DOE Basic Energy Sciences (DE )Collaborative Project: Regulation of Sustained Cyclic Electron Flow (CEF) in the Photopsychrophile Chlamydomonas sp. UWO241
Investigators: Xin Wang (Miami University), Ru Zhang (Donald Danforth Plant Science Center), Petra Fromme (Biodesign Institute, Arizona State University)
Participants: Isha Kalra (PhD in progress), Abby Mills (MSc in progress), Susanna D'Silva (undergrad), Isaiah Jacques (undergrad)
Photosynthesis is vital for agricultural yields and has important applications in biofuel production. Photosynthesis generates energy through a process called linear electron transport (LEF) using two pigment-protein complexes, Photosystem I (PSI) and Photosystem II (PSII). Imbalances between energy production by photosynthesis and consumption by carbon metabolism impacts plant health and therefore crop productivity. To achieve optimal energy balance, plants employ several alternative electron transport pathways, including cyclic electron flow (CEF). Unlike LEF, CEF uses PSI only and generates one type of energy carrier, ATP. CEF also prevents photo-damage during environmental stress. Increased CEF activity has been frequently reported under several stressful conditions, suggesting an important role in plant protection against environmental stress. Despite the importance of CEF in photosynthesis, a precise mechanism for CEF has not been fully described. Most previous research has focused on CEF in a small number of model plant and algal species exposed to short-term stress, ignoring the role of CEF under long-term stress conditions. In this project, we will use an Antarctic alga, Chlamydomonas sp. UWO241, as a model to advance our understanding of the mechanism of CEF. Unlike other model plants and algae, UWO241 has strong CEF activity under steady growth conditions. Sustained CEF in UWO241 is related to long-term adaptation to permanent low temperature and high salinity, and correlates with the formation of a novel PSI protein supercomplex. In this research, we will use a multidisciplinary approach to accomplish three specific aims: (1) determine why UWO241 utilizes high CEF; (2) describe the mechanism(s) which support sustained CEF in UWO241; (3) investigate whether a model alga, C. reinhardtii, uses UWO-like supercomplexes to support sustained CEF to survive long-term stress. This project supports the mission of DOE Basic Energy Sciences Program / Photosynthetic Systems program because it investigates an important photosynthetic electron transport pathway essential for plant survival under variable environments. The knowledge gained from this project will help engineer more efficient and robust photosynthesis in field conditions to improve agriculture production and provide engineering targets for artificial photosynthesis.
Supercomplex formation in UWO241 and C. reinhardtii under high salinity and state 2 respectively. Fractionation of major thylakoid chlorophyll-protein complexes from UWO241 by sucrose density ultracentrifugation from low salt (LS) - and high salt (HS)- grown cultures (A, B). Fractionation of major thylakoid chlorophyll-protein complexes from C. reinhardtii exposed to State 1 and State 2 conditions (C, D). Cultures of C. reinhardtii were grown under control conditions (20°C/100 umol) and either dark adapted for 10 minutes (State 1, A) or incubated under anaerobic conditions for 30 minutes (State 2, B).
A restructured photosynthetic apparatus supports rewiring of central metabolism in C. sp. UWO241. The photosynthetic apparatus of UWO241 is assembled to promoted high rates of CEF which is sustained by formation of a PSI supercomplex (A). CEF supports photoprotection of PSII and PSI and provides additional ATP for downstream metabolism. High ATP is consumed, in part, by the CBB cycle as well as an upregulated shikimate pathway and carbon storage pathways (starch, glycerol) (B). Model is based on data presented here and other studies (Cook et al., 2019; Szyszka-Mroz et al., 2015; 2019)
Publications:
Cook G.P.**, Teufel A.G.**, Kalra I.**, Li W.**, Priscu J.P., Wang X., Morgan-Kiss R.M. (2019) The Antarctic psychrophiles Chlamydomonas spp. UWO241 and ICE-MDV exhibit differential restructuring of Photosystem I in response to iron. Photosynthesis Research. 141:209-228
Kalra I.**, Wang X., Jeong J., McHargue W., Cvetkovska M., Zhang R., Huner N., Yuan J., Morgan-Kiss R. (2019) The Antarctic Chlamydomonas sp. UWO241 exhibits constitutively high cyclic electron flow and rewired metabolism under permanent low temperature and high salinity stress. In Review.
Cook G.P.**, Teufel A.G.**, Kalra I.**, Li W.**, Priscu J.P., Wang X., Morgan-Kiss R.M. (2019) The Antarctic psychrophiles Chlamydomonas spp. UWO241 and ICE-MDV exhibit differential restructuring of Photosystem I in response to iron. Photosynthesis Research. 141:209-228
Kalra I.**, Wang X., Jeong J., McHargue W., Cvetkovska M., Zhang R., Huner N., Yuan J., Morgan-Kiss R. (2019) The Antarctic Chlamydomonas sp. UWO241 exhibits constitutively high cyclic electron flow and rewired metabolism under permanent low temperature and high salinity stress. In Review.