coral bleaching and thermal stress: the first step is not damage to photosystem ii

Coral bleaching and thermal Coral bleaching and thermal stress: The first step is not stress: The first step is not damage to Photosystem II.damage to Photosystem II.

Ove Hoegh-GuldbergOve Hoegh-Guldberg

School of Biological SciencesSchool of Biological Sciences

University of SydneyUniversity of Sydney

OutlineOutlineElevated temperature and Elevated temperature and

coral-dinoflagellate symbioses.coral-dinoflagellate symbioses.

Light, photoinhibition and photoprotectionLight, photoinhibition and photoprotection

Primary effects of temperature: A modelPrimary effects of temperature: A model

Take home message: Take home message: Bleaching is due to a lowering Bleaching is due to a lowering of the threshold for photoinhibition.of the threshold for photoinhibition.

Stylophora pistillataStylophora pistillata

Seriatopora hystrixSeriatopora hystrix

Hoegh-Guldberg and Smith (1989)Hoegh-Guldberg and Smith (1989)

S. pistillata S. hystrix S. pistillata S. hystrix

Photosynthetic ratePhotosynthetic rate Respiratory rateRespiratory rate


Classic photoinhibition.Classic photoinhibition.Classic photoinhibition.Classic photoinhibition.

-40

-20

0

20

40

60

80

100

0 500 1000 1500 2000 2500

PhotoinhibitionPhotoinhibition

IrradianceIrradianceNet

Pho

tosy

nthe

t ic R

ate

Net

Pho

tosy

nthe

t ic R

ate

Rub

isco

Rub

isco

LHC LHC

Higher Plants: Low light and Normal COHigher Plants: Low light and Normal CO2 2 Fixation Fixation

e-

PSII

PSI COCO22

H+

HH++

POOLPOOL

Organic COrganic C(Dark Reactions)(Dark Reactions)

StromaStromaLumenLumen

OO22

HH22OO

NADPNADP

NADPHNADPH + ATP+ ATP

ATPATPATPATP

ADPADPADPADP

DARK REACTIONSDARK REACTIONSDARK REACTIONSDARK REACTIONS

Thylakoid membraneThylakoid membraneThylakoid membraneThylakoid membrane

LHC LHC PSII

PSI

HH++

POOLPOOL

DVE

ZeaxanthinZeaxanthin

NPQ

ViolaxanthinViolaxanthin

OO22

HH22OOStimulatedStimulatedas as pH builds pH builds due to due to reduction of Oreduction of O22

OO22

OO2 2 --

Mehler

H+

e-

Violaxanthin and Zeaxanthin are higher Violaxanthin and Zeaxanthin are higher plant xanthophylls. In dinoflagellates, plant xanthophylls. In dinoflagellates, monoepoxide diadinoxanthin and monoepoxide diadinoxanthin and diatoxanthin probably perform thediatoxanthin probably perform thesame roles.same roles.

Violaxanthin and Zeaxanthin are higher Violaxanthin and Zeaxanthin are higher plant xanthophylls. In dinoflagellates, plant xanthophylls. In dinoflagellates, monoepoxide diadinoxanthin and monoepoxide diadinoxanthin and diatoxanthin probably perform thediatoxanthin probably perform thesame roles.same roles.

NADPNADP

NADPHNADPH

Photoprotection Photoprotection against the effects against the effects of high irradiance.of high irradiance.

Photoprotection Photoprotection against the effects against the effects of high irradiance.of high irradiance.

SOD

SOD

APO

APO

HH22OO22

HH22O + OO + O22+ MDA+ MDA

Rub

isco

Rub

isco

LHCLHC

Higher Plants: High light and photo-oxidation Higher Plants: High light and photo-oxidation

e-

PSII

PSI COCO22

H+

HH++

POOLPOOL



OO22

HH22OO

NADPNADP


OO22

OO2 2 --

Mehler

Active oxygenActive oxygenActive oxygenActive oxygen

Mehler Reaction:Mehler Reaction:Electrons donated Electrons donated from near PS I to from near PS I to oxygen => superoxide.oxygen => superoxide.

Chronic photoinhibitionChronic photoinhibitionChronic photoinhibitionChronic photoinhibition

Singlet oxygen Singlet oxygen originating from originating from electron donation at electron donation at or near PS IIor near PS II

Fo

qP

qN

Ft

FV’/FM

Time (min)

Pulsed Amplitude Modulated (PAM) Pulsed Amplitude Modulated (PAM) fluorescence analysisfluorescence analysisPulsed Amplitude Modulated (PAM) Pulsed Amplitude Modulated (PAM) fluorescence analysisfluorescence analysis

Pulsed amplitude modulated Pulsed amplitude modulated (PAM) Fluorometry(PAM) FluorometryPulsed amplitude modulated Pulsed amplitude modulated (PAM) Fluorometry(PAM) Fluorometry

Chl Chl aa (PSII) (PSII)Chl Chl aa (PSII) (PSII)

LHC LHC PSII

PSI

HH++

POOLPOOL

DVE

ZeaxanthinZeaxanthin

NPQ

ViolaxanthinViolaxanthin

OO22

HH22OOStimulatedStimulatedas as pH builds pH builds due to due to reduction of Oreduction of O22

OO22

OO2 2 --

Mehler

H+

e-

NADPNADP

NADPHNADPH

PAM Fluorometer PAM Fluorometer measures efficiency measures efficiency of light utilisation of of light utilisation of Photosystem II Photosystem II

PAM Fluorometer PAM Fluorometer measures efficiency measures efficiency of light utilisation of of light utilisation of Photosystem II Photosystem II

SOD

SOD

APO

APO

HH22OO22


PSII

NPQ - heat

Phot

osyn

th

Photochemistry versus heatPhotochemistry versus heat

Fo

qP

qN

Ft

FV’/FM

Porites cylindrica (June 1997)Porites cylindrica (June 1997)

DarkDark 800 umol m-2 s-1800 umol m-2 s-1

11 22 33 44

Yield versus time of day

0.400

0.450

0.500

0.550

0.600

0.650

0.700

0.750

0.800

0 5 10 15 20 25

Time

Yie

ld

Pink Sp

Brow n Sp

PoritesSunriseSunrise SunsetSunset

YesYes

Yield versus time of day

0.400

0.500

0.600

0.700

0.800

0 20 40 60 80

Time

Yie

ldPink Sp

Brow n Sp

Porites

Dynamic PhotoinhibitionDynamic Photoinhibition

Stylophora pistillataStylophora pistillataOne Tree IslandOne Tree IslandFeb ‘97Feb ‘97

Stylophora pistillataStylophora pistillataOne Tree IslandOne Tree IslandFeb ‘97Feb ‘97Normal Normal Normal Normal Normal (28Normal (28ooC)C)Normal (28Normal (28ooC)C)

Electron flow in heat stressed zooxanthellae is oxygen dependent(I.e. MP pathway)

Electron flow in heat stressed zooxanthellae is oxygen dependent(I.e. MP pathway)

Calvin cycle doesn’t turn on. qN has to continuedumping heat.

Calvin cycle doesn’t turn on. qN has to continuedumping heat.Heat stressed Heat stressed

(32(32ooC, 4 h)C, 4 h)measured in measured in presence presence of oxygen.of oxygen.

Heat stressed Heat stressed (32(32ooC, 4 h)C, 4 h)measured in measured in presence presence of oxygen.of oxygen.

Heat stressed Heat stressed (32(32ooC, 4 h)C, 4 h)measured in measured in absence absence of oxygen.of oxygen.

Heat stressed Heat stressed (32(32ooC, 4 h)C, 4 h)measured in measured in absence absence of oxygen.of oxygen.

Effects of heat on zooxanthellae:Effects of heat on zooxanthellae:

• Primary effectPrimary effect is to stall the flow of electrons to is to stall the flow of electrons to dark reactions of photosynthesis. The first step is dark reactions of photosynthesis. The first step is not to disrupt the light harvesting reactions as not to disrupt the light harvesting reactions as previously thought.previously thought.

• PhotoprotectionPhotoprotection is induced as dark reactions fail is induced as dark reactions fail through oxygen dependent electron flow (Mehler through oxygen dependent electron flow (Mehler Reactions). Reactions).

Rub

isco

Rub

isco

LHCLHC

Zooxanthellae: High light and Normal COZooxanthellae: High light and Normal CO2 2 Fixation Fixation

e-

PSII

PSI COCO22

H+

HH++

POOLPOOL


Ascorbate Ascorbate PoolPool

DVE

DiatoxanthinDiatoxanthin

NPQ


SOD = Superoxide dismutaseSOD = Superoxide dismutaseAPO = Ascorbate peroxidaseAPO = Ascorbate peroxidaseDVE = Violaxanthin deepoxidase DVE = Violaxanthin deepoxidase

DiadinoxanthinDiadinoxanthin

OO22

HH22OO

NPQ reducesNPQ reduces possibility of possibility of singlet oxygen singlet oxygen formation. formation. Singlet oxygen Singlet oxygen promotes promotes degradation of degradation of D1 protein and D1 protein and damage to reaction damage to reaction centre componentscentre components

StimulatedStimulatedas as pH builds pH builds due to due to reduction of Oreduction of O22

OO22

OO2 2 --

Mehler O2 -

SOD

SOD

APO

APO

HH22OO22 (Stromal SOD and APO not shown)

NADPNADP



Rub

isco

Rub

isco

LHCLHC

New model (step 1): reduced CONew model (step 1): reduced CO2 2 FixationFixation

e-

PSII

PSI CO2

H+

HH++

POOLPOOL

Organic C(Dark Reactions)


DDE


NPQ



OO22

HH22OO

Capacity of NPQ Capacity of NPQ to quench PS IIto quench PS IIexceeded. exceeded.


OO22

OO2 2 --

Mehler O2 -

SOD

SOD

APO

APO


NADPNADP



O2 -

O2 -

OO2 2 --

1. Calvin cycle begins to fail1. Calvin cycle begins to fail Electron pressure builds.Electron pressure builds.2. NPQ then MP pathways2. NPQ then MP pathways come into play come into play 3. Quantum yield still in 3. Quantum yield still in tact as electrons aretact as electrons are passed to oxygenpassed to oxygen

1. Calvin cycle begins to fail1. Calvin cycle begins to fail Electron pressure builds.Electron pressure builds.2. NPQ then MP pathways2. NPQ then MP pathways come into play come into play 3. Quantum yield still in 3. Quantum yield still in tact as electrons aretact as electrons are passed to oxygenpassed to oxygen

Rub

isco

Rub

isco

LHCLHC

e-

PSII

PSI

H+

HH++

POOLPOOL


DDE

NPQ


OO22

HH22OO



OO22

OO2 2 --

Mehler O2 -

SOD

SOD

APO

APO



O2 -

OO2 2 --

1O2

OO2 2 --

OO2 2 --

OO2 2 --

OO2 2 --

OO2 2 --

OO2 2 --OO2 2

--

OO2 2 --

OO2 2 --

11OO22



4. MP pathway cannot 4. MP pathway cannot absorb all singlet oxygenabsorb all singlet oxygen5. Singlet oxygen and 5. Singlet oxygen and superoxide builds upsuperoxide builds up and photosystems and and photosystems and general p/syn components general p/syn components are damagedare damaged6. Oxygen evolution reduced6. Oxygen evolution reduced

4. MP pathway cannot 4. MP pathway cannot absorb all singlet oxygenabsorb all singlet oxygen5. Singlet oxygen and 5. Singlet oxygen and superoxide builds upsuperoxide builds up and photosystems and and photosystems and general p/syn components general p/syn components are damagedare damaged6. Oxygen evolution reduced6. Oxygen evolution reduced

New model (step 2): redox buildupNew model (step 2): redox buildup

Rub

isco

Rub

isco

LHCLHC

Zooxanthellae: High light and Normal COZooxanthellae: High light and Normal CO2 2 Fixation Fixation

e-

PSII

PSI COCO22

H+

HH++

POOLPOOL



DVE


NPQ


SOD = Superoxide dismutaseSOD = Superoxide dismutaseAPO = Ascorbate peroxidaseAPO = Ascorbate peroxidaseDVE = Violaxanthin deepoxidase DVE = Violaxanthin deepoxidase


OO22

HH22OO



OO22

OO2 2 --

Mehler O2 -

SOD

SOD

APO

APO


NADPNADP



0

200

400

600

800

0 50 200 800 1600

PAR (µmol quanta m-2 s-1)

dar

k-ad

apte

d F

v/F

m

Upper surface Lower surface

0

200

400

600

800

0 50 200 800 1600

(a) 28ºC

(b) 33ºC

The interaction of light and temperature may explain some of the differences in bleaching on the upper versus lower surfaces of corals.

The interaction of light and temperature may explain some of the differences in bleaching on the upper versus lower surfaces of corals.

Upper surfaceUpper surface

Lower surfaceLower surfaceLi

ght

Ligh

t

Rub

isco

Rub

isco

LHCLHC

e-

PSII

PSI CO2

H+

HH++

POOLPOOL

Organic C(Dark Reactions)


DDE


NPQ


OO22

HH22OO

OO22

OO2 2 --

Mehler O2 -

SOD

SOD

APO

APO

HH22OO22

NADPNADP

NADPHNADPH + ATP+ ATPO2

-

O2 -

OO2 2 --

XX

coral bleaching and thermal stress: the first step is not damage to photosystem ii

Documents

classic photoinhibition

coral bleaching

coraldinoflagellate

low light

modeltake home message

mehlerh eviolaxanthin

ove hoeghguldbergschool

higher plant xanthophylls