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Localisation and characterisation of thylakoid membrane-shaping factors in Synechocystis sp. PCC 6803
Localisation and characterisation of thylakoid membrane-shaping factors in Synechocystis sp. PCC 6803
Oxygenic photosynthesis converts light energy to chemical energy and releases molecular oxygen as a byproduct. Furthermore, the energy fixed during photosynthesis is the source for the main production of biomass on earth. Its evolutionary development goes back more than 2700 million years and has shaped a large part of life on our earth. Photosynthesis is a highly complex process involving a large number of factors. The most important photosynthetic complexes are photosystem I, photosystem II, cytochrome b6f and the ATP synthase. A co-evoled endomembrane system called thylakoids serves as carrier and reaction space for photosynthesis. While the photosynthetic complexes were relatively conserved in the course of evolution and differentiation of species, the shape and arrangement of the thylakoids were subject to constant change in adaptation to the respective environmental circumstances. This ranges from simple circular or star-shaped arrangements in cyanobacteria to the clear discrimination of stroma and grana lamellae in chloroplasts of today’s plants. In the cyanobacterium Synechocystis sp. PCC 6803 (hereafter Synechocystis 6803) the individual thylakoids are arranged in layers parallel to the plasma membrane and interrupted by convergence zones. These are regions where the thylakoid membranes partially fuse and curve towards the plasma membrane forming contact sites called thylapses. Due to the very high number of ribosomes in these areas, they have been shown to be biogenic regions. CurT, the cyanobacterial homolog of the CURVATURE THYLAKOID1 protein family, is essential for the curvature of thylakoids in cyanobacteria as well as in chloroplasts of green algae and higher plants. A lack of CurT triggers dramatic alterations in the thylakoid architecture of Synechocystis 6803 including the loss of convergence zones. Moreover, photosynthetic activity and growth are reduced. By whole-genome sequencing of a strain partially suppressing the photosynthetic curT- phenotype, the protein AncM (anchor of convergence membranes) was identified. AncM is an integral membrane protein located at thylakoid membrane convergence zones that form thylapses. An ancM- mutant is shown to exhibit an altered thylakoid ultrastructure with converged membranes detached from the plasma membrane and reduced photosynthetic performance. Furthermore, reduction in one protein, CurT or AncM, effects the other, which suggests an antagonistic function. Another important factor for thylakoid architecture and maintenance is VIPP1. It has been shown that it belongs to a highly conserved superfamily of stabilizing and stress-counteracting proteins. Despite its essential role and apparent coevolution with thylakoids, the exact mechanism and action of VIPP1 has not been fully deciphered. However, by means of high-resolution microscopic techniques, the structure of homooligomeric supercomplexes could be shown in detail. Amphiphilic structures were identified and thereby a potential mechanism of how VIPP1 builds large hydrophobic columns to bind and curve membranes. In summary, the present work represents an extension of the previous knowledge about factors shaping the thylakoid membrane, their effects on photosynthesis and an expanded understanding of this important process.
Cyanobacteria, Synechocystis, AncM, VIPP1, CLEM
Ostermeier, Matthias
2022
English
Universitätsbibliothek der Ludwig-Maximilians-Universität München
Ostermeier, Matthias (2022): Localisation and characterisation of thylakoid membrane-shaping factors in Synechocystis sp. PCC 6803. Dissertation, LMU München: Faculty of Biology
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Abstract

Oxygenic photosynthesis converts light energy to chemical energy and releases molecular oxygen as a byproduct. Furthermore, the energy fixed during photosynthesis is the source for the main production of biomass on earth. Its evolutionary development goes back more than 2700 million years and has shaped a large part of life on our earth. Photosynthesis is a highly complex process involving a large number of factors. The most important photosynthetic complexes are photosystem I, photosystem II, cytochrome b6f and the ATP synthase. A co-evoled endomembrane system called thylakoids serves as carrier and reaction space for photosynthesis. While the photosynthetic complexes were relatively conserved in the course of evolution and differentiation of species, the shape and arrangement of the thylakoids were subject to constant change in adaptation to the respective environmental circumstances. This ranges from simple circular or star-shaped arrangements in cyanobacteria to the clear discrimination of stroma and grana lamellae in chloroplasts of today’s plants. In the cyanobacterium Synechocystis sp. PCC 6803 (hereafter Synechocystis 6803) the individual thylakoids are arranged in layers parallel to the plasma membrane and interrupted by convergence zones. These are regions where the thylakoid membranes partially fuse and curve towards the plasma membrane forming contact sites called thylapses. Due to the very high number of ribosomes in these areas, they have been shown to be biogenic regions. CurT, the cyanobacterial homolog of the CURVATURE THYLAKOID1 protein family, is essential for the curvature of thylakoids in cyanobacteria as well as in chloroplasts of green algae and higher plants. A lack of CurT triggers dramatic alterations in the thylakoid architecture of Synechocystis 6803 including the loss of convergence zones. Moreover, photosynthetic activity and growth are reduced. By whole-genome sequencing of a strain partially suppressing the photosynthetic curT- phenotype, the protein AncM (anchor of convergence membranes) was identified. AncM is an integral membrane protein located at thylakoid membrane convergence zones that form thylapses. An ancM- mutant is shown to exhibit an altered thylakoid ultrastructure with converged membranes detached from the plasma membrane and reduced photosynthetic performance. Furthermore, reduction in one protein, CurT or AncM, effects the other, which suggests an antagonistic function. Another important factor for thylakoid architecture and maintenance is VIPP1. It has been shown that it belongs to a highly conserved superfamily of stabilizing and stress-counteracting proteins. Despite its essential role and apparent coevolution with thylakoids, the exact mechanism and action of VIPP1 has not been fully deciphered. However, by means of high-resolution microscopic techniques, the structure of homooligomeric supercomplexes could be shown in detail. Amphiphilic structures were identified and thereby a potential mechanism of how VIPP1 builds large hydrophobic columns to bind and curve membranes. In summary, the present work represents an extension of the previous knowledge about factors shaping the thylakoid membrane, their effects on photosynthesis and an expanded understanding of this important process.