Exocytosis of the silicified cell wall of diatoms involves extensive membrane disintegration

Abstract

Diatoms are unicellular algae that are characterized by their silica cell walls. The silica elements form intracellularly in a membrane-bound organelle, and are exocytosed after completion. How diatoms maintain membrane homeostasis during the exocytosis of these large and rigid silica elements is a long-standing enigma. We studied membrane dynamics during cell wall formation and exocytosis in the diatom Stephanopyxis turris, using live-cell confocal microscopy and advanced electron microscopy. Our results provide detailed information on the ultrastructure and dynamics of the silicification process, showing that during cell wall formation, the organelle membranes tightly enclose the mineral phase, creating a precise mold of the delicate geometrical patterns. Surprisingly, during exocytosis of the mature silica elements, the proximal organelle membrane becomes the new plasma membrane, and the distal membranes gradually disintegrate into the extracellular space without any noticeable endocytic retrieval or extracellular repurposing. These observations suggest that diatoms evolved an extraordinary exocytosis mechanism in order to secrete their cell wall elements.

Enhancement of hemostatic properties of Cyclotella cryptica frustule through genetic manipulation

“…Recently, De Hann et al used live-cell confocal microscopy and advanced electron microscopy to observe the frustule assembly process for the rst time and con rmed that the frustule forms inside a membrane-bound compartment (Silica Deposition Vesicle, SDV) called the silicalemma. The authors also found that the silicalemma tightly surrounds the forming frustule during the whole silici cation process, suggesting an essential role of the silicalemma in frustule morphology [32]. Based on previous observations that the cytoskeleton plays an important role in shaping frustule, it can be speculated that silicalemma-spanning proteins mediate the interaction between the SDV and cytoskeleton [28, 29,33].…”

“…(2) only the proximal silicalemma SAPs were observed to interact with microtubules, whereas the distal silicalemma SAPs may interact with other cellular components or the original plasma membrane. De Hann et al discovered that the distal silicalemma is in very close proximity to the original plasma membrane, with a spacing distance of only 20 nm [32]. Such a con ned space is too narrow for microtubules to t into.…”

“…Nowadays, the facts that the formation of frustule occurs in SDV and the silicalemma spanning proteins play essential roles on frustule biogenesis by interaction with cytoskeleton or other cellular components are de nite [32,51], while several important questions are still open for discussion. Based on the results of this study and other related research reported recently, we further propose a assemble model of frustule biogenesis (Fig.…”

“…According to the results reported by De Hann et al, the mature silica valve is secreted outside by exocytosis, during which procedure the proximal silicalemma will fuse with the original plasma membrane generating the new plasma membrane, while the distal silicalemma will gradually disintegrate after exocytosis[32]. In addition, other two studies conducted byKotzsch et al and Tesson et al demonstrated that the C-terminal segments (cytoplasm domain) of silicalemma spanning proteins, will be cleaved off during biosilica formation[28,29].…”