Paradoxical effects of temperature and solar irradiance on the photodegradation state of killed phytoplankton

Abstract

The aim of this paper was to study the effects of temperature and irradiance on the photodegradation state of killed phytoplankton cells. For this purpose, killed cells of the diatom Chaetoceros neogracilis RCC2022 were irradiated (photosynthetically active radiation) at 36 and 446 J · s(-1) · m(-2) (for the same cumulative dose of irradiation energy) and at two temperatures (7°C and 17°C). Analyses of specific lipid tracers (fatty acids and sterols) revealed that low temperatures and irradiances increased photooxidative damages of monounsaturated lipids (i.e., palmitoleic acid, cholesterol and campesterol). The high efficiency of type II photosensitized degradation processes was attributed to: (i) the relative preservation of the sensitizer (chlorophyll) at low irradiances allowing a longer production of singlet oxygen and (ii) the slow diffusion rate of singlet oxygen through membranes at low temperatures inducing more damages. Conversely, high temperatures and irradiances induced (i) a rapid degradation of the photosensitizer and a loss of singlet oxygen by diffusion outside the membranes (limiting type II photosensitized oxidation), and (ii) intense autoxidation processes degrading unsaturated cell lipids and oxidation products used as photodegradation tracers. Our results may explain the paradoxical relationship observed in situ between latitude and photodegradation state of phytoplankton cells.

Identification of di- and triterpenoid lipid tracers confirms the significant role of autoxidation in the degradation of terrestrial vascular plant material in the Canadian Arctic

“…This apparent paradox (i.e. increased photooxidation despite relatively low temperature and solar irradiance) has been attributed recently by Amiraux et al (2016) to: (i) the relative preservation of the sensitizer (chlorophyll) at low irradiance, which permits a longer production time for 1 O2, and (ii) the slower diffusion rate of 1 O2 through the cell membranes at low temperature (Ehrenberg et al, 1998), thereby favoring the intracellular involvement of type II photosensitized reactions.…”

Autoxidation as a major player in the fate of terrestrial particulate organic matter in seawater

“…It was evidenced that the role of photooxidation, averaging 10.3 ± 1.1% for sitosterol in the Rhône River between 2011 and 2013 [ Galeron et al ., ], was much more important in the Arctic, where it can reach 48.0 ± 2% [ Rontani et al ., ], than in temperate zones. This paradoxical enhancement of type II photooxidation processes in high‐latitude colder regions, receiving less solar irradiance, has recently been explained by a better conservation of photosensitizers and lower diffusion rates of singlet oxygen in biological membranes [ Amiraux et al ., ]. Together, these conditions favor a longer action time for photooxidation, causing extensive degradation and creating hydroperoxide‐rich suspended particulate matter.…”

Lipoxygenase-induced autoxidative degradation of terrestrial particulate organic matter in estuaries: A widespread process enhanced at high and low latitude

“…In order to explain this unexpected efficiency, we recently carried out in vitro incubations of the diatom Chaetoceros neogracilis RCC2022 at different temperature and irradiance values. Interestingly, the results allowed us to show that type II photosensitized oxidation in senescent phytoplanktonic cells is strongly favored at low temperature and low irradiance (Amiraux et al, 2016). This apparent paradox has been attributed to: (i) the relative preservation of the sensitizer (chlorophyll) at low irradiance, which permits a longer production time for singlet oxygen, and (ii) the slower diffusion rate of singlet oxygen through the cell membranes at low temperature (Ehrenberg et al, 1998), thereby favoring the intracellular involvement of type II photosensitized reactions.…”

“…The low photooxidation state of sitosterol in SPM from the river shows that this process is also limited on land in senescent terrestrial higher plants. As discussed above, such results might seem paradoxical in these highly irradiated regions (solar irradiance ranging from 100 to 250 W/m 2 in the Amazon Basin; Pinker and Laszlo, 1992), but recent findings have shown that both high temperature and high irradiance increase the diffusion rate of singlet oxygen outside cell membranes and quickly consume the photosensitizer (Amiraux et al, 2016). The conjunction of the short lifespan of the photosensitizer, coupled with the high diffusion rate of singlet oxygen, results in the involvement of a weakly damaging photooxidative process.…”

“…9). In tropical zones, photooxidation does not play a major role in the degradation of riverine SPM, for reasons discussed by Amiraux et al (2016). However, the higher temperature seems to favor autoxidation, which is clearly the main driver in SPM degradation within the Amazon River, along with biodegradation (Amon and Benner, 1996;Ward et al, 2013).…”