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"We are conducting a great geochemical experiment, unlike anything in human history and unlikely to be repeated again on Earth. Within a few centuries we are returning to the atmosphere and oceans the concentrated organic carbon stored in sedimentary rocks over hundred of millions of years" (Revelle and Suess, 1957; Houghton, 2005).

1. Oceanic CO2 sinks and DMS sources as buffers of global climate changes

The comparison of the present atmospheric concentration of carbon dioxide (CO2) with the ice core record reveals that we have left the domain that defined the Earth system for the 650,000 yr before the industrial revolution. Atmospheric CO2 concentration is now nearly 100 ppmv higher, and has risen to that level at a rate at least 10 and possibly 100 times faster than at any other time in the past 650,000 yr (Falkowski et al., 2000; Siegenthaler et al., 2005). We have therefore driven the Earth system from the tightly bounded domain glacial-interglacial oscillations (Falkowski et al., 2000). The assessment of socio-economic repercussions of greenhouse-gas-induced climate changes is still challenging. However, perspectives are worrying enough to trigger the implementation of the Kyoto Protocol aiming to stabilize the concentration of greenhouse gases in the atmosphere.

Among the major naturally occurring atmospheric greenhouse gases (excluding water vapour), CO2 plays a dominant role in global warming, since it currently contributes about 55% of anthropogenic greenhouse forcing. The open ocean plays a crucial role in the sequestration of anthropogenic CO2: Human activities presently release about 7.1 Petagrams of carbon per year (PgC/yr) to the atmosphere, by fossil fuel burning and land use change. It is well established that 3.3 PgC/yr remain in the atmosphere, while the open ocean behaves as a sink estimated to be 1.9 PgC/yr and the terrestrial biosphere is often assumed to trap the remaining 1.9 PgC/yr. Hence, the open ocean acts as a major sink for anthropogenic CO2, which accounts for 27% of the total emissions of the anthropocene. Furthermore, the current fraction of total anthropogenic CO2 emissions stored in the open ocean appears to be about one-third of the long-term potential (Sabine et al., 2004).

It has been recently highlighted that marginal seas act on the whole as a significant sink for atmospheric CO2 ranging from -0.4 to -1.0 PgC/yr (Tsunogai et al., 1997; Thomas et al., 2004; Borges, 2005; Borges et al., 2005), which leads to a major revaluation of the overall oceanic sink for atmospheric CO2. Nonetheless, coastal ecosystems remain grossly under-represented in the global trace gas budgets used to inform global climate models and hence international climate policy. In addition, the air-water fluxes of CO2 from coastal environments stay highly uncertain and to a large extent this reflects insufficient data coverage (Borges 2005; Borges et al. 2005). Importantly, there is also a lack of fundamental understanding and quantification of biogeochemical drivers of air-sea CO2 fluxes. This hampers the validation and reliability of biogeochemical numerical models and their predictive quality that is intimately linked to the representation of the present-day CO2 fluxes and biogeochemical processes.

Dimethyl sulphide (DMS) through its oxidation products affects the number and size distribution of tropospheric cloud condensation nuclei, with possible consequences for cloud albedo and heat balance. The efficiency of this mechanism is still poorly constrained, but it could have a strong influence on climate (Watson and Liss, 1998). DMS acts on a much shorter time-scale than CO2, and as a result may well be a player on the "global change" time-scale. The direction of both the CO2 and the DMS mechanisms is such that an increase of marine productivity would lead to a decrease in the rise of global temperature.

2. Role of coccolithophores in the marine carbon and sulphur cycles

2.1 Coccolithophores and the carbon biological pump

Coccolithophores, among which Emiliania huxleyi (E. huxleyi) is the most abundant and widespread species, are considered to be the most productive calcifying organism on earth. E. huxleyi often forms massive blooms in temperate and sub-polar oceans, and in particular at continental margins and shelf seas. The intrinsic coupling of organic matter production and calcification in coccolithophorid blooms underlines their biogeochemical importance in the marine carbon cycle. Primary production via photosynthesis in the photic zone and vertical export of organic matter to deep waters draws down CO2:

CO2 + H2O → CH2O + O2

this is the so-called "organic carbon pump". In contrast, calcification and thus formation of biogenic calcium carbonate (CaCO3), consumes total and carbonate alkalinity and releases CO2:

Ca2+ + 2HCO3- → CaCO3 + H2O + CO2

this is often named the "carbonate counter-pump" because it counter-acts the effect on CO2 fluxes. This intimate coupling of the two pumps in coccolithophores, together with other calcifying organisms (mainly planktonic foraminifera), has been considered to be responsible for generating and maintaining the ocean's vertical distribution of total alkalinity (TA) in seawater and for regulating the atmospheric pCO2 since the Mesozoic era (Rost and Riebesell, 2004). The so-called Rain Ratio, defined here as the ratio of particulate inorganic carbon (PIC) to particulate organic carbon (POC) in exported biogenic matter, determines the relative strength of the two biological carbon pumps and consequently the flux of CO2 across the surface ocean - atmosphere interface. CaCO3 may also act as "ballast" and increase the transfer efficiency of organic matter from the surface ocean to the deep sea where it is remineralised (Armstrong et al., 2002; Klaas and Archer, 2002). Coccolithophores could thus contribute to the export of organic matter and the efficiency of the oceanic biological pump (atmospheric CO2 storage).

The status as source or sink for atmospheric CO2 is well established in ecosystems where the organic and inorganic carbon metabolisms are much contrasted. Three field studies on CO2 fluxes during coccolithophorid blooms (Robertson et al., 1994; Buitenhuis et al., 1996; Head et al., 1998) were carried out during the calcifying phase and not the organic carbon production phase of the life cycle of E. huxleyi. From one of these investigations conducted in the Northern North Atlantic, it was suggested that a coccolithophorid bloom acts a source of CO2 to the atmosphere (Robertson et al. 1994). However, during a recent mesocosm experiment that allowed the sampling through the full life cycle of E. huxleyi a distinct decreasing trend in pCO2 was observed, suggesting that the overall balance of the blooms was towards a sink for atmospheric CO2 (Delille et al., 2005). These mesocosm experiments lasted 4 weeks and the conclusions drawn cannot be readily extrapolated to field conditions where recurrent and successive blooms of coccolithophores occur.

2.2 Coccolithophores and Transparent Exopolymer Particles (TEP)

Carbon sequestration in the ocean is largely mediated by the rapidly sinking biogenic particles such as marine snow. Recent evidence suggests that the high-molecular weight (HMW) fraction of dissolved organic matter (DOM), the dissolved polysaccharides (PCHO), plays an important role in aggregation processes. Production and exudation of PCHO by phytoplankton cells is viewed as the result of a physiological imbalance between the assimilation of CO2 and of nutrients such as nitrate and phosphate, and generally increases with the degree of nutrient limitation (Wood and Van Valen, 1990). The exuded PCHO accumulate first in the dissolved pool (Fogg, 1966; Myklestad, 1995). Once the concentration of PCHO reaches the point at which aggregation occurs, PCHO rapidly form larger polysaccharide particles, known as transparent exopolymer particles (TEP) (Alldredge et al., 1993, Chin et al., 1998, Engel et al., 2004b), a process that substantially contributes to POC production towards the end of phytoplankton blooms (Engel et al., 2002 and 2004a).

It has been shown that TEP enhance particle aggregation (Logan et al., 1995; Engel, 2000; Ruiz et al., 2002) and participate in particle-mediated processes such as marine snow formation and sinking (Alldredge et al., 1993; Logan et al., 1995; Passow et al., 2001; Passow, 2002). During a recent mesocosm experiment with E. huxleyi, TEP concentration has been shown to increase after nutrient exhaustion and accumulated steadily until the end of the study (Engel, 2004a). Polysaccharide aggregation via TEP formation together with the CaCO3 ballast effect in E. huxleyi blooms have thus the potential to promote deep export of carbon on relatively short time scales.

2.3 Dissolution of biogenic CaCO3

Surface ocean waters are supersaturated with respect to CaCO3 (calcite or aragonite), which becomes more soluble with decreasing temperature and increasing pressure (hence depth). A natural boundary, the saturation horizon develops when the saturation states falls under unity and CaCO3 readily dissolves.

Dissolution of CaCO3 above the saturation horizon is required in order to explain the vertical profile of total alkalinity in the water column (Morse and Mackenzie, 1990; Wollast, 1994). Studies based on the vertical distribution of CaCO3 and sediment trap data in the Northeast Atlantic suggest that significant dissolution of CaCO3 is occurring in the upper 1000 m of the water column above the calcite or aragonite saturation horizon (Wollast and Chou, 1998; 2001). Milliman et al. (1999) explored the biologically mediated dissolution above the saturation horizon and suggested various pathways by which dissolution could take place. Even if grazing pressure is supposed to contribute greatly to dissolution, the influence of microbial activity, whether it is associated or not within microenvironments, cannot be excluded. Based on several water column inorganic carbon variables and ancillary data, Chung et al. (2003) estimated in situ CaCO3 dissolution rate in the Atlantic ocean to be 11.1 x 10^12 molC/yr corresponding to about 31% of a recent estimate of net CaCO3 production by Lee (2001) for the same area. In situ dissolution of CaCO3 provides additional total alkalinity to seawater and increases thus the capacity of the ocean to absorb CO2 from the atmosphere. Finally, based on global vertical distributions of TA and ancillary data, Feely et al. (2004) have shown that in most parts of the ocean anthropogenic CO2 has penetrated down to CaCO3 saturation horizons, leading to a rise of the latter. Hence, CaCO3 dissolution is at present time acting as a biogeochemical pump for anthropogenic CO2, and that could be underestimated since biologically mediated dissolution above the saturation horizon is not accounted for, as discussed in Sabine and Mackenzie (1991).

2.4 Coccolithophores and DMS cycling

Coccolithophorid blooms are known to produce extremely high amounts of DMS that is the principal source of sulphur to the atmosphere (Malin et al., 1993). Recent investigations during a coccolithophorid bloom in the North Sea, have underlined the importance of the microbial food web in the transformation of dimethylsulfoniopropionate (DMSP), the precursor of DMS, produced by phytoplankton (Burkill et al., 2002). The bacterial community was dominated by one taxon, α-proteobacteria related to Roseobacter that satisfied its entire sulphur demand by metabolising DMSP. In vitro DMSP-lyase activity was very high, but there was little evidence for high in situ activity (Zubkov et al., 2001). The abundance and diversity of these bacteria in marine habitats have been shown to be closely linked to DMS producing phytoplanktonic blooms (Gonzalez et al., 2000).

3. Responses of ecosystems and coccolithophorid calcification to oceanic acidification

Current model projections predict that surface ocean partial pressure of CO2 (pCO2) levels will double over their pre-industrial values by the middle of this century, with accompanying surface ocean pH changes that are 3 times greater than those experienced during the transition from glacial to interglacial periods (Falkowski et al., 2000). In vitro experiments suggest that the repercussions of such acidification could be significant on the phytoplanktonic communities, ecosystems and carbon cycle. Indeed, even if some studies have shown that marine autotrophic communities are often insensitive to pCO2 changes, several investigations have revealed that some seagrass (Zimmerman et al., 1997), macroalgae (Gao et al., 1993), diatom (Riebesell et al., 1993; Chen and Durbin, 1994), coccolithophore (Riebesell et al., 2000; Zondervan et al., 2001; Delille et al., 2005; Engel et al., 2005) and cyanobacteria (Qiu and Gao, 2002) species exhibit higher rates of photosynthesis under CO2 enrichment. It has also been shown that phytoplanktonic assemblages can experience marked shifts in composition under elevated pCO2 conditions (Boyd and Doney, 2002, Tortell et al., 2002; Martin-Jezequel et al., 2004). In mesocosm experiments, raising CO2 concentration enhances carbon export of coccolithophores, mainly due to the increase of TEP production and changes in the rain ratio (Delille et al., 2005; Engel et al., 2005).

Coccolithophores may respond in different ways to fossil fuel emissions and climate change over the next few centuries. In common with other marine calcifying organisms, there is evidence for sensitivity of coccolithophorid calcification rate to oceanic saturation state of calcite and aragonite (Ωcalcite and Ωaragonite), which will fall sharply as a consequence of rising atmospheric CO2 concentration and subsequent oceanic acidification. Conversely the acidification of seawater could increase in situ CaCO3 dissolution and thus the buffer capacity of the ocean. Comparison of global bloom maps from remote sensing suggests another possible response to global change. Despite the intrinsic decrease of Ωcalcite and Ωaragonite in the cold high latitude waters, blooms of E. huxleyi appear to be moving northwards towards/into the Arctic Ocean, with satellite images showing new bloom areas in the eastern Bering Sea and the Barents Sea (Tyrrell and Merico, 2004). The main drivers of future changes in the coccolithophorid distribution and the associated feedback mechanisms need thus to be better evaluated. For the time being, the large scale impacts of oceanic acidification on phytoplanktonic communities and carbon cycle (particularly in relation to CO2 sequestration) remain to be investigated (Gruber et al., 2004) and require a transdisciplinary approach.

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