High salt-induced PSI-supercomplex is associated with high CEF and attenuation of state transitions

Abstract

While PSI-driven cyclic electron flow (CEF) and assembly of thylakoid supercomplexes have been described in model organisms like Chlamydomonas reinhardtii, open questions remain regarding their contributions to survival under long-term stress. The Antarctic halophyte, C. priscuii UWO241 (UWO241), possesses constitutive high CEF rates and a stable PSI-supercomplex as a consequence of adaptation to permanent low temperatures and high salinity. To understand whether CEF represents a broader acclimation strategy to short- and long-term stress, we compared high salt acclimation between the halotolerant UWO241, the salt-sensitive model, C. reinhardtii, and a moderately halotolerant Antarctic green alga, C. sp. ICE-MDV (ICE-MDV). CEF was activated under high salt and associated with increased non-photochemical quenching in all three Chlamydomonas species. Furthermore, high salt-acclimated cells of either strain formed a PSI-supercomplex, while state transition capacity was attenuated. How the CEF-associated PSI-supercomplex interferes with state transition response is not yet known. We present a model for interaction between PSI-supercomplex formation, state transitions, and the important role of CEF for survival during long-term exposure to high salt.

Sentinel protist taxa of the McMurdo Dry Valley lakes, Antarctica: a review

“…Chlamydomonas sp. ICE-MDV grows faster than C. priscuii under nonstress conditions and is capable of state transitions (Figure 8A), but exhibits significantly lower salinity tolerance (≤ 500 mM NaCl) (Kalra et al, 2023) compared to C. priscuii (up to 1200 mM NaCl; Pocock et al, 2011). Overall, we conclude that Chlamydomonas sp.…”

“…priscuii has lost the rapid response mechanism of state transitions (Morgan-Kiss et al, 2002b); however, it possess a high capacity for photoprotection and oxidative stress detoxification and grows remarkably well under light conditions which are >10-fold higher than native light levels (Stahl-Rommel et al, 2022). Adaptation to the permanently high salinity environment may have contributed to the loss in capacity for state transitions: C. priscuii assembles a pigment-protein super complex which supports sustained rates of an alternative electron transport pathway around photosystem I (Kalra et al, 2020(Kalra et al, , 2023. Last, Hüner and colleagues reported that C. priscuii forms immobile, multicellular palmelloid structures which are functionally distinct from single cells and exhibit higher photoprotection from short-term high light stress (Szyszka-Mroz et al, 2022;Hüner et al, 2023).…”

“…Labcontrolled experiments have also shown that Chlamydomonas sp. ICE-MDV has greater metabolic plasticity relative to C. priscuii, including some capacity for state transitions (Figure 8A; Kalra et al, 2023). Chlamydomonas sp.…”

“…Unlike marine and freshwater systems which are geographically separated, salinity is a major physicochemical factor with strong gradients within the MDV lakes. As studies on MDV algal isolates have shown, there are protist lineages within the same lake which possess different salinity tolerances and physiology (Kalra et al, 2020, Kalra et al, 2023. Identifying additional protist lineages with varying salt sensitivity could make them valuable sentinels of climate change.…”

Light quality affects chlorophyll biosynthesis and photosynthetic performance in Antarctic Chlamydomonas

“…In contrast, ICE-MDV displays a more flexible physiology and a photosynthetic apparatus similar to its non-extremophilic relatives. ICE-MDV has retained the capacity for state transitions, PSI restructuring and phototaxis (Cook et al 2019;Kalra et al 2023;Poirier et al 2023), and can induce protective mechanisms under temperature stress (Cvetkovska et al 2022b). Its plastid genome does encode for DPOR, giving this alga the flexibility of both light dependent and independent chlorophyll biosynthesis (Smith et al 2019).…”