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Is the Growth of Phytoplankton Limited by the Current Low Concentration of Atmospheric CO2?
Volume 7, Number 21: 26 May 2004

Gordillo et al. (2003) note that "one of the main queries for depicting future scenarios of evolution of atmospheric composition and temperature is whether an atmospheric CO2 increase stimulates primary production, especially in aquatic plants."  Why do they say aquatic plants?  Because, in their words, "aquatic primary producers account for about 50% of the total carbon fixation in the biosphere (Falkowski and Raven, 1997)."

Although the question Gordillo et al. address sounds simple enough, its answer is not nearly as straightforward.  In many marine and freshwater phytoplankton, for example, photosynthesis appears to be saturated under current environmental conditions.  Raven (1991), however, has proposed that those very same species, many of which employ carbon-concentrating mechanisms, could well decrease the amount of energy they expend in this latter activity in a CO2-enriched world, which metabolic readjustment would leave a larger proportion of their captured energy available for fueling enhanced growth.

To explore this possibility, the four scientists from the Universidad de Malaga in Spain studied various aspects of the growth response of the microalgal chlorophyte Dunaliella viridis Teodoresco (which possesses a carbon concentrating mechanism and has been used as a model species for the study of inorganic carbon uptake) to atmospheric CO2 enrichment.  Specifically, they batch cultured the chlorophyte, which is one of the most ubiquitous eukaryotic organisms in hypersaline environments, in 250-ml Perspex cylinders under controlled laboratory conditions at high (5 mM) and low (0.5 mM) nitrate concentrations, while continuously aerating half of the cultures with ambient air of approximately 350 ppm CO2 and the other half with air of approximately 10,000 ppm CO2.  So what did they find?

Atmospheric CO2 enrichment had little effect on dark respiration in both N treatments.  Likewise, it had little effect on photosynthesis in the low-N treatment.  In the high-N treatment, on the other hand, the extra CO2 increased photosynthesis by 114%.  In the case of biomass production the results were even more extreme: in the low-N treatment elevated CO2 had no effect at all, while in the high-N treatment it nearly tripled the cell density of the culture solution.

In discussing their findings, Gordillo et al. note that "it has long been debated whether phytoplankton species are growth-limited by current levels of CO2 in aquatic systems, i.e. whether an increase in atmospheric CO2 could stimulate growth (Riebesell et al., 1993)."  Their results clearly indicate that it can ? if sufficient nitrogen is available.

But that was not all that Gordillo et al. learned.  In the high-N treatment, where elevated CO2 greatly stimulated photosynthesis and biomass production, once the logarithmic growth phase had run its course and equilibrium growth was attained, approximately 70% of the carbon assimilated by the chlorophyte was released to the water, while in the low-CO2 treatment only 35% was released.

With respect to this suite of observations, Gordillo et al. report that "the release of organic carbon to the external medium has been proposed as a mechanism for maintaining the metabolic integrity of the cell (Ormerod, 1983)," and that "according to Wood and Van Valen (1990), organic carbon release would be a sink mechanism protecting the photosynthetic apparatus from an overload of products that cannot be invested in growth or stored."  They additionally state that stores of photosynthetic products "are reduced to avoid overload and produce a high demand for photosynthates."  Under these conditions, they conclude that "the process would then divert assimilated C to either the production of new biomass, or the release to the external medium once the culture conditions do not allow further exponential growth."  Interestingly, these ideas are closely analogous to the concept of acclimation in terrestrial plants that are exposed to elevated levels of atmospheric CO2 (see Acclimation in our Subject Index).

A second consequence of enhanced organic carbon release in the face of atmospheric CO2 enrichment and sufficient N availability is that the internal C:N balance of the phytoplankton is maintained within a rather tight range.  Even more exciting is the fact that this phenomenon has also been observed in the green seaweed Ulva rigida (Gordillo et al., 2001) and the cyanobacterium Spirulina platensis (Gordillo et al., 1999).  Hence, what the study of Gordillo et al. implies about the response of Dunaliella viridis to atmospheric CO2 enrichment may well be widely applicable to many, if not most, aquatic plants, not the least of which may be the zooxanthellae that by this means (enhanced organic carbon release) provide their coral hosts with the source of extra energy they need to continue building their skeletons at a non-reduced rate in the face of the negative calcification pressure produced by the changes in seawater chemistry that have been predicted to result from the ongoing rise in the air's CO2 concentration [see our Editorial of 25 Feb 2004].

Sherwood, Keith and Craig Idso

References
Falkowski, P.G. and Raven, J.A.  1997.  Aquatic Photosynthesis.  Blackwell Science, Massachusetts, USA.

Gordillo, F.J.L, Jimenez, C., Figueroa, F.L. and Niell, F.X.  1999.  Effects of increased atmospheric CO2 and N supply on photosynthesis, growth and cell composition of the cyanobacterium Spirulina platensis (Arthrospira).  Journal of Applied Phycology 10: 461-469.

Gordillo, F.J.L, Jimenez, C., Figueroa, F.L. and Niell, F.X.  2003.  Influence of elevated CO2 and nitrogen supply on the carbon assimilation performance and cell composition of the unicellular alga Dunaliella viridisPhysiologia Plantarum 119: 513-518.

Gordillo, F.J.L., Niell, F.X. and Figueroa, F.L.  2001.  Non-photosynthetic enhancement of growth by high CO2 level in the nitrophilic seaweed Ulva rigida C. Agardh (Chlorophyta).  Planta 213: 64-70.

Ormerod, J.G.  1983.  The carbon cycle in aquatic ecosystems.  In: Slater, J.H., Whittenbury, R. and Wimpeny, J.W.T.  (Eds.).  Microbes in Their Natural Environment.  Cambridge University Press, Cambridge, UK, pp. 463-482.

Raven, J.A.  1991.  Physiology of inorganic carbon acquisition and implications for resource use efficiency by marine phytoplankton: Relation to increased CO2 and temperature.  Plant, Cell and Environment 14: 774-794.

Riebesell, U., Wolf-Gladrow, D.A. and Smetacek, V.  1993.  Carbon dioxide limitation of marine phytoplankton growth rates.  Nature 361: 249-251.

Wood, A.M. and Van Valen, L.M.  1990.  Paradox lost?  On the release of energy rich compounds by phytoplankton.  Marine Microbial Food Webs 4: 103-116.