Functional flexibility of cyanobacterial light harvesting phycobilisomes enable acclimation to the complex light regime of mixing marine water columns

Abstract

The light environment in a mixing water column is arguably the most erratic condition under which photosynthesis functions. Shifts in light intensity, by an order of magnitude, can occur over the time scale of hours. In marine Synechococcus, light is harvested by massive, membrane attached, phycobilisome chromophore‐protein complexes (PBS). We examined the ability of a phycobilisome‐containing marine Synechococcus strain (WH8102) to acclimate to illumination perturbations on this scale. Although changes in pigment composition occurred gradually over the course of days, we did observe significant and reversible changes in the pigment's fluorescence emission spectra on a time scale of hours. Upon transition to ten‐fold higher intensities, we observed a decrease in the energy transferred to Photosystem II. At the same time, the spectral composition of PBS fluorescence emission shifted. Unlike fluorescence quenching mechanisms, this phenomenon resulted in increased fluorescence intensities. These data suggest a mechanism by which marine Synechococcus WH8102 detaches hexamers from the phycobilisome structure. The fluorescence yield of these uncoupled hexamers is high. The detachment process does not require protein synthesis as opposed to reattachment. Hence, the most likely process would be the degradation and resynthesis of labile PBS linker proteins. Experiments with additional species yielded similar results, suggesting that this novel mechanism might be broadly used among PBS‐containing organisms.

Multiparameter-based photosynthetic state transitions of single phytoplankton cells

“…The data observed here, on a single cell basis, exhibits a similar trend to the previously-reported bulk spectroscopic parameters of light jump experiments ( 31 ). Previous experiments, however, could not have resolved the distinct fluorescence-based cell-state transitions that we report here, due to ensemble averaging over multiple unsynchronized cells.…”

“…WH8102 indicates that the acclimation of cyanobacteria to light intensity perturbations involves a choice that occurs independently for each cell. The nonradiative excitation energy transfer-sensitized emission observed as positive values in the 𝝉 𝟒𝟖𝟖 𝒄𝒉𝒍 − 𝝉 𝟔𝟒𝟐 𝒄𝒉𝒍 parameter, combined with the increase in PE fluorescence lifetime values, further indicates that the transition is a result of PE decoupling, in whole or in part from the PBS core (31,32), which drastically reduces the rate of nonradiative excitation energy transfer. Therefore, this decoupling must be tied with a signal transduction mechanism that coordinates rapid decoupling in many photosynthetic systems across vast regions of the cell.…”

“…accumulation of “closed” photosystems) which, according to eq. 5, would result in longer fluorescence lifetimes, or (2) PE decoupling, in whole or in part from the PBS core (38, 39), which drastically reduces the rate of EET. Considering that cells were dark adapted for 30 minutes in the flow path before detection, the second option should hold true.…”