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Title: Mutation of Photosystem II D1 protein that empower efficient phenotypes of Chlamydomonas Reinhardtii under extreme environment in space

Author
item GIARDI, MARIA - National Research Council - Italy
item REA, GIUSEPPINA - National Research Council - Italy
item LAMBREVA, MAYA - National Research Council - Italy
item ANTONACCI, A - National Research Council - Italy
item PASTORELLI, S - National Research Council - Italy
item BERTALAN, IVO - National Research Council - Italy
item JOHANNINGMEIER, U - National Research Council - Italy
item Mattoo, Autar

Submitted to: PLOS ONE
Publication Type: Peer Reviewed Journal
Publication Acceptance Date: 4/11/2013
Publication Date: 5/14/2013
Citation: Giardi, M.T., Rea, G., Lambreva, M., Antonacci, A., Pastorelli, S., Bertalan, I., Johanningmeier, U., Mattoo, A.K. 2013. Mutation of Photosystem II D1 protein that empower efficient phenotypes of Chlamydomonas Reinhardtii under extreme environment in space. PLoS One. 8(5):e64352.

Interpretive Summary: Oxygenic photosynthesis involves carbon dioxide fixation and release of oxygen that we breathe. This is the process that has made life possible on earth. This process is initiated in chloroplasts by critical protein components associated with a system known as photosystem II. This photosystem constitutes reaction center proteins made of two sister proteins called D1 and D2. Out of these two proteins, D1 rapidly turns over in plants and its life history is tuned to light radiation. D1 protein is a key protein involved in photochemistry that ultimately enhances crop productivity. Substitution of certain amino acids in the protein backbone of D1 results in changing the dynamics of its stable nature under different irradiation conditions. Being a component of photosystem II reaction centre, modification of D1 can differentially affect photosynthesis and thereby crop productivity. Oxygenic photosynthesis is thought to be a phenomenon prevalent on earth and little is known about performance of photosystem II photochemistry in space. An opportunity arose to test a model organism, an algal strain of Chlamydomonas, and its two D1 mutants, called A251C and I163N, in the environment of outer space. In this collaborative work with scientists at CNR, Italy, we show here that the two D1 algal mutants are capable of capturing cosmic radiation and utilize it for efficient photosynthesis and growth. We show that substituting ileu163 with asn and ala252 with cys empower the D1 protein to be relatively stable to cosmic radiation and thereby enable better photosystem II photochemistry in space. These data pinpoint the important role of D1 conformation in stabilizing (and enhancing) photosystem II function and add a novel facet to the dynamic role of D1 in algae and plants This research is important to biologists and biochemists involved with improvement of crop productivity through efficient photosynthesis.

Technical Abstract: Oxygenic photosynthesis involves capture and conversion of light energy into chemical energy, a process fundamental to life including plant productivity on Earth. Photosynthetic electron transport is catalyzed by two photochemical reaction centres in series, photosystem II (PS II) and photosytem I (PS I). PS II is the only pigment-protein complex in nature capable of catalyzing oxidation of water to produce molecular oxygen. It consists of chloroplast membrane-embedded multi-subunit pigment-protein complexes: the oxygen-evolving complex, a light-harvesting chlorophyll protein complex and a reaction centre core. The PS II reaction centre is made of D1, D2, ' and ' subunits of cytochrome b559, PsbI, and PsbW polypeptides. The D1-D2 heterodimer binds all the electron carriers and cofactors necessary for electron transport: P680 (' chlorophyll a dimer), pheophytin a, a non-heme-iron, '-carotene, the electron donor tyrosine, and the electron acceptor plastoquinone. D1 is the pivotal reaction centre component characterized by its rapid turnover during light-mediated photochemistry, and is a target of ultraviolet B (UVB) radiation, photosynthetic herbicides and environmental stress. Its rapid turnover makes D1 a major factor of PS II instability and its replacement a primary event of the PS II repair cycle. Conservation and ubiquitous nature of the dynamic metabolism of D1 throughout evolution among oxygen evolving species has made it a central object of studies in photosynthesis and plant biology. Interestingly, mutation or genetic substitution of some amino acids in D1 can result in either an increase or a decrease in photosynthetic activity. Oxygenic photosynthesis is thought to be a phenomenon prevalent on earth and little is known about performance of PS II photochemistry in space. We have tested the effects of space environment on PS II and photochemical dynamics of an engineered unicellular green alga Chlamydomonas reinhardtii and its two D1 mutants, A251C and I163N. We show here that the two D1 C. reinhardtii mutants are capable of capturing cosmic radiation and utilize it for efficient photosynthesis and growth.