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Cyclic electron flow (CEF) and ascorbate pathway activity provide constitutive photoprotection for the photopsychrophile, Chlamydomonas sp. UWO 241 (renamed Chlamydomonas priscuii)

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Abstract

Under environmental stress, plants and algae employ a variety of strategies to protect the photosynthetic apparatus and maintain photostasis. To date, most studies on stress acclimation have focused on model organisms which possess limited to no tolerance to stressful extremes. We studied the ability of the Antarctic alga Chlamydomonas sp. UWO 241 (UWO 241) to acclimate to low temperature, high salinity or high light. UWO 241 maintained robust growth and photosynthetic activity at levels of temperature (2 °C) and salinity (700 mM NaCl) which were nonpermissive for a mesophilic sister species, Chlamydomonas raudensis SAG 49.72 (SAG 49.72). Acclimation in the mesophile involved classic mechanisms, including downregulation of light harvesting and shifts in excitation energy between photosystem I and II. In contrast, UWO 241 exhibited high rates of PSI-driven cyclic electron flow (CEF) and a larger capacity for nonphotochemical quenching (NPQ). Furthermore, UWO 241 exhibited constitutively high activity of two key ascorbate cycle enzymes, ascorbate peroxidase and glutathione reductase and maintained a large ascorbate pool. These results matched the ability of the psychrophile to maintain low ROS under short-term photoinhibition conditions. We conclude that tight control over photostasis and ROS levels are essential for photosynthetic life to flourish in a native habitat of permanent photooxidative stress. We propose to rename this organism Chlamydomonas priscuii.

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Availability of data and material

The data supporting the findings of this study are available from the corresponding author (RMK) upon request.

Code availability

Not applicable.

Abbreviations

A820 :

Absorbance at 820 nm

ΦPSII:

Yield of photosystem II

APX:

Ascorbate peroxidase

AsA-GSH:

Ascorbate–glutathione pathway

C:

Control

CAT:

Catalase

CBB:

Calvin Benson Bassham

CEF:

Cyclic electron flow

FR:

Far red

F V/F M :

Maximum photosynthetic efficiency of photosystem II

GR:

Glutathione reductase

H2DCFDA:

2′,7′-Dichlorodihydrofluorescein diacetate

HL:

High light

HS:

High salt

LHCI:

Light harvesting complex I

LHCII:

Light harvesting complex II

LHCSR:

Light harvesting complex stress related protein

LT:

Low temperature

qL:

Photochemical quenching

MDHAR:

Dehydroascorbate reductase

NBT:

Nitroblue tetrazolium

NPQ:

Nonphotochemical quenching

PGR5:

Proton gradient regulation 5 protein

PGRL1:

PGR5-like protein 1

pmf:

Proton motive force

PQ:

Plastoquinone

PSI:

Photosystem I

PSII:

Photosystem II

ROS:

Reactive oxygen species

RT-qPCR:

Real time quantitative PCR

SOD:

Super oxide dismutase

t ½ red :

Half-time for P700 re-reduction

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Acknowledgements

The authors thank Prof. John C. Priscu (Montana State University) for isolation and donation of the algal strain Chlamydomonas sp. UWO 241 (originally named Chlamydomonas subcaudata) from Lake Bonney, McMurdo Dry Valleys, Antarctica. RMK, SS-R, and MH were supported by the National Science Foundation, Office of Polar Programs under Award #OPP-1056396 (growth physiology, photoinhibition, antioxidant measurements). IK, SD and DP were supported by the U.S. Department of Energy (DOE), Office of Science, Basic Energy Sciences (BES) under award #DE-SC0019138 (PSI, CEF measurements). MC was supported by a National Sciences and Engineering Research Council of Canada (NSERC) Discovery Grant RGPIN-2019-05763 and University of Ottawa start-up funding (genome screening).

Funding

RMK, SS-R, and MH were supported by the National Science Foundation, Office of Polar Programs under Award #OPP-1056396 (growth physiology, photoinhibition, antioxidant measurements). IK, SD and DP were supported by the U.S. Department of Energy (DOE), Office of Science, Basic Energy Sciences (BES) under Award #DE-SC0019138 (PSI, CEF, H2O2 measurements). MC is supported by a National Sciences and Engineering Research Council of Canada (NSERC) Discovery Grant RGPIN-2019–05763 and University of Ottawa start-up funding (genome screening).

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  1. Sarah Stahl-Rommel

    Present address: JES Tech, Houston, TX, 77058, USA

Authors and Affiliations

  1. Department of Microbiology, Miami University, Oxford, OH, 45045, USA

    Sarah Stahl-Rommel, Isha Kalra, Susanna D’Silva, Mark M. Hahn, Devon Popson & Rachael M. Morgan-Kiss

  2. Department of Biology, University of Ottawa, Ottawa, ON, K1N 6N5, Canada

    Marina Cvetkovska

  3. Department of Microbiology, Miami University, 700 E High St., 212 Pearson Hall, Oxford, OH, 45056, USA

    Rachael M. Morgan-Kiss

Authors
  1. Sarah Stahl-Rommel
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  2. Isha Kalra
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  5. Devon Popson
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Contributions

SS-R and RMK conceptualized the research; SS-R, SD, IK, MH, DP, and MC performed the investigations; SS-R, RMK, and MH developed the methodology; SS-R, RMK and MC performed data curation; RMK provided project administration; RMK and MC helped with funding acquisition; SS-R and RMK wrote the original draft of the manuscript; SD, IK, MH, and MC reviewed and edited the manuscript.

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Correspondence to Rachael M. Morgan-Kiss.

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Stahl-Rommel, S., Kalra, I., D’Silva, S. et al. Cyclic electron flow (CEF) and ascorbate pathway activity provide constitutive photoprotection for the photopsychrophile, Chlamydomonas sp. UWO 241 (renamed Chlamydomonas priscuii). Photosynth Res 151, 235–250 (2022). https://doi.org/10.1007/s11120-021-00877-5

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