Limitations on microalgal growth at very low photon fluence rates: the role of energy slippage.

The lower limits of photosynthetically useable radiation at which growth and photosynthesis can occur establish the lower boundaries for the extent of photolithotrophy in the biosphere. Photolithotrophic growth denotes the capacity to grow with photons as the sole energy input. Slippage in terms of photosynthetic energy conversion implies a less than theoretical stoichiometry of energy-transduction process(es) such as the dissipation of intermediates of O(2) evolution and of ATP synthesis (H(+)/e(-) and H(+)/ATP ratios). Slippage is particularly important in limiting the growth of photolithotrophic organisms at very low photon fluence rates. We found that Dunaliella tertiolecta and Phaeodactylum tricornutum avoid such reductions in photon use efficiency by increasing the size and number of their photosynthetic units, respectively, and by altering Q(A) reduction kinetics on the reducing side of PS II. P. tricornutum is also less susceptible to slippage in terms of the breakdown of intermediates in its O(2) evolution pathway than D. tertiolecta. Minimizing H(+) leakage through the CF(0)-CF(1) ATP synthetase (and other H(+ )porters) is also discussed briefly. In combination, strategies employed by P. tricornutum effectively allow it to grow and photosynthesize at lower rates of energy input than D. tertiolecta, consistent with our observations. Differences in the responses of the photosynthetic apparatus of these two marine microalgae are mechanistic and probably representative of evolutionary divergences associated with strategies for dealing with environmental perturbations.