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Multilayer gyroid cubic membrane organization in green alga Zygnema

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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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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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Correspondence to Yuru Deng.

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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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