Protection of photosystem II against UV-A and UV-B radiation in the cyanobacterium Plectonema boryanum: The role of growth temperature and growth irradiance

Photochemistry and Photobiology, Dec 2000 by Ivanov, Alexander G, Miskiewicz, Ewa, Clarke, Adrian K, Greenberg, Bruce M, Huner, Norman P A

Protection of Photosystem II Against UV-A and UV-13 Radiation in the Cyanobacterium Plectonema boryanum: The Role of Growth Temperature and Growth Irradiance(Para)

ABSTRACT

Plectonema boryanum UTEX 485 cells were grown at 29 deg C and 150 ;Lmol m-2 s-1 photosynthetically active radiation (PAR) and exposed to PAR combined with ultraviolet-A radiation (UV-A) at 15 deg C. This induced a timedependent inhibition of photosystem II (PSII) photochemistry measured as a decrease of the chlorophyll a fluorescence ratio, F,/Fm, to 50% after 2 h of UV-A treatment compared to nontreated control cells. Exposure of the same cells to PAR combined with UV-A ultravioletB radiation (UV-B) caused only a 30% inhibition of PSII photochemistry relative to nontreated cells. In contrast, UV-A and UV-A UV-B irradiation of cells cultured at 15 deg C and 150 pmol m-2 s-1 had minimal effects on the F,/Fm values. However, cells grown at 15 deg C and lower PAR irradiance (6 pmol m-2 s-') exhibited similar inhibition patterns of PSII photochemistry as control cells. The decreased sensitivity of PSH photochemistry of P. boryanum grown at 15 deg C and 150 N,mol m-2 s-1 to subsequent exposure to UV radiation relative to either control cells or cells grown at low temperature but low irradiance was correlated with the following: (1) a reduced efficiency of energy transfer to PSH reaction centers; (2) higher levels of a carotenoid tentatively identified as myxoxanthophyll; (3) the accumulation of scytonemin and mycosporine amino acids; and (4) the accumulation of ATP-dependent caseinolytic proteases. Thus, acclimation of P. boryanum at low temperature and moderate irradiance appears to confer significant resistance to UV-induced photoinhibition of PSII. The role of excitation pressure in the induction of this resistance to UV radiation is discussed.

INTRODUCTION

Recent studies have indicated that exposure to ultraviolet-B radiation (UV-B)t induced photodestruction of the major cyanobacterial light harvesting complex, the phycobilisome, and each of its constituent phycobiliproteins as well as linker polypeptides (1,2). This resulted in a reduced efficiency of energy transfer from the accessory pigments to the reaction center of photosystem II (PSII) (2). UV-B exposure of a number of freshwater and marine cyanobacteria also leads to the inhibition of PSII photochemical efficiency estimated in vivo by the room temperature chlorophyll (Chl) a fluorescence emission ratio, Fv/Fm (3), whole chain photosynthetic electron transport as well as 02 evolution (4). In addition, it has been reported that photosynthetic COZ fixation (4), nitrate uptake (5) and nitrogenase activity (6) were severely inhibited by UV-B treatment.

The major UV-B target sites on the acceptor-side of PSI in cyanobacteria include the depletion of the plastoquinone pool (7) as well as the degradation of the DI protein of PSH reaction center due to the cleavage of the second, transmembrane segment of the DI polypeptide (3,7). Alternatively, a donor-side mechanism for UV-B-induced damage to PSII involving the inhibition of the water-splitting complex has been proposed as the main cleavage site of the DI protein (7). Recently, Campbell et al. (3) reported that UV-B strongly regulates expression of psbA genes and leads to exchange of alternate PSII DI polypeptides in Synechococcus sp. PCC 7942 cells. The capability to exchange the DI: 1 form for the D1:2 form has been considered as one of the main mechanisms in developing resistance to UV-B-induced inhibition of photosynthesis (3).

In addition to this mechanism, cyanobacteria have developed a number of adaptive strategies to reduce the damaging effects of excessive UV radiation (8). Besides the accumulation of enzymes (9) and xanthophylls (10) to detoxify the highly reactive oxidants produced photochemically under UV radiation, the synthesis and accumulation of UV-absorbing compounds was suggested as an important mechanism preventing UV photodamage in cyanobacteria (11,12). It has been demonstrated that the accumulation of water soluble oligosaccharide-mycosporine amino acids (OS-MAA) with absorption maxima between 310 and 360 nm provides passive protection against UV-B and far-ultraviolet-A (UV-A) irradiation (12), while the lipid soluble scytonemin (Scy) localized in the cyanobacterial sheath with absorption maxima at 370 nm has been proposed to serve mainly as a UV-A sunscreen (11).

Variations in the UV-B/UV-A and UV-B/photosynthetically active radiation (PAR) ratios resulting from changes in the ozone layer in the upper atmosphere could have a significant biological impact on aquatic ecosystems (8). It has been suggested that changes in the UV-B/UV-A balance could affect some species more severely than others (13). The present study was performed to examine the impact of acclimation of the filamentous cyanobacterium, Plectonema boryanum UTEX 485, to various growth irradiance and temperatures on its susceptibility to PSII photoinhibition induced by UV-B irradiation in combination with UV-A as well as UV-A alone. We tested the hypothesis that acclimation of P. boryanum to low growth temperature induces increased resistance to UV-induced photoinhibition.