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J. Biol. Chem., Vol. 283, Issue 50, 34946-34953, December 12, 2008

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Watching the Native Supramolecular Architecture of Photosynthetic Membrane in Red Algae

TOPOGRAPHY OF PHYCOBILISOMES AND THEIR CROWDING, DIVERSE DISTRIBUTION PATTERNS^*

Lu-Ning Liu, Thijs J. Aartsma, Jean-Claude Thomas^¶, Gerda E. M. Lamers^||, Bai-Cheng Zhou, and Yu-Zhong Zhang¹

From the State Key Lab of Microbial Technology, Marine Biotechnology Research Center, Shandong University, Jinan 250100, China, the Department of Biophysics, Huygens Laboratory, Leiden University, Leiden 2300RA, The Netherlands, the ^¶UMR 8186 CNRS & Ecole Normale Supérieure, Biologie Moléculaire des Organismes Photosynthétiques, Paris F-75230, France, and the ^||Institute of Biology, Leiden University, Wassenaarseweg 64, Leiden 2333AL, The Netherlands

The architecture of the entire photosynthetic membrane network determines, at the supramolecular level, the physiological roles of the photosynthetic protein complexes involved. So far, a precise picture of the native configuration of red algal thylakoids is still lacking. In this work, we investigated the supramolecular architectures of phycobilisomes (PBsomes) and native thylakoid membranes from the unicellular red alga Porphyridium cruentum using atomic force microscopy (AFM) and transmission electron microscopy. The topography of single PBsomes was characterized by AFM imaging on both isolated and membrane-combined PBsomes complexes. The native organization of thylakoid membranes presented variable arrangements of PBsomes on the membrane surface. It indicates that different light illuminations during growth allow diverse distribution of PBsomes upon the isolated photosynthetic membranes from P. cruentum, random arrangement or rather ordered arrays, to be observed. Furthermore, the distributions of PBsomes on the membrane surfaces are mostly crowded. This is the first investigation using AFM to visualize the native architecture of PBsomes and their crowding distribution on the thylakoid membrane from P. cruentum. Various distribution patterns of PBsomes under different light conditions indicate the photoadaptation of thylakoid membranes, probably promoting the energy-harvesting efficiency. These results provide important clues on the supramolecular architecture of red algal PBsomes and the diverse organizations of thylakoid membranes in vivo.

Received for publication, July 7, 2008 , and in revised form, October 15, 2008.

^* The work was supported by the National Natural Science Foundation of China (Grant 40676078), by the Hi-Tech Research and Development program of China (Grant 2008AA09Z404), and by the Key International S&T Cooperation Project of China (Grant 2008DFA30440). This project is part of the research programme "From Molecule to Cell" funded by the Netherlands Organization for Scientific Research and the Foundation for Earth and Life Sciences. The costs of publication of this article were defrayed in part by the payment of page charges. This article must therefore be hereby marked "advertisement" in accordance with 18 U.S.C. Section 1734 solely to indicate this fact.

¹ To whom correspondence should be addressed. Tel.: 86-531-8856-4326; Fax: 86-531-8856-4326; E-mail: zhangyz{at}sdu.edu.cn.

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