Diverse strategies of O2 usage for preventing photo-oxidative damage under CO2 limitation during algal photosynthesis

Abstract

Photosynthesis produces chemical energy from photon energy in the photosynthetic electron transport and assimilates CO2 using the chemical energy. Thus, CO2 limitation causes an accumulation of excess energy, resulting in reactive oxygen species (ROS) which can cause oxidative damage to cells. O2 can be used as an alternative energy sink when oxygenic phototrophs are exposed to high light. Here, we examined the responses to CO2 limitation and O2 dependency of two secondary algae, Euglena gracilis and Phaeodactylum tricornutum. In E. gracilis, approximately half of the relative electron transport rate (ETR) of CO2-saturated photosynthesis was maintained and was uncoupled from photosynthesis under CO2 limitation. The ETR showed biphasic dependencies on O2 at high and low O2 concentrations. Conversely, in P. tricornutum, most relative ETR decreased in parallel with the photosynthetic O2 evolution rate in response to CO2 limitation. Instead, non-photochemical quenching was strongly activated under CO2 limitation in P. tricornutum. The results indicate that these secondary algae adopt different strategies to acclimatize to CO2 limitation, and that both strategies differ from those utilized by cyanobacteria and green algae. We summarize the diversity of strategies for prevention of photo-oxidative damage under CO2 limitation in cyanobacterial and algal photosynthesis.

The Liverwort, Marchantia, Drives Alternative Electron Flow Using a Flavodiiron Protein to Protect PSI

“…PCC 7002), under suppressed photosynthesis conditions equilibrated with air, AEF is driven by FLVs, not by photorespiration (Hayashi et al, 2014;Shimakawa et al, 2015Shimakawa et al, , 2016bShaku et al, 2016). Furthermore, some eukaryotic algae, including the green alga Chlamydomonas reinhardtii and the diatom Phaeodactylum tricornutum, do not utilize photorespiration as the main alternative electron sink under suppressed photosynthesis conditions (Shimakawa et al, 2016a(Shimakawa et al, , 2017. These facts suggest that oxygenic phototrophs that reside in or are exposed to aqueous environments use FLV in AEF to oxidize P700 in PSI.…”

Land plants drive photorespiration as higher electron‐sink: comparative study of post‐illumination transient O2‐uptake rates from liverworts to angiosperms through ferns and gymnosperms

“…In aqueous environments, their gas‐diffusion efficiencies are 10 −4 lower, compared with the atmosphere. Almost all algae can use O 2 at lower concentration for their electron sinks under CO 2 limitation (Shimakawa et al ). Algal O 2 ‐dependent electron flows show the K M for O 2 below 10 µ M .…”

“…In aqueous environments, their gas-diffusion efficiencies are 10 −4 lower, compared with the atmosphere. Almost all algae can use O 2 at lower concentration for their electron sinks under CO 2 limitation (Shimakawa et al 2017a (Shimakawa et al 2015). On the other hand, the K M for O 2 in the RuBP-oxygenation reaction catalyzed by Rubisco, which is the primary reaction and limits the photorespiration rate, exceeds 300 μM (von Caemmerer 2000).…”

“…Badger et al () showed O 2 ‐dependent electron flows in algae including green algae, brown algae and diatoms. These algal O 2 ‐dependent electron fluxes were larger than that in photorespiration, and have a high affinity for O 2 , comparable to FLV proteins, indicating that FLV mainly drives O 2 ‐dependent electron flow in these algae (Shimakawa et al ).…”

Changing frequency of fluctuating light reveals the molecular mechanism for P700 oxidation in plant leaves

“…In C 3 plants, the flux of electrons to O 2 is mainly driven by photorespiration (Hanawa et al., ; Sejima et al., ; Wiese, Shi, & Heber, ). Even although photorespiration is the largest alternative electron sink in land plants (except for C 4 plants; Hanawa et al., ), it is not used as the main alternative electron sink by many prokaryotic and eukaryotic algae (Hayashi et al., ; Shimakawa et al., ; Shimakawa, Akimoto et al., ; Shimakawa, Matsuda et al., ). Cyanobacteria, which are the ancestors of chloroplasts in land plants, use flavodiiron proteins (FLV) to mediate electron flow to O 2 , instead of photorespiration (Helman, Barkan, Eisenstadt, Luz, & Kaplan, ; Helman et al., ; Shimakawa et al., ), and to alleviate photo‐oxidative damage (Allahverdiyeva et al., ; Shimakawa, Shaku et al., ; Zhang, Allahverdiyeva, Eisenhut, & Aro, ).…”