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The Antarctic psychrophiles Chlamydomonas spp. UWO241 and ICE-MDV exhibit differential restructuring of photosystem I in response to iron

Abstract

Chlamydomonas sp. UWO241 is a psychrophilic alga isolated from the deep photic zone of a perennially ice-covered Antarctic lake (east lobe Lake Bonney, ELB). Past studies have shown that C. sp. UWO241 exhibits constitutive downregulation of photosystem I (PSI) and high rates of PSI-associated cyclic electron flow (CEF). Iron levels in ELB are in the nanomolar range leading us to hypothesize that the unusual PSI phenotype of C. sp. UWO241 could be a response to chronic Fe-deficiency. We studied the impact of Fe availability in C. sp. UWO241, a mesophile, C. reinhardtii SAG11-32c, as well as a psychrophile isolated from the shallow photic zone of ELB, Chlamydomonas sp. ICE-MDV. Under Fe-deficiency, PsaA abundance and levels of photooxidizable P700 (ΔA820/A820) were reduced in both psychrophiles relative to the mesophile. Upon increasing Fe, C. sp. ICE-MDV and C. reinhardtii exhibited restoration of PSI function, while C. sp. UWO241 exhibited only moderate changes in PSI activity and lacked almost all LHCI proteins. Relative to Fe-excess conditions (200 µM Fe2+), C. sp. UWO241 grown in 18 µM Fe2+ exhibited downregulation of light harvesting and photosystem core proteins, as well as upregulation of a bestrophin-like anion channel protein and two CEF-associated proteins (NdsS, PGL1). Key enzymes of starch synthesis and shikimate biosynthesis were also upregulated. We conclude that in response to variable Fe availability, the psychrophile C. sp. UWO241 exhibits physiological plasticity which includes restructuring of the photochemical apparatus, increased PSI-associated CEF, and shifts in downstream carbon metabolism toward storage carbon and secondary stress metabolites.

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Abbreviations

Δψ:

Electric field gradient

A820 :

P700 + absorbance at 820 nm

Δ/A820 :

Proportion of photooxidizable P700

AL:

Actinic light

CEF:

Cyclic electron flow

Chl a:

Chlorophyll a

e /P700:

Intersystem electron pool size per PSI reaction center

ELB:

East lobe Lake Bonney

F 685 :

77 K fluorescence maximum, 685 nm

F 715 :

77 K fluorescence maximum, 715 nm

FR:

Far red

F V/F M :

Maximum photosynthetic efficiency

HNLC:

High nutrient, low chlorophyll

LHCI:

Light harvesting complex I

LHCII:

Light harvesting complex II

MT/ST:

Multiple turn-over/single turn-over actinic light flash

NPQ:

Nonphotochemical quenching

P700+:

Photochemical reaction center of photosystem I, oxidized form

pmf:

Proton motive force

PSI:

Photosystem I

PSII:

Photosystem II

qP:

Photochemical quenching

t 1/2 red :

Half-time for re-reduction of P700+

Y(PSI):

Effective quantum yield of PSI

Y(PSII):

Effective quantum yield of PSII

Y(NA):

Energy loss due to acceptor side limitation

Y(ND):

Energy loss due to donor side limitation

Y(NO):

Energy dissipation from nonregulated processes

Y(NPQ):

Nonphotochemical energy dissipation from antenna quenching

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Acknowledgements

The authors thank Prof. Joshua S. Yuan at Texas A&M University for helping us obtain the preliminary proteomics data for C. sp. UWO241.

Funding

GC, IK, AT, WL, XW and RM-K were supported by NSF Grants OPP-1056396 and -1637708, DOE Grant DE-SC0019138. JP was supported by NSF Grant PLR-1637708.

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Correspondence to Rachael Morgan-Kiss.

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Cook, G., Teufel, A., Kalra, I. et al. The Antarctic psychrophiles Chlamydomonas spp. UWO241 and ICE-MDV exhibit differential restructuring of photosystem I in response to iron. Photosynth Res 141, 209–228 (2019). https://doi.org/10.1007/s11120-019-00621-0

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Keywords

  • Antarctica
  • Cyclic electron flow
  • Iron
  • Photosystem I
  • Psychrophile