Cold-Adapted Protein Kinases and Thylakoid Remodeling Impact Energy Distribution in an Antarctic Psychrophile

Szyszka‐Mroz, Beth; Cvetkovska, Marina; Ivanov, Alexander G.; Smith, David Roy; Possmayer, Marc; Maxwell, Denis P.; Hüner, Norman P. A.

doi:10.1104/pp.19.00411

Cited by 24 publications

(27 citation statements)

References 73 publications

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“…Constitutively high rates of CEF in UWO 241 are associated with a general reorganization of PSI and PSII complexes (Szyszka-Mroz et al, 2019) and the formation of a PSI-cyt b 6 f supercomplex (Szyszka-Mroz et al, 2015). In this study, following optimization of thylakoid protein complex solubilization by substituting b-DDM with a-DDM, the vast majority of PSI shifted from free PSI in the LS-grown cultures to association with the UWO 241-SC in the HS-grown cultures.…”

Section: Discussionmentioning

confidence: 71%

“…Despite more than two decades of study on UWO 241, there are many questions that remain unanswered regarding how this enigmatic organism thrives in an environment inhospitable to most of life on Earth. Recent articles have added to the breadth of knowledge on the photosynthetic apparatus, including a cold-adapted ferredoxin isoform (Cvetkovska et al, 2018) and a thylakoid kinase exhibiting temperature-dependent phosphorylation patterns (Szyszka-Mroz et al, 2019). Here, we extend our understanding of long-term photosynthetic adaptation to permanent cold and hypersalinity by proposing a model for sustained PSI-CEF that supports a robust growth and photosynthesis (Fig.…”

Section: Discussionmentioning

confidence: 71%

“…4). Lastly, a recent study reported that UWO 241 transfers light energy from PSII to PSI via constitutive energy spillover through an undescribed mechanism (Szyszka-Mroz et al, 2019). Thus, UWO 241 favors down-regulated LHCI and constitutive energy spillover in response to its extreme habitat, most likely the natural light environment of extreme shade enriched in blue wavelengths (Neale and Priscu, 1995).…”

Section: Discussionmentioning

confidence: 99%

“…Morgan-Kiss et al (2002b) reported that UWO 241 lacks phosphorylation of LHCII and state transitions. Recently, Szyszka-Mroz et al (2019) showed that UWO 241 exhibits some LHCII phosphorylation and cold-adapted forms of the thylakoid protein kinases Stt7 and Stl1. They suggested that UWO 241 may rely on energy spillover between PSII and PSI rather than state transitions (Szyszka-Mroz et al, 2019).…”

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confidence: 99%

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Chlamydomonas sp. UWO 241 Exhibits High Cyclic Electron Flow and Rewired Metabolism under High Salinity

et al. 2020

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The Antarctic green alga Chlamydomonas sp. UWO 241 (UWO 241) is adapted to permanent low temperatures, hypersalinity, and extreme shade. One of the most striking phenotypes of UWO 241 is an altered 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 UWO 241 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 UWO 241 exhibited increased thylakoid proton motive flux and an increased capacity for nonphotochemical quenching. Under high salt, a significant proportion of the upregulated enzymes were associated with the Calvin-Benson-Bassham cycle, carbon storage metabolism, and protein translation. Two key enzymes of the shikimate pathway, 3-deoxy-D-arabinoheptulosonate 7-phosphate synthase and chorismate synthase, were also up-regulated, as well as indole-3-glycerol phosphate synthase, an enzyme involved in the biosynthesis of L-Trp and indole acetic acid. In addition, several compatible solutes (glycerol, Pro, and Suc) accumulated to high levels in high salt-grown UWO 241 cultures. We suggest that UWO 241 maintains constitutively high CEF through the associated PSI-cytochrome b 6 f supercomplex to support robust growth and strong photosynthetic capacity under a constant growth regime of low temperatures and high salinity.

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Section: Discussionmentioning

confidence: 71%

Section: Discussionmentioning

confidence: 71%

Section: Discussionmentioning

confidence: 99%

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confidence: 99%

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Chlamydomonas sp. UWO 241 Exhibits High Cyclic Electron Flow and Rewired Metabolism under High Salinity

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“…2010;Rochaix, 2014). In contrast to C. reinhardtii , Stt7 in UWO241 has higher LHCII-phosphorylation activity at 8ºC than at 23ºC, which appears to reflect the reorganization of the photosynthetic apparatus required for energy spillover (Szyszka-Mroz et al 2019). Thus, these two key photosynthetic proteins appear to have evolved to optimize photosynthetic light harvesting, energy transfer, and carbon fixation at low temperatures at the expense of lower activities at moderate and high temperatures.…”

Section: Introductionmentioning

confidence: 98%

Constitutively Up-regulated Carbon Metabolism is an Adaptation to Low Temperature in the Antarctic Psychrophile Chlamydomonas sp. UWO241

Cvetkovska

Szyszka‐Mroz

Malczewski

et al. 2021

Preprint

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The Antarctic alga Chlamydomonas sp. UWO241 is an obligate psychrophile that thrives in the cold but is unable to survive at moderate, seemingly innocuous temperatures. We dissect the responses of UWO241 to temperature stress using global metabolomic approaches. UWO241 exhibits slow growth at 4°C, a temperature closest to its natural habitat, and faster growth at higher temperatures of 10-15°C. We demonstrate that the slower growth-rate characteristic of UWO241 at 4⁰C is not necessarily a hallmark of stress. UWO241 constitutively accumulates high levels of protective metabolites including soluble sugars, polyamines and antioxidants at a range of steady-state temperatures. In contrast, the mesophile Chlamydomonas reinhardtii accumulates these metabolites only during cold stress. Despite low growth rates, 4°C-grown UWO241 cultures had a higher capacity to respond to heat stress (24°C) and accumulated increased amounts of antioxidants, lipids and soluble sugars, when compared to cultures grown at 10-15°C. We conclude that the slower growth rate and the unique psychrophilic physiological characteristic of UWO241 grown at 4⁰C result in a permanently re-routed steady-state metabolism, which contributes to its increased resistance to heat stress. Our work adds to the growing body of research on temperature stress in psychrophiles, many of which are threatened by climate change.

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Exploring Regulatory Roles of Plant Thylakoid-Bound Proteins Involved in Abiotic Stress Responses

Billah,

Aktar,

Sikder

et al. 2024

J Plant Growth Regul

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Cold-Adapted Protein Kinases and Thylakoid Remodeling Impact Energy Distribution in an Antarctic Psychrophile

Cited by 24 publications

References 73 publications

Chlamydomonas sp. UWO 241 Exhibits High Cyclic Electron Flow and Rewired Metabolism under High Salinity

Chlamydomonas sp. UWO 241 Exhibits High Cyclic Electron Flow and Rewired Metabolism under High Salinity

Constitutively Up-regulated Carbon Metabolism is an Adaptation to Low Temperature in the Antarctic Psychrophile Chlamydomonas sp. UWO241

Exploring Regulatory Roles of Plant Thylakoid-Bound Proteins Involved in Abiotic Stress Responses

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