University of Groningen Can photoinhibition control phytoplankton abundance in deeply mixed water columns of the Southern Ocean? Alderkamp,

To study how natural Southern Ocean phytoplankton communities acclimate to rapid fluctuations in irradiance levels that result from deep wind-driven mixing of the upper water column, we measured their fluorescence properties (Fv : Fm, maximum quantum yield of photosystem II; and qN, non-photochemical quenching) and pigment composition. Values of Fv : Fm were low (, 0.46) and qN was high (. 0.67) throughout the upper mixed layer (UML). Short-term (20-min) exposure to incident surface irradiance strongly reduced Fv : Fm and recovery was slow under subsequent incubation at low irradiance. This suggests that phytoplankton cells are frequently photodamaged when mixed up to the surface from depth. Recovery of Fv : Fm was suppressed when lincomycin was added, inhibiting synthesis of the photosystem II reaction center D1 protein. This indicates that D1 protein repair is crucial in maintaining photosynthetic performance under fluctuating irradiance levels. Regions within the Antarctic Circumpolar Current (ACC) with a deep UML had lower depth-integrated phytoplankton biomass than regions close to the Antarctic continent with a shallow UML. Surprisingly, the depth-averaged light level within the UML in these latter regions was lower than in the ACC. Thus, it appears that photodamage incurred during the high irradiance portion of the vertical mixing cycle, rather than light limitation, controls phytoplankton growth in regions of the Southern Ocean with a deep UML. This concept represents a shift from the widely accepted paradigm that phytoplankton growth in the open Southern Ocean is limited by low levels of light or inadequate iron supply. The Southern Ocean (south of 44uS) is an important component of the global carbon cycle due to its large size and unique physical and chemical characteristics. Recent studies indicate that some regions of the Southern Ocean are a strong sink for anthropogenic CO2 (Arrigo et al. 2008; Gruber et al. 2009) and that its lower latitudes are important areas of anthropogenic CO2 storage (Sabine et al. 2004). In regions south of the Polar Front, major inorganic nutrients such as nitrate, phosphate, and silicate are seldom fully utilized, but low trace metal concentrations, especially of iron (Fe), limit phytoplankton growth in large areas of the Southern Ocean (Martin et al. 1990; Boyd et al. 2007), making it the largest of the three high nutrient– low chlorophyll (HNLC) regions of the global ocean. In addition, phytoplankton productivity is light limited in many areas of the Southern Ocean because weak water column stratification and strong winds create deep mixed layers, especially in the vicinity of the Antarctic Circumpolar Current (ACC; Mitchell et al. 1991; De Baar et al. 2005). Wind-induced vertical mixing imposes strong and rapid changes in the irradiance regime experienced by phytoplankton cells (Denman and Gargett 1983; Neale et al. 2003). This mixing reduces the total irradiance dose but periodically exposes phytoplankton to periods of excessive irradiance when residing near the surface. In response to low irradiance, algae maximize their light-harvesting capacity by increasing their photosynthetic pigment content and photosynthetic efficiency (Falkowski and La Roche 1991). In contrast, at saturating irradiance, Calvin cycle activity increases at the expense of light-harvesting pigments (Falkowski and La Roche 1991). Irradiance exceeding photosynthetic requirements often causes photoinhibition and viability loss (Van de Poll et al. 2006). Initially, photoinhibition is associated with a decrease in functional photosystem II (PS II) reaction centers, which decreases photosynthetic activity. Progressive reduction of functional PS II limits the reducing power of antioxidant metabolism, which leads to uncontrolled formation of reactive oxygen species and eventually to loss of viability (Van de Poll et al. 2006, 2007). Photoinhibition is reversible, but recovery requires synthesis of damaged PS II components, such as the PS II reaction center D1 protein that is involved in a complex and metabolically expensive damage–repair cycle (Aro et al. 1993; Hazzard et al. 1997). An important photoprotection mechanism is the thermal dissipation of excess energy by xanthophyll cycle pigments in their de-epoxidated state. The xanthophyll cycle of algae comprises the enzymatic conversion of carotenoids such as violaxanthin to antheraxanthin and zeaxanthin in green algae, and diadinoxanthin to diatoxanthin in diatoms (Olaizola et al. 1994; Van Leeuwe et al. 2005). Energy dissipation can be quantified in vivo by estimating nonphotochemical quenching (NPQ) of chlorophyll a (Chl a) fluorescence (Demmig et al. 1987; Olaizola et al. 1994). NPQ is a result of both fast-acting energy-dependent quenching (qE), which involves the thermal dissipation of excess light-energy by xanthophyll cycle pigments, and slowly relaxing photoinhibitory quenching (qI), which has been attributed to damage or down-regulation of PS II reaction centers (Baker and Horton 1987; Oquist et al. * Corresponding author: Alderkamp@Stanford.edu Limnol. Oceanogr., 55(3), 2010, 1248–1264 E 2010, by the American Society of Limnology and Oceanography, Inc. doi:10.4319/lo.2010. 55.3. 1248