Abstract
Biological cubic membranes (CM), which are fluid membranes draped onto the 3D periodic parallel surface geometries with cubic symmetry, have been observed within subcellular organelles, including mitochondria, endoplasmic reticulum, and thylakoids. CM transition tends to occur under various stress conditions; however, multilayer CM organizations often appear associated with light stress conditions. This report is about the characterization of a projected gyroid CM in a transmission electron microscopy study of the chloroplast membranes within green alga Zygnema (LB923) whose lamellar form of thylakoid membrane started to fold into multilayer gyroid CM in the culture at the end of log phase of cell growth. Using the techniques of computer simulation of transmission electron microscopy (TEM) and a direct template matching method, we show that these CM are based on the gyroid parallel surfaces. The single, double, and multilayer gyroid CM morphologies are observed in which space is continuously divided into two, three, and more subvolumes by either one, two, or several parallel membranes. The gyroid CM are continuous with varying amount of pseudo-grana with lamellar-like morphology. The relative amount and order of these two membrane morphologies seem to vary with the age of cell culture and are insensitive to ambient light condition. In addition, thylakoid gyroid CM continuously interpenetrates the pyrenoid body through stalk, bundle-like, morphologies. Inside the pyrenoid body, the membranes re-folded into gyroid CM. The appearance of these CM rearrangements due to the consequence of Zygnema cell response to various types of environmental stresses will be discussed. These stresses include nutrient limitation, temperature fluctuation, and ultraviolet (UV) exposure.
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References
Almsherqi ZA, Kohlwein SD, Deng Y (2006) Cubic membranes: a legend beyond the flatland of cell membrane organization. J Cell Biol 173:839–844
Almsherqi ZA, Landh T, Kohlwein SD, Deng Y (2009) Chapter 6 cubic membranes: the missing dimension of cell membrane organization. Int Rev Cell Mol Biol 274:275–341
Almsherqi Z, Margadant F, Deng Y (2012) A look through “lens” cubic mitochondria. Interface Focus 2:539–545
Angelova A, Angelov B, Mutafchieva R, Lesieur S (2015) Biocompatible mesoporous and soft nanoarchitectures. J Inorg Organomet Polym Mater 25:214–232
Angelov B, Angelova A, Vainio U, Garamus VM, Lesieur S, Willumeit R, Couvreur P (2009) Long-living intermediates during a lamellar to a diamond-cubic lipid phase transition: a small-angle X-ray scattering investigation. Langmuir 25:3734–3742
Angelov B, Angelova A, Drechsler M, Garamus VM, Mutafchieva R, Lesieur S (2015) Identification of large channels in cationic PEGylated cubosome nanoparticles by synchrotron radiation SAXS and Cryo-TEM imaging. Soft Matter 11:3686–3692
Berkaloff C (1967) Ultrastructural changes of the chloroplast thylakoids during the development of the encystment. J Microsc (France) 6:839–852
Chong K, Deng Y (2012) The three dimensionality of cell membranes: lamellar to cubic membrane transition as investigated by electron microscopy. Methods Cell Biol 108:317–343
De Rosier DJ, Klug A (1968) Reconstruction of three dimensional structures from electron micrographs. Nature 217:130–134
Deng Y, Almsherqi ZA (2015) Evolution of cubic membranes as antioxidant defence system. Interface Focus 5:20150012
Deng Y, Mieczkowski M (1998) Three-dimensional periodic cubic membrane structure mitochondria of amoeba Chaos carolinensis. Protoplasma 203:16–25
Gunning BES (1965) The greening process in Plast. 1. The structure of the prolamellar body. Protoplasma 60:111–130
Gunning BES (2001) Membrane geometry of ‘open’ prolamellar bodies. Protoplasma 215:4–15
Holzinger A, Roleda MY, Lütz C (2009) The vegetative arctic freshwater green alga Zygnema is insensitive to experimental UV exposure. Micron 40:831–838
Hyde S, Andersson S, Larsson K, Blum Z, Landh T, Lidi S, Ninham BW (1997) Cytomembranes and cubic membrane system revisited. In: The language of shape: the role of curvature in condensed matter: physics, chemistry and biology. Elsevier, Amsterdam, pp 257–338
Kowalewska Ł, Mazur R, Suski S, Garstka M, Mostowska A (2016) Three-dimensional visualization of the tubular-lamellar transformation of the internal plastid membrane network during runner bean chloroplast biogenesis. Plant Cell 28:875–891
Landh T (1995) From entangled membranes to eclectic morphologies: cubic membranes as subcellular space organizers. FEBS Lett 369:13–17
Landh T (1996) Cubic cell membrane architectures. Taking another look at membrane.bound cell spaces. PhD Thesis. Lund University, Sweden
McLean RJ, Pessoney GF (1970) A large quasi-crystalline lamellar lattice in chloroplasts of the green algae Zygnema. J Cell Biol 45:522–531
Selstam E, Schelin J, Williams W, Brain A (2007) Structural organization of prolamellar bodies (PLB) isolated from Zea mays. Parallel TEM, SAXS and absorption spectra measurements on samples subjected to freeze-thaw, reduced pH and high-salt perturbation. Biochim Biophys Acta 1768:2235–2245
Stamenković M, Woelken E, Hanelt D (2014) Ultrastructure of Cosmarium strains (Zygnematophyceae, Streptophyta) collected from various geographic locations shows specie-specific differences both at optimal and stress temperatures. Protoplasma 251:1491–1509
Starr RC, Zeikus JA (1993) UTEX- the cell culture collection of algae at the University of Texas at Austin. J Phycol 14:47–100
Unwin PNT, Henderson R (1975) Molecular structure determination by electron microscopy of unstained crystalline specimens. J Mol Biol 94:425–440
Williams WP, Selstam E, Brain T (1998) X-ray diffraction studies of the structural organization of prolamellar bodies isolated from Zea mays. FEBS Lett 422:252–254
Acknowledgments
We thank Tomas Landh for his help on the TEM image analysis and the insightful inputs for the discussion. We also thank Mark Mieczkowski for providing “Cubic Membrane Simulation Projection” program (QMSP). We also thank the Electron Microscopy Center at Wenzhou Medical University. This work is supported by grants from the National Natural Science Foundation, China (Grant No: 31670841) and Wenzhou Institute of Biomaterials and Engineering (Grant No: WIBEZD2015010-02) to Y.D.
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Zhan, T., Lv, W. & Deng, Y. Multilayer gyroid cubic membrane organization in green alga Zygnema . Protoplasma 254, 1923–1930 (2017). https://doi.org/10.1007/s00709-017-1083-2
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DOI: https://doi.org/10.1007/s00709-017-1083-2