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Critical role of oxygen photoreduction downstream of PSI in Symbiodinium: photoprotection, energetic adjustement and ROS production

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Pierre Cardol Research Associate Belgian funds for research

(F.R.S.-FNRS)

Genetics and Physiology of microalgae

Prof. C. Remacle University of Liège

Botany Institute Belgium

EPC6, London, august 25th 2015, Symbiodinium session

Critical role of oxygen photoreduction

downstream of photosystem I :

photoprotection, energetic adjustment and ROS

production in Symbiodinium

(2)

Centre Scientifique de Monaco C. Ferrier-Pagès

E. Béraud

EPC6, London, august 25th 2015, Symbiodinium session

University of Liège S. Roberty (Poster 2 in session 6) Nicolas Berne F. Franck C. Remacle J.C. Plumier B. Bailleul F. Rappaport

G.Finazzi (now CEA grenoble) J. Alric (now CEA cadarache) C. Bowler (ENS, Paris)

(3)

Bioenergetics in microalgae

Mitochondrial respiration

CH2O + O2  CO2+ H2O (+ATP)

Versus

Chloroplastic photosynthesis

CO2 + H2O + light  CH2O + O2 (+ATP) Nucleus Mitochondrion Chloroplast

(4)

Diversity of photosynthetic microalgae

primary endosymbiosis Heterotroph ancestor Cyanobacteria Photosynthetic ancestor Nucleus Mitochondrion Multiple secondary endosymbiosis Pagotroph ancestor Alveolates Euglenozoa Diatoms Rhizaria Haptophyta

Second

ary Ph

ot

os

yn

th

etic

eu

kary

ot

es

Chlorophyta Streptophyta

Prima

ry

Phot

os

yn

the

ti

c

euk

ar

yot

es

Rhodophyta

(5)

Adjustment of photoproduced NADPH/ATP

Electron transport chain : 2 NADPH / 2.6 ATP

CO

2

fixation (CBB cycle) : 2 NADPH / 3 ATP

 Regulatory mechanisms

-to consume NADPH in excess

-to produce extra ATP

O2 + 4H+ PQ PQH2 2 H20 2 NADPH 8H+ PC thylakoid ATPase 14 H+ 3ADP 3ATP lumen stroma PSII B6f PSI

Linear electron flow : 4é / 2 NADPH / 12 H+

ATP synthase : 14H+ /3 ATP

(6)

Alternative electron flows

H2O PQ B PC PSI Fdx NADP+ 6f CBB -CHO PSII O2 FNR PGR NDA

PSI-cyclic electron flow

1H

+

/e

-1H

+

/e

-

3H

+

/e

-

≥3H

+

/e

-O2 O2 Chlororespiration -PTOX Mehler reaction O2 Mitochondrial respiration

(7)

H2O PQ B PC PSI Fdx NADP+ 6f CBB -CHO PSII O2 FNR PGR NDA O2 O2 Chlororespiration -PTOX Mehler reaction O2 Mitochondrial respiration

Alternative electron flows : Biophysical tools

PSI-cyclic electron flow : comparison of PSI and PSII rates

ETRPS = YPS . I . sPS . nPS

Light-dependent oxygen uptake (OUL) : comparison of PSII and O2 exchange rate

ETRPSII = O2 (gross) VO2 = O2 (gross) - OUL

(8)

H2O PQ B PC PSI Fdx NADP+ 6f CBB -CHO PSII FNR PGR NDA O2 O2 Mehler reaction O2 Chlororespiration -PTOX Mitochondrial respiration

Diversity of photosynthetic regulations

Ostreococcus sp.

(Prasinophyte, Archaeplastida) (Cardol et al., 2008, PNAS)

Chlamydomonas reinhardtii

(Chlorophyte, Archaeplastida) (Cardol et al., 2003, Plant Physiol.

Cardol et al., 2009, PNAS Dang et al., 2014, Plant Cell)

Phaeodactylum tricornutum

(diatom, stramenopile) (Bailleul et al, 2015, Nature)

PSI-cyclic electron flow

Symbiodinium (Alveolata)

Light-dependent O2 uptake (UOL) capacity up to 45% of ETRPSII

(Jones et al., 1998; Leggat et al., 1999; Badger et al., 2000).

(9)

H2O PQ B PC PSI Fdx NADP+ 6f CBB -CHO PSII FNR O2 O2 O2 O2

(10)

H2O PQ B PC PSI Fdx NADP+

6f CBB -CHO

PSII FNR

O2

O2 O2

Light-oxygen uptake in Symbiodinium

(Roberty et al., 2014, New Phytol.)

HIGH Light

LOW Light

(11)

H2O PQ B PC PSI Fdx NADP+

6f CBB -CHO

PSII FNR

O2

O2 O2

Relationship between PSII and PSI

(Roberty et al., 2014, New Phytol.)

Chlororespiration -PTOX LOW HIGH Light Light Mitochondrial respiration Photorespiration Calvin Cycle Cyanide + SHAM Glycoladehyde O2 O2

(12)

H2O PQ B PC PSI Fdx NADP+

6f CBB -CHO

PSII FNR

O2

Roles of Mehler reaction in Symbiodinium

Light-dependent oxygen uptake Mehler-like reaction

2 e

-

+ 2 O

2

2 O

2-

(PSI-Fdx)

2 O

2-

+

2 H

+

H

2

O

2

+ O

2

(SOD)

H

2

O

2

+

2ASC

 2 H

2

O +

2 MDA

(APX)

2 MDA

+ 2e

-

+

2H

+

2 ASC

(MDAR)

(Mehler, 1951; Asada et al., 1999)

O2

Acts a valve for excess electrons in high light

(13)

13

2 H

2

O  O

2

+

4 H

+

+ 4e

-

(PSII)

2 e

-

+ 2 O

2

2 O

2-

(PSI-Fdx)

Increase of ETR towards O

2

(Roberty et al., 2015, Coral Reefs)

Mehler and ROS detoxification capacity

(26°C vs 33°C in High Light)

Imbalance might participate to coral bleaching under

high light and high temperature

Decrease of ROS scavenging capacity

2 O

2-

+

2 H

+

H

2

O

2

+ O

2

(SOD)

H

2

O

2

+

2ASC

 2 H

2

O +

2 MDA

(APX)

(14)

isolated

Symbiodinium / Stylophora pistillata

14

Does Mehler reaction occur in hospite ?

HIGH Light HIGH Light LOW Light LOW Light

(15)

15 PQ B PC PSI Fdx NADP+ 6f CBB -CHO PSII FNR O2 Glycoladehyde Acetazolamide

(16)

The main light-dependent oxygen uptake in

isolated Symbiodinium (up to 50% of ETR)

16

H2O PQ B PC PSI Fdx NADP+

6f CBB -CHO

PSII FNR

O2

Photoprotection mechanism as long as ROS

detoxification occurs

Provides extra ATP for cellular needs

Does not occurs under controlled laboratory

conditions in S. pistillata unless carbon

fixation capacity is compromised

Conclusions :

Références

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