2 treatment under high light. Light-dependent oxygen uptake was only detected under low pCO2 combined with high light or when low-light-acclimated cells were exposed to high light, indicating that the Mehler reaction functions also as a photoprotective mechanism in Trichodesmium. Our data confirm the pronounced pCO2 effect on N2 fixation and growth in Trichodesmium and further show a strong modulation of these effects by light intensity. We attribute these responses to changes in the allocation of photosynthetic energy between carbon acquisition and the assimilation of carbon and nitrogen under elevated pCO2. These findings are supported by a complementary study looking at photosynthetic fluorescence parameters of photosystem II, photosynthetic unit stoichiometry (photosystem I:photosystem II), and pool sizes of key proteins in carbon and nitrogen acquisition.

Iron Limitation Modulates Ocean Acidification Effects on Southern Ocean Phytoplankton Communities

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 CO2 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 (Fv/Fm; 0.3 for Fe-depleted and 0.5 for Fe-enriched conditions), non-photochemical quenching (NPQ), and relative electron transport rates (rETR). pCO2 treatments significantly affected NPQ and rETR, but had no effect on Fv/Fm. Under Fe limitation, increased pCO2 had no influence on C fixation whereas under Fe enrichment, primary production increased with increasing pCO2 levels. These CO2-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 pCO2 treatments (Pseudo-nitzschia sp. and Synedropsis sp. for low and high pCO2, 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 CO2 fertilization effect.

Ocean acidification reduces growth and calcification in a marine dinoflagellate

Ocean acidification is considered a major threat to marine ecosystems and may particularly affect calcifying organisms such as corals, foraminifera and coccolithophores. Here we investigate the impact of elevated pCO2 and lowered pH on growth and calcification in the common calcareous dinoflagellate Thoracosphaera heimii. We observe a substantial reduction in growth rate, calcification and cyst stability of T. heimii under elevated pCO2. Furthermore, transcriptomic analyses reveal CO2 sensitive regulation of many genes, particularly those being associated to inorganic carbon acquisition and calcification. Stable carbon isotope fractionation for organic carbon production increased with increasing pCO2 whereas it decreased for calcification, which suggests interdependence between both processes. We also found a strong effect of pCO2 on the stable oxygen isotopic composition of calcite, in line with earlier observations concerning another T. heimii strain. The observed changes in stable oxygen and carbon isotope composition of T. heimii cysts may provide an ideal tool for reconstructing past seawater carbonate chemistry, and ultimately past pCO2. Although the function of calcification in T. heimii remains unresolved, this trait likely plays an important role in the ecological and evolutionary success of this species. Acting on calcification as well as growth, ocean acidification may therefore impose a great threat for T. heimii.

Transcriptome analyses reveal differential gene expression patterns between the life-cycle stages of Emiliania Huxleyi (haptophyta) and reflect specialization to different ecological niches

Coccolithophores, especially the abundant, cosmopolitan species Emiliania huxleyi (Lohmann) W. W. Hay et H. P. Mohler, are one of the main driving forces of the oceanic carbonate pump and contribute significantly to global carbon cycling, due to their ability to calcify. A recent study indicates that termination of diploid blooms by viral infection induces life‐cycle transition, and speculation has arisen about the role of the haploid, noncalcifying stage in coccolithophore ecology. To explore gene expression patterns in both life‐cycle stages, haploid and diploid cells of E. huxleyi (RCC 1217 and RCC 1216) were acclimated to limiting and saturating photon flux densities. Transcriptome analyses were performed to assess differential genomic expression related to different ploidy levels and acclimation light intensities. Analyses indicated that life‐cycle stages exhibit different properties of regulating genome expression (e.g., pronounced gene activation and gene silencing in the diploid stage), proteome maintenance (e.g., increased turnover of proteins in the haploid stage), as well as metabolic processing (e.g., pronounced primary metabolism and motility in the haploid stage and calcification in the diploid stage). Furthermore, higher abundances of transcripts related to endocytotic and digestive machinery were observed in the diploid stage. A qualitative feeding experiment indicated that both life‐cycle stages are capable of particle uptake (0.5 μm diameter) in late‐stationary growth phase. Results showed that the two life‐cycle stages represent functionally distinct entities that are evolutionarily shaped to thrive in the environment they typically inhabit.

Environmental stability affects phenotypic evolution in a globally distributed marine picoplankton

Marine phytoplankton can evolve rapidly when confronted with aspects of climate change because of their large population sizes and fast generation times. Despite this, the importance of environment fluctuations, a key feature of climate change, has received little attention—selection experiments with marine phytoplankton are usually carried out in stable environments and use single or few representatives of a species, genus or functional group. Here we investigate whether and by how much environmental fluctuations contribute to changes in ecologically important phytoplankton traits such as C:N ratios and cell size, and test the variability of changes in these traits within the globally distributed species Ostreococcus. We have evolved 16 physiologically distinct lineages of Ostreococcus at stable high CO2 (1031±87 μatm CO2, SH) and fluctuating high CO2 (1012±244 μatm CO2, FH) for 400 generations. We find that although both fluctuation and high CO2 drive evolution, FH-evolved lineages are smaller, have reduced C:N ratios and respond more strongly to further increases in CO2 than do SH-evolved lineages. This indicates that environmental fluctuations are an important factor to consider when predicting how the characteristics of future phytoplankton populations will have an impact on biogeochemical cycles and higher trophic levels in marine food webs.