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

  • Greg Cook
  • Amber Teufel
  • Isha Kalra
  • Wei Li
  • Xin Wang
  • John Priscu
  • Rachael Morgan-KissEmail author
Original Article

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.

Keywords

Antarctica Cyclic electron flow Iron Photosystem I Psychrophile 

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

F685

77 K fluorescence maximum, 685 nm

F715

77 K fluorescence maximum, 715 nm

FR

Far red

FV/FM

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

t1/2red

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

Notes

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.

Compliance with ethical standards

Conflict of interest

The authors declare that they have no conflicts of interest.

Supplementary material

11120_2019_621_MOESM1_ESM.docx (3.3 mb)
Supplementary material 1 (DOCX 3407 KB)

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© Springer Nature B.V. 2019

Authors and Affiliations

  1. 1.Department of MicrobiologyMiami UniversityOxfordUSA
  2. 2.Land Resources and Environmental SciencesMontana State UniversityBozemanUSA

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