A photosynthetic strategy for coping in a high-light, low-nutrient environment

Phytoplankton in high-light, low-nutrient ocean environments are challenged with maintaining high photosynthetic efficiency and simultaneously preventing photodamage that results from low levels of electron acceptors downstream of photosystem II (PSII). Here, we identify a process in open ocean picophytoplankton that preserves PSII activity by diverting electrons from the photosystem I (PSI) complex–mediated carbon assimilation to oxygen via a propyl gallate–sensitive oxidase associated with the photosynthetic electron transport chain. This process stabilizes diel photochemical efficiency of PSII, despite midday photoinhibition, by maintaining oxidized PSII reaction centers. Although measurements of the maximum photochemical efficiency of PSII, Fv : Fm show midday photoinhibition, midday CO2 fixation is not depressed. Moreover, CO2 fixation saturates at low irradiances even though PSII electron flow is not saturated at irradiances of 1,985 mmol photons m22 s21. This disparity between PSII fluorescence and CO2 fixation is consistent with the activity of an oxidase that serves as a terminal electron acceptor, maintaining oxidized PSII reaction centers even when CO2 fixation has saturated and the total number of functional reaction centers decreases because of photoinhibition (reflected in lower midday Fv : Fm values). This phenomenon is less apparent in coastal phytoplankton populations, suggesting that it is a strategy particularly distinctive of phytoplankton in the oligotrophic ocean. Spatial variability in features of photosynthetic electron flow could explain biogeographical differences in productivity throughout the ocean and should be represented in models that use empirical photosynthesis and chlorophyll fluorescence measurements from a limited number of ocean sites to estimate the productivity of the entire ocean. The open ocean presents numerous challenges to photosynthetic organisms. Physiological stresses imposed by a rapidly fluctuating light environment are exacerbated by oligotrophic nutrient conditions that limit the availability of iron, a nutrient required for maintenance and repair of the photosynthetic apparatus, and macronutrients, such as nitrogen and phosphorus, that are required for cell growth. Despite these challenges, picophytoplankton are remarkably well adapted to life in the open ocean. Recent estimates suggest that the dominant picocyanobacteria genera Prochlorococcus and Synechococcus are responsible for up to two thirds of primary production in the oceans or nearly one third of the total primary production on Earth (Field et al. 1998; Scanlan 2003). Picophytoplankton also comprise eukaryotes such as the Prasinophytes Ostreococcus and Micromonas. These organisms are located primarily in coastal areas where they can contribute up to 75% of total CO2 fixation (Fouilland et al. 2004; Worden et al. 2004). However, they are also present in the oligotrophic oceans where they have successfully colonized the deep euphotic zone (Campbell and Vaulot 1993; Dı́ez et al.