So how are lipids affected by elevated concentrations of atmospheric CO2?

Sgherri et al. (1998) grew alfalfa in open-top chambers at ambient (340 ppm) and enriched (600 ppm) CO2 concentrations for twenty-five days, after which they withheld water from the plants for five additional days.  Among other things, they found that the plants grown at the elevated CO2 concentration maintained greater leaf lipid to protein ratios, especially under conditions of water stress.  Moreover, leaf lipid contents in the plants grown in the CO2-enriched air were 22 and 83% higher than those in the plants grown in ambient air for periods of ample and insufficient soil moisture, respectively.  Also, the degrees of unsaturation of two of the most important lipids of the thylakoid membranes (which are found within chloroplasts and contain chlorophyll, other pigments that absorb sunlight, and specialized protein complexes that convert sunlight into usable cellular energy during photosynthesis) were approximately 20 and 37% greater in the high- compared to the low-CO2 treatments during times of adequate and inadequate soil moisture, respectively.

Sgherri et al. suggest that the greater lipid contents observed in CO2-enriched air and their increased degree of unsaturation may allow thylakoid membranes to maintain a more fluid and stable environment, which is critical during periods of water stress in enabling plants to continue photosynthetic carbon uptake.  These effects are so important, in fact, that some researchers have suggested that adaptive plant responses such as these may allow plants to better cope with any altered environmental condition that produces stress.  Hence, with greater amounts of CO2 in the air, the resulting greater lipid contents of thylakoid membranes plus their greater degree of unsaturation may provide greater membrane stability and integrity, thereby allowing proper functioning in times of drought or other adverse environmental conditions; and in some situations, these CO2-induced adaptations may mean the difference between a plant's living or dying.

Consider, for example, the stress of exposure to overly cold temperatures that often leads to chilling injury in plants.  In our Editorial of 13 Nov 2002, we describe a number of studies of this phenomenon and the roll played by membrane lipid unsaturation in alleviating chilling injury.

In one of the studies, Hughly and Somerville (1992) worked with wild-type Arabidopsis thaliana and two mutants of the species that were deficient in thylakoid lipid unsaturation.  They found that "chloroplast membrane lipid polyunsaturation contributes to the low-temperature fitness of the organism," and that it is required for some aspect of chloroplast biogenesis.  When lipid polyunsaturation was low, for example, they observed what they call "dramatic reductions in chloroplast size, membrane content, and organization in developing leaves."  Furthermore, they say there was a positive correlation "between the severity of chlorosis in the two mutants at low temperatures and the degree of reduction in polyunsaturated chloroplast lipid composition."

Working with tobacco, Kodama et al. (1994) demonstrated that the low-temperature-induced suppression of leaf growth and concomitant induction of chlorosis observed in wild-type plants was much less evident in transgenic plants containing a gene that allowed for greater expression of unsaturation in the fatty acids of leaf lipids.  This observation and others led them to conclude that substantially unsaturated fatty acids "are undoubtedly an important factor contributing to cold tolerance."

In a closely related study, Moon et al. (1995) found that heightened unsaturation of the membrane lipids of chloroplasts stabilized the photosynthetic machinery of transgenic tobacco plaints against low-temperature photoinibition "by accelerating the recovery of the photosystem II protein complex."  Likewise, Kodama et al. (1995), also working with transgenic tobacco plants, showed that increased fatty acid desaturation is one of the prerequisites for normal leaf development at low, nonfreezing temperatures; and Ishizaki-Nishizawa et al. (1996) demonstrated that transgenic tobacco plants with a reduced level of saturated fatty acids in most membrane lipids "exhibited a significant increase in chilling resistance."

These observations are laden with significance for earth's agro-ecosystems.  Many economically important crops, such as rice, maize and soybeans, are classified as chilling-sensitive; and they experience injury or death at temperatures between 0 and 15°C (Lyons, 1973).  If atmospheric CO2 enrichment enhances their production of thylakoid lipids and their degree of unsaturation, as it does in alfalfa, a continuation of the ongoing rise in the air's CO2 content could increase the abilities of these critically important agricultural species to withstand periodic exposure to debilitating low temperatures; and this phenomenon could provide the extra boost to food production that will be needed to sustain our increasing numbers in the years and decades ahead (Tilman et al., 2001).

Ratcheting up the elevated CO2 exposure time of Sgherri et al.'s alfalfa study from days to years, Hussain et al. (2001) collected and analyzed seeds from loblolly pine trees exposed to atmospheric CO2 concentrations of either 350 or 560 ppm since 1996 in the Duke Forest FACE study.  They found that seeds collected from the CO2-enriched trees were 90% heavier than seeds collected from the trees growing in ambient air, and that their mean lipid content was 265% greater.  In working further with the two sets of seeds, they found that the germination success of those developed under CO2-enriched conditions was more than three times greater than that of the seeds from the ambient-air treatment, regardless of germination CO2 concentration.  In addition, seeds from the CO2-enriched trees germinated approximately five days earlier, regardless of germination CO2 concentration; and the seedlings derived from the seeds collected from the CO2-enriched trees displayed significantly greater root lengths and needle numbers than those derived from seeds collected from the ambient-treatment trees.

Moving from years to decades of atmospheric CO2 enrichment, Schwanz and Polle (1998) evaluated the degree of lipid peroxidation in leaves of mature holm and white oak trees that had been growing in the vicinity of natural CO2 springs in central Italy for close to half a century.  In doing so, they found that the trees growing in close proximity to the CO2-emitting springs often exhibited lipid peroxidation reductions, which are indicative of less intrinsic oxidative stress and the presence of fewer internal harmful oxidants, in harmony with results that have been obtained from experiments ranging in duration form days to years.

Another important change of experimental venue is that which occurs in moving from the aerial terrestrial environment to the watery world that exists beneath the surface of the sea. One study to address this situation was that of Yu et al. (2004), who grew the marine microalgae Platymonas subcordiformis in the laboratory at ambient levels of atmospheric CO2 concentration and UV-B radiation flux density, as well as at elevated levels of 5000 ppm CO2 and the UV-B radiation flux anticipated to result from a 25% stratospheric ozone depletion under clear sky conditions in summer.  By itself, they report that the elevated UV-B treatment significantly increased the production of the toxic superoxide anion and hydrogen peroxide, as well as malonyldialdehyde, which is an end product of lipid peroxidation, whereas elevated CO2 by itself did just the opposite.  In addition, in the treatment consisting of elevated UV-B and elevated CO2, the concentrations of these three substances were all lower than those observed in the elevated UV-B and ambient CO2 treatment.  Consequently, Yu et al. conclude that "CO2 enrichment could reduce oxidative stress of reactive oxygen species to P. subcordiformis, and reduce the lipid peroxidation damage of UV-B to P. subcordiformis."

An interesting aspect of these findings is what they imply about coral bleaching.  In the introduction to their recent review of this important subject, Smith et al. (2005) report that "photoinhibition of photosynthesis and photodamage to photosystem II of the zooxanthellae, with the consequent increase in the production of damaging reactive oxygen species (ROS), have been implicated as the cause of thermal bleaching (Brown, 1997; Fitt et al., 2001; Lesser, 2004; Tchernov et al., 2004)," while at the end of their review, they additionally report that the "thermal bleaching of many corals is ultimately the result of the destruction of photosynthetic pigments by ROS," and that the production by the zooxanthellae of one particular ROS, hydrogen peroxide, "may be a signal that triggers a response in the host cell to eject the zooxanthellae or shed the host cell from the coral."  Combining these observations with the finding of Yu et al. that CO2 enrichment counters the production of hydrogen peroxide, it follows that some degree of atmospheric CO2 enrichment should likewise cause host cells to not eject their zooxanthellae (see our Editorial of 18 May 2005).

Last of all, we report on a study (Goverde et al., 2002) of the impact of atmospheric CO2 enrichment on lipid concentrations in the body of an animal, specifically, the satyrid butterfly (Coenonympha pamphilus), larvae of which were raised in seminatural, undisturbed calcareous grassland plots exposed to atmospheric CO2 concentrations of 370 and 600 ppm for five growing seasons.  This work revealed, among other things, that the elevated atmospheric CO2 concentration increased lipid concentrations in the bodies of adult male butterflies by nearly 14%.  Consequently, since these compounds are used as energy resources in these and other butterflies, this animal species - and perhaps others - will likely exhibit positive responses to future increases in the air's CO2 concentration.

In summary, it would appear that the positive impacts of atmospheric CO2 enrichment on lipid concentrations and characteristics in various terrestrial and aquatic plants, and on the satyrid butterfly discussed in the preceding paragraph, portend nothing but good for both the managed and unmanaged components of the biosphere as the air's CO2 content continues to climb in the years and decades ahead.

References
Brown, B.E.  1997.  Coral bleaching: causes and consequences.  Coral Reefs 16: S129-S138.

Fitt, W.K., Brown, B.E., Warner, M.E. et al.  2001.  Coral bleaching: interpretation of thermal tolerance limits and thermal thresholds in tropical corals.  Coral Reefs 20: 51-65.

Goverde, M., Erhardt, A. and Niklaus, P.A.  2002.  In situ development of a satyrid butterfly on calcareous grassland exposed to elevated carbon dioxide.  Ecology 83: 1399-1411.

Hugly, S. and Somerville, C.  1992.  A role for membrane lipid polyunsaturation in chloroplast biogenesis at low temperature.  Plant Physiology 99: 197-202.

Hussain, M., Kubiske, M.E. and Connor, K.F.  2001.  Germination of CO2-enriched Pinus taeda L. seeds and subsequent seedling growth responses to CO2 enrichment.  Functional Ecology 15: 344-350.

Ishizaki-Nishizawa, O., Fujii, T., Azuma, M., Sekiguchi, K., Murata, N., Ohtani, T. and Toguri T.  1996.  Low-temperature resistance of higher plants is significantly enhanced by a nonspecific cyanobacterial desaturase.  Nature Biotechnology 14: 1003-1006.

Kodama, H., Hamada, T., Horiguchi, G., Nishimura, M. and Iba, K.  1994.  Genetic enhancement of cold tolerance by expression of a gene for chloroplast w-3 fatty acid desaturase in transgenic tobacco.  Plant Physiology 105: 601-605.

Kodama, H., Horiguchi, G., Nishiuchi, T., Nishimura, M. and Iba, K.  1995.  Fatty acid desaturation during chilling acclimation is one of the factors involved in conferring low-temperature tolerance to young tobacco leaves.  Plant Physiology 107: 1177-1185.

Lesser, M.P.  2004.  Experimental biology of coral reef systems.  Journal of Experimental Marine Biology and Ecology 300: 217-252.

Lyons, J.M.  1973.  Chilling injury in plants.  Annual Review of Plant Physiology 24: 445-466.

Moon, B.Y., Higashi, S.-I., Gombos, Z. and Murata, N.  1995.  Unsaturation of the membrane lipids of chloroplasts stabilizes the photosynthetic machinery against low-temperature photoinhibition in transgenic tobacco plants.  Proceedings of the National Academy of Sciences, USA 92: 6219-6223.

Schwanz, P. and Polle, A.  1998.  Antioxidative systems, pigment and protein contents in leaves of adult mediterranean oak species (Quercus pubescens and Q. ilex) with lifetime exposure to elevated CO2.  New Phytologist 140: 411-423.

Sgherri, C.L.M., Quartacci, M.F., Menconi, M., Raschi, A. and Navari-Izzo, F.  1998.  Interactions between drought and elevated CO2 on alfalfa plants.  Journal of Plant Physiology 152: 118-124.

Smith, D.J., Suggett, D.J. and Baker, N.R.  2005.  Is photoinhibition of zooxanthellae photosynthesis the primary cause of thermal bleaching in corals?  Global Change Biology 11: 1-11.

Tchernov, D., Gorbunov, M.Y. de Vargas, C. et al.  2004.  Membrane lipids of symbiotic algae are diagnostic of sensitivity to thermal bleaching in corals.  Proceedings of the National Academy of Sciences USA 101: 13,531-13,535.

Tilman, D., Fargione, J., Wolff, B., D'Antonio, C., Dobson, A., Howarth, R., Schindler, D., Schlesinger, W.H., Simberloff, D. and Swackhamer, D.  2001.  Forecasting agriculturally driven global environmental change.  Science 292: 281-284.

Yu, J., Tang, X-X., Zhang, P-Y., Tian, J-Y. and Cai, H-J.  2004.  Effects of CO2 enrichment on photosynthesis, lipid peroxidation and activities of antioxidative enzymes of Platymonas subcordiformis subjected to UV-B radiation stress.  Acta Botanica Sinica 46: 682-690.