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Acclimation of the Photosynthetic Apparatus of the Endemic Antarctic Red Macroalga Palmaria Decipiens to Seasonally Changing Light Conditions

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Acclimation of the Photosynthetic Apparatus of the Endemic Antarctic Red Macroalga Palmaria Decipiens to Seasonally Changing Light Conditions Acclimation of the photosynthetic apparatus of the endemic Antarctic red macroalga Palmaria decipiens to seasonally changing light conditions Akklimatisation des Photosyntheseapparates der endemisch antarktischen roten Makroalge Palmaria decipiens an saisonal wechselnde Lichtbedingungen Ulrike H. Luder Ber. Polarforsch. Meeresforsch. 469 (2003) ISSN I618 - 3193 Ulrike H. Luder Institut fü Zellbiologie, Biochemie und Biotechnologie Universitat Bremen Postfach 33 04 40 28334 Bremen Alfred-Wegener-Institut fü Polar und Meeresforschung in der Helmholtz-Gemeinschaft Am Handelshafen 12 27570 Bremerhaven Die vorliegende Arbeit ist die inhaltlich unverändert Fassung einer kumulativen Dissertation, die bei PD. Dr. Jürge Knoetzel in der Arbeitsgruppe ,,Biologie mit dem Schwerpunkt Biochemie und Stoffwechselphysiologie" von Prof. Dr. L. Horst Grimme am Institut fü Zellbiologie, Biochemie und Biotechnologie der Universitat Bremen und bei Prof. Dr. Christian Wiencke in der Projektgruppe ,,Solare UV-Strahlung" am Alfred-Wegener-Institut angefertigt und Januar 2002 dem Fachbereich 2 (Biologielchemie) der Universitat Bremen vorgelegt wurde. TABLE OF CONTENTS ABBREVIATIONS 111 SUMMARY V ZUSAMMENFASSUNG X 1. INTRODUCTION l 1.1. The life strategy of Antarctic macroalgae I 1 .2. The phycobilisomes and phycobiliproteins 3 1.2.1. Phycobilisome structure 5 1.2.2. Phycobiliproteins 7 1.2.3. Linker polypeptides 14 1.2.4. Genes enconding the phycobilisome components 16 1.3. Thesis outline 17 2. MATERIAL AND METHODS 19 2.1. Culture conditions and experimental design 19 2.2. Measurements of optimal quantum yield and photosynthetic performance -20 2.3. Determination of phycobiliprotein and chlorophyll U contents 2 1 2.4. Isolation and characterisation of phycobilisomes 22 3. PUBLICATIONS 25 3.1 . List of publications 25 3.2. Declaration about my working part of the publications 25 Publication 1: Two forms of phycobilisomes in the Antarctic red macroalga Pult~~uriudecipiens (Palmariales, Florideophyceae) 26 Publication 2: Acclimation of photosynthesis and pigments to seasonally changing light conditions in the endernic Antarctic red macroalga Palmana decipiens 37 Publication 3: New insights into phycobilisome structure and their vaiiability according to seasonal changing light conditions in the Antarctic red macroalga Palt~luriadecipiens 44 Publication 4: Acclimation of photosynthesis and pigments during and after six months of darkness in PU~~TVIT~L~decipietls (Rhodophyta) - a study to simulate Antarctic winter sea ice cover 7 1 Publication 5: Dynamics of phycobilisome assembly during and after six months of darkness in Pultmti~~decifiens (Florideophyceae) - a study to simulate Antarctic winter sea ice cover 82 4. SUMMARY OF RESULTS 100 4.1. Isolation and characterisation of phycobilisomes 100 4.2. Acclimation of photosynthesis, pigments and phycobilisome assembly to seasonal changing daylengths 102 4.2.1. Acclimation of photosynthesis and pigments (tissue content) 102 4.2.2. Acclimation of phycobilisome assembly 103 4.3. Accliniation of photosynthesis, pigments and phycobilisome assembly during and after six months of darkness - a study to simulte Antarctic winter sea ice cover 106 4.3.1. Photosynthesis and pigments (tissue content) during darkness and after re-exposure to light 106 4.3.2. Phycobilisome assembly during darkness and after re- exposure to light 107 5. DISCUSSION 110 5.1. Characterisation of phycobilisomes 110 5.2. Acclimation of photosynthesis, pigments and phycobilisome assembly to seasonal changing daylengths 113 5.2.1. Seasonal changes in photosynthesis and pigments tissue content 113 5.2.2. Seasonal changes in phycobilisome assembly 115 5.3. Acclimation of photosynthesis, pigments and phycobilisome assembly during and after six rnonths of darkness - simulte Antarctic winter sea ice cover 120 5.3.1. The influence of darkness On photosynthesis and pigments tissue content 120 5.3.2. The influence of darkness on phycobilisome assembly 123 5.4. Conclusion and furture outlook 126 6. REFERENCES 130 ACKNOWLEDGEMENTS 141 Abbreviations 111 ABBREVIATIONS APC allophycocyanin APB allophycocyanin B Car carotinoid Chi a chlorophyll a ETR relative electron transport rate ETRà maximal ETR Fm maximal chlorophyll fluorescence of PSII after dark incubation Fm1 maximal chlorophyll fluorescence of PSII after light incubation F0 minimal chlorophyll fluorescence of PSII after dark incubation F"' minimal chlorophyll fluorescence of PSII after light incubation FS steady state chlorophyll fluorescence of PSII after light incubation F" variable chlorophyll fluorescence of PSII after dark incubation, (F" =Fm- Fã FÃFm optimal quantum yield of PSII in dark-acclimated state AF differente between F'and Fs AF/Fml effective quantum yield of PSII in light-acclimated state FNR ferredoxin NADP oxidoreductase FW fresh weight L r core linker "CM core membrane linker LHCI light-harvesting antennae of PSI LR rod linker LRC rod core linker PAM pulse-amplitude modulated fluorometer PB S phycobilisome(s) PBão total phycobiliproteins (APC+PC+PE) PB S phycobilisomes PC phycocyanin PCB phycocyanobilin PE phycoerythrin PEB phycoetythrobilin PFD photon tlux density of actinic irradiance PS I photosystem I Abbreviations IV PSI1 photosystem I1 PUB phycourobilin PVB phycoviolobilin RCI reaction center of PSI RCII reaction center of PSI1 S D standard deviation Summary V SUMMARY Palt~u~riadecipiens is an Antarctic endemic and one of the most common red macroalgac in the sublittoral. In this study the influence of the seasonally strongly changing daylengths and of exposure to darkness simulating winter sea-ice Cover, On the photosynthetic apparatus of P. decipietzs was studied in long-term culture experiments. The phycobilisomes, the main light harvesting antennae of red algae consisting of phycobiliproteins, were isolated and characterised (1 ). Their dynamics in response to the seasonally changing daylengths (2) and to dark exposure (3) was investigated and related to phycobiliprotein tissue contents and to the photosynthetic performance. 1. At first the method of Isolation of phycobilisomes was established and the general structure of phycobilisomes of P. decipiens studied. The phycobilisomes from P. decipiens were isolated on discontinuous sucrose gradients as two discrete bands and not in one as expected. To exclude methodical faults, phycobilisomes from the temperate Palmatia paltnata and the unicellular red algae Porphyridium cruetzt~inz and Rhodella violacea were isolated as well. In P. palmata the phycobilisomes were also separated in two discrete bands, whereas the phycobilison~esfrom Porphyridiim and Rhodella were found in one band. The double banded phycobilisomes (PBS and PBS,^,) from P. decipiens were characterised by absorption and fluorescence spectroscopy. Their PE-, PC- and APC- trimers or rather hexan~ers,inclusive their associated linkers, were isolated by native PAGE and were also characterised by absorption and fluorescence spectroscopy. The a- and ß-subunitof PE, PC and APC as well as the associated linker polypeptides and y- subunits were identified by SDS-PAGE, and their apparent molecular masses were caiculated by densitometric analysis. The hemiellipsiodal phycobilisome structure was shown by negative staining and electron microscopy. The phycobiliproteins RIII- phycoerythrin, RI-phycocyanin and allophycocyanin were identified. The PBS and PBS,,,.,, showed no significant differences in their absorption spectra and phycobiliprotein ratios, although PBSlWseem to be somewhat smaller. Differentes were found in their low molecular mass subunit complexes, which are assumed to be r-phycoerythrin. The polypeptide Pattern of the PBS and PBSlw showed no differences in the molecular masses of their subunits and linker polypeptides, but in their percentage distribution. The results suggest that the PBSlw is a closer packed and PBS a little more loosely aggregated hemiellipsiodal phycobilisome fonn. Summary V1 Furthermore, three coloured 7-subunits (Y3', 3, y403) and three hexarneric PE-subunit complexes ((aß),,?' (~ß)~y'3, (aß)6"y03 with different absorption characteristics around 544.5 nm and with a red shift in their absorption maxima were identified, both in PBS and PBS,,,,,,. Moreover, a red shift in their fluorescence emission maxima was detected, which probably improves the energy transfer downhill the rod. The p-subunit and its associated PE-hexamer ((aß)6?35shows a further fluorescence maximum at 595 nm, which also enhances the energy transfer downhill the rod and makes a coupling of PE directly to APC most probable. 2. The influence of seasonally fluctuating Antarctic daylength On the photosynthetic apparatus of P. decipiet1.y was studied in a long-term culture experiment, mirnicking the Antarctic year. Over one year P. decipiens was cultivated under weekly changing daylengths (under constant irradiance), simulating the seasonal variations of daylength, present at the collecting site on King George Island, South Shetland Islands, Antarctica varying between 5 h in winter and 20 h in summer. The maximal photosynthetic performance (ETR) and the optimal quantum yield (Fv/Fm)were measured by in vivo chlorophyll fluorescence in monthly intervals. The phycobiliprotein and chlorophyll a tissue contents were quantified. Phycobilisomes were isolated monthly and changes in their phycobiliprotein and polypeptide composition were determined. In Antarctic summer, ETR, F/F and pigment tissue contents showed its lowest values, probably to avoid photodamage caused
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