Photosynthesis in organisms in the oligotrophic oceans:
Carbon assimilation by marine phytoplankton is responsible for approximately 50% of the global primary productivity on the planet. Cyanobacteria dominate the world’s oceans where iron is often barely detectable. One manifestation of low iron adaptation in the oligotrophic marine environment is a decrease in levels of iron-rich photosynthetic components, including the reaction center of photosystem I and the cytochrome b6f complex. These thylakoid membrane components have well characterized roles in linear and cyclic photosynthetic electron transport and their low abundance creates potential impediments to photosynthetic function. Early in these studies, working with Synechococcus WH8102, we noticed a disparity between the activity of photosystem II and CO2 fixation; while CO2 fixation saturated at ~150 µmol photon m-2s-1, the photosysem II reaction centers were not completely closed, even at a light intensity of 2,000 µmol photon m-1s-1. This phenomenon was not apparent in organisms adapted to coastal environments (where there is much more available iron and nitrogen). The results were eye-opening for us. Ultimately, we demonstrated that the reason the reaction centers remained open was because of a very significant alternative flow of electrons out of photosystem II and to O2 (rather than using the electrons to fix CO2, see Figure 1) (Bailey et al., 2008). This alternative electron flow to O2 was observed in a mixed population of organisms collected (during a cruise) from open-ocean environments (Mackey et al., 2008). Furthermore, our recent collaborations with Francis-Andre Wollman’s group and Giovanni Finazzi have demonstrated that the photosynthetic picoeukaryotes (not only the cyanobacteria) in the open-ocean environment, also show significant electron flow to O2 (Cardol et al., 2008). This alternative electron flow appears to extract electrons from the intersystem electron transport chain, prior to photosystem I. Inhibitor studies demonstrate that a propylgallate-sensitive oxidase mediates electron flow to O2. There are a number of ecological/physiological reasons why this adaptation would have occurred. Since iron is limiting and photosystem I requires a lot of iron for its biogenesis (12 irons per photosystem I), the cells have adapted to live with less iron, and consequently with less photosystem I (even if you give the cells iron they can’t make more photosystem I). The lack of photosystem I is dangerous and would ultimately result in the generation of reactive species at the level of photosystem II and burn up the cell. Therefore, the oxidase would alleviate excessive photosystem II excitation pressure by pulling electrons out of photosystem II, which would rapidly de-excite the pigment molecules and prevent the formation of reactive oxygen species. But this adaptation would also result in a larger ΔpH across the thylakoid membranes, which could be rapidly converted into useful energy that would drive the efficient uptake of any nutrients that can be scavenged from the environment (the cells probably can’t grow very fast because of the lack of nutrients, but they do want to have the energy available to take up the nutrients when they become available). Furthermore, since this seems to be a dominant phenomenon in the open oceans, and open ocean samples were not well represented in the data set used to establish correlations between photosynthetic pigments in the oceans and primary CO2 fixation, we feel (and this has been controversial) that this needs to be considered more when generating models predicting primary productivity in the open oceans.
Figure 1. Photosynthetic electron flow and state transitions were monitored using PAM fluorescence in the absence of O2. In (A) and (B) the fluorescence was monitored under anoxic conditions after purging the cell suspensions with argon gas for 1 min, which was delivered via a needle through the rubber stopper of a home made cuvette. The rubber stopper was made air-tight with silica gel following removal of the needle. A further 5–10 min of dark respiration was required to achieve full anoxia, which was necessary to observe the characteristic light-dependent quenching of fluorescence. O2 was re-introduced into the cell suspension through delivery of 1 ml of air (indicated as +1 ml air) using a needle and syringe (A). In (B), the cuvette remained sealed throughout the recording of the fluorescence trace. The asterisk in both (A) and (B) highlights the saturating light pulse during actinic irradiance, showing no variable fluorescence early after exposing the cells to light.