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«Wiebke E. Krämer PhD Thesis, University of Bremen Bremen, February 2012 University of Bremen Photoecophysiology of symbiotic zooxanthellae of ...»

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Photoecophysiology of symbiotic zooxanthellae

of hermatypic corals

Wiebke E. Krämer

PhD Thesis, University of Bremen

Bremen, February 2012

University of Bremen

Photoecophysiology of symbiotic zooxanthellae of hermatypic corals

Dissertation submitted by

Wiebke E. Krämer

In partial fulfilment of the requirements for the degree of

Doctor of natural sciences (Dr. rer. nat.)

Faculty of Biology/Chemistry

University of Bremen

February 2012

The present study has been realized at the Department of Marine Botany, Bremen Marine Ecology Centre for Research and Education (BreMarE), Faculty Biology/Chemistry, University of Bremen. It was funded by the Comprehensive Research Funding Program (Zentrale Forschungsförderung, ZF) at the University of Bremen (Project No. 02/115/06).

Examination Committee:

First Examiner: Prof. Dr. Kai Bischof Department of Marine Botany, University of Bremen Second Examiner: Prof. Dr. Claudio Richter Alfred Wegener Institute for Polar and Marine Research, Bremerhaven Additional Examiner I: Prof. Dr. Wilhelm Hagen Department of Marine Zoology, University of Bremen Additional Examiner II: Dr. Martina Löbl MARUM, University of Bremen Student Member I: Dipl.-Biol. Dorothea Kohlmeier PhD student, Department of Marine Botany, University of Bremen Student Member II: Sandra Straub Marine biology student, University of Bremen Zooxanthellae… without which it is just possible that such immense aggregations of living matter which constitute a coral reef could not originate and flourish.

(C.M. Yonge, 1930) Table of Contents Table of Contents Table of Contents

List of Figures

List of Tables




1. Introduction

1.1 Coral-algae symbiosis – key to the ecological success of corals

1.2 The ‘golden-brown’ side of the symbiosis

1.3 Importance of different coral-algal associations

1.4 Coral bleaching

1.5 Coral bleaching and photoinhibition

1.6 Photoprotection

1.6.1 Adjustments of light-harvesting antenna size

1.6.2 Xanthophyll cycle-mediated dissipation of excess excitation energy

1.6.3 Antioxidative system

2. Objectives

4. 1 Laboratory experiments

4.1.1 Maintenance of stock cultures

4.1.2 Experimental design

4.2 Field work

4.2.1 Study area

4.2.2 Coral species

Pocillopora damicornis (Linnaeus, 1758)

Pavona decussata (Dana, 1846)

4.2.3 Experimental design High-light exposure of Pavona decussata and Pocillopora damicornis Photophysiological response of Symbiodinium in Pocillopora damicornis to light deprivation.. 37

4.3 Analytical methods

4.3.1 Chlorophyll a fluorescence measurements

4.3.2 Determination of cell densities

4.3.3 Pigment analysis

4.3.4 Determination of chlorophyll a-specific absorption

4.3.5 Measurement of total glutathione content

4.3.6 Statistical analysis

–  –  –

5. Thesis chapters

Chapter I Dynamic regulation of photoprotection determines thermal tolerance of two phylotypes of Symbiodinium clade A at two photon fluence rates

Chapter II Differential photosynthetic responses of Symbiodinium in two scleractinian corals to high irradiance

Chapter III Site-specific photophysiological response of Symbiodinium in Pocillopora damicornis to light deprivation – A field study

6. Synopsis of discussion

6.1 Physiological response of Symbiodinium to high irradiance

6.2 Physiological response of Symbiodinium to high irradiance and elevated temperatures

6.3 Host-mediated differences in symbiont physiology

6.4 Host-specific differences in symbiont physiology

6.5 Contribution of heterotrophic feeding to the functionality of the coral-algae symbiosis................. 159

6.6 Towards the understanding of coral bleaching

6.7 Ecological implications

6.8 Perspectives



II List of Figures List of Figures Figure 1.1 (a) Drawing of the motile form of Symbiodinium (McLaughlin and Zahl 1959).

(b) Light micrograph of cultured Symbiodinium showing mainly vegetative (and dividing) cells (Photograph by W. Krämer)

Figure 1.2 Maximum likelihood phylogram of currently known clades of the genus Symbiodinium based on LSU rDNA sequence data and associated hosts (adapted from Pochon and Gates 2010).

Numbers at nodes are bootstrap values, while black dots represent values of 100% bootstrap support. Nodes without numbers indicate supports 70%.

Figure 1.3 Representation of the light-induced photosynthetic electron flow through the ‘Z’-scheme involving the sequential operation of photosystem II (P680) and I (P700) reaction centres interconnected by the cytochrome b6f (cyt b6f) complex.

In the course of the two light-induced reactions electrons derived from the oxygen evolving complex (OEC; thereby liberating oxygen and protons) are transferred through the photosynthetic electron transport chain to the acceptor side of PSI, where they are used to reduce NADP+. Through the electron transfer, protons are released into the thylakoid lumen to generate a transthylakoidal proton gradient, which is utilized in the ATP synthesis through the action of ATP synthases. 4Mn - manganese cluster of the OEC; Yz – tyrosine residue of the D1 protein; Pheo – pheophytin; QA and QB – primary and secondary plastoquinone electron acceptor in PSII; PQ –plastoquinone;

FeS – Rieske iron-sulfur protein; Cyt f – cytochrome f; Cyt bH – high potential cytochrome b6; Cyt bL – low potential cytochrome b6; PC – plastocyanine; A0 – specialized chlorophyll a in PSI; A1 – specialized quinone; FX, FB, FA – ironsulfur centres; Fd – ferredoxin; FNR – ferredoxin-NADP+ reductase.

Approximate estimated times for various steps are also noted on the figure (Govindjee and Govindjee 2000). The circular path around the cyt b6f complex indicates the Q cycle, while the dark blue arrow from the acceptor side of the PSI to the cyt b6f complex symbolizes cyclic electron transport around PSI. The scale to the left indicates the redox potential Em of the electron carriers at pH 7.

(modified from Govindjee 2004 by S. Krämer)

Figure 1.4 Antioxidative network, also referred to as water–water cycle, showing the photosynthetic splitting of water at the donor side of PSII, the electron transport to PSI including the photoreduction of O2 at its acceptor side to yield O2–, the disproportionation to H2O2, the reduction of H2O2 to H2O and the concomitant oxidation of ascorbate to monodehydroascorbate and the different pathways of regeneration of ascorbate.

APX – ascorbate peroxidase;

AsA – ascorbate; CuZn-SOD – copper-zinc superoxide dismutase; DHA – dehydroascorbate; DHAR – dehydroascorbate reductase; Fd – ferredoxin; FNR – Fd-NADP+ reductase; GR – glutathione reductase; GSH, GSSG – reduced and oxidized form of glutathione, respectively; MDA – monodehydroascorbate;

MDAR – monodehydroascorbate reductase; sAPX – stromal APX; SF – stromal factor; tAPX – thylakoidal APX; VDE – violaxanthin de-epoxidase (functionally equivalent to the diadinoxanthin de-epoxidase; from Asada 2000).........19

IIIList of Figures

Figure 4.1 (a) Experimental setup illustrating exposure of cultures to high light (upper array) and low light (lower array) at one temperature, (b) close-up of the experimental setup showing one treatment.

(c) Cultures growing at 145 µmol photons m-2 s-1 at different temperatures (from left to right: 25, 30 and 32°C) on day 21; note different cell densities in the treatments.

Figure 4.2 Map showing the study area around Heron Island, Capricorn Bunker Group, Great Barrier Reef (GBR), Australia (23.

44 S 151.917 E) and the location of the two study sites of the in situ experiment: 1, Coral Gardens (23.447 S 151.912 E) and 2, North Wistari Reef (23.435 S 151.876 E). Map was produced using Ocean Data View (Schlitzer, 2011, http://odv/awi.de) with data from ‘Coral reef distribution of the World (2010)’ provided by UNEP-WCMC

Figure 4.3 (a) Colony of Pocillopora damicornis in Southern Great Barrier Reef, Australia, illustrating its branching growth structure (Photograph by Neville Coleman).

(b) Colony of Pavona decussata in the Great Barrier Reef, Australia, showing its foliaceous morphology (Photograph by Charlie Veron).

Figure 4.4 (a) Experimental design of the study.

Nubbins of Pavona decussata and Pocillopora damicornis were exposed to a combination of two irradiance and two lincomycin treatments over four days. Large coral nubbins were used for pigment analysis via HPLC and determination of symbiont densities subsequent to the measurement of the effective quantum yield of PSII (ΔF/Fm’). Measurements of maximum quantum yield (Fv/Fm) conducted at night-time were performed on an additional set of coral nubbins. (b,c) Photographs of the experimental set-up in the outdoor tank

Figure 4.5 (a) Schematic diagram and (b) photograph showing the setup of the in situ experiment.

‘+ Light’ – translucent tubes allowing corals to perform photosynthesis; ‘- Light’ – opaque tubes excluding light. The blue arrow indicates the direction of the water flow

Figure 4.6 Schematic illustration of the three competing de-excitation pathways of excited states of chlorophyll a in the photosystem II: primary photochemistry, heat dissipation and fluorescence (in descending order of their importance under optimal conditions)

Figure 4.7 Schematic depiction of the principle of fluorescence quenching analysis by the saturation pulse method.

F0 – minimum fluorescence of a dark-adapted sample;

Fm – maximum fluorescence of a dark-adapted sample after application of a saturation pulse; Fv – variable fluorescence, calculated as the difference between Fm and F0; Ft and Fm’ – minimum and maximum fluorescence of a light-adapted sample, respectively. (Figure taken from Walz).

Figure 6.1 Model of cell signalling pathways in the host cell, which culminate in bleaching by host cell apoptosis or by programmed cell death (PCD) of the symbiont cell.

Also shown is the potential role of glutathione (GSH; highlighted in yellow), which is proposed, based on the results of this study. In spite of the presence of reactive oxygen species (ROS) scavenging systems in both the host and the symbiont cell, the antioxidative systems can become overwhelmed by the accelerated ROS generation during thermal stress. Primary sites of damage under thermal stress (indicated by red flashes) include photosystem II (PSII) and Calvin-cycle (CZ) in the symbiont cell and mitochondrial membranes in the host cell. ROS as superoxide (O2–) and hydrogen peroxide (H2O2) along with IV List of Figures nitric oxide (NO) leaking out the symbiont cell can, in conjunction with O2– and NO generated in the host cell, initiate apoptotic cascades by the activation of pro-apoptotic factors (e.g. AIF, p53, NF-κB; see Weis 2008 for details). GSH can react with NO to form of S-nitrosoglutathione (GSNO) in the algal cell.

Thereby, it minimizes the induction of PCD in the algae cell and the initiation of host’s apoptotic cascades. AsA-GSx cycle – ascorbate-glutathione cycle;

iNOS – inducible nitric oxide synthase; ONOO– – peroxynitrite; PSI – photosystem I. There is direct evidence in coral-algae symbiosis for pathways shown in red, indirect evidence for those shown in blue and evidence only in other metazoan or host-microbe interactions and in higher plants for those shown in green and black, respectively (modified from Weis 2008).

–  –  –

List of Tables Table 4.1 Details on Symbiodinium strains exposed to elevated temperatures in combination with two photon fluence rates (Chapter I).

–  –  –

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