Chlamydomonas sp. UWO241 exhibits constitutively high cyclic electron flow and rewired metabolism under high salinity

ABSTRACT The Antarctic green alga Chlamydomonas sp. UWO241 (UWO241) was isolated from the deep photic zone of a permanently Antarctic ice-covered lake. Adaptation to permanent low temperatures, hypersalinity, and extreme shade has resulted in survival strategies in this halotolerant psychrophile. One of the most striking phenotypes of UWO241 is an altered photosystem I (PSI) organization and constitutive PSI cyclic electron flow (CEF). To date, little attention has been paid to CEF during long-term stress acclimation and the consequences of sustained CEF in UWO241 are not known. In this study, we combined photobiology, proteomics, and metabolomics to understand the underlying role of sustained CEF in high salinity stress acclimation. High salt-grown UWO241 exhibited increased thylakoid proton motive flux and an increased capacity for NPQ. A Bestrophin-like Cl- channel was identified in the whole cell proteomes and transcriptome of UWO241 which likely supports ion homeostasis during high transthylakoid pH. Under high salt, a significant proportion of the upregulated enzymes were associated with the Calvin Benson Bassham Cycle (CBB), secondary metabolite biosynthesis, and protein translation. Two key enzymes of the Shikimate pathway, DAHP synthase and chorismate synthase, were also upregulated, as well as indole-3-glycerol phosphate synthase, an enzyme involved in biosynthesis of L-tryptophan and indole acetic acid. In addition, several compatible solutes (glycerol, proline and sucrose) accumulated to high levels in high salt-grown UWO241 cultures. We suggest that UWO241 maintains constitutively high CEF with associated PSI-cytb6f supercomplex to support robust growth and strong photosynthetic capacity under a constant growth regime of low temperatures and high salinity.