Anomalies in the valve morphogenesis of the centric diatom alga Aulacoseira islandica caused by microtubule inhibitors

Abstract

Of all unicellular organisms possessing a cell wall, diatoms are the most adept at micro- and nanoscale embellishment of their frustules. Elements of their cell walls are formed inside the cell under cytoskeletal control. In this work, we used laser scanning microscopy and electron microscopy to describe the major stages of cell wall formation in the centric diatom algae Aulacoseira islandica and to study the effect of various microtubule inhibitors on the morphogenesis of frustule elements. Our results show that colchicine inhibits karyokinesis and cytokinesis in A. islandica colonies. In contrast, valve morphogenesis is changed, rather than inhibited altogether. In normal cells, this process starts simultaneously in both daughter cells, beginning with the formation of two adjacent discs that later become valve faces and connecting spines. Under colchicine treatment, however, the cleavage furrow is blocked and a single lateral valve forms on the side of the cylindrical frustule. As a result, a single hollow pipe forms instead of two separate drinking glass-shaped frustules; such pipes can form up to 35% of all forming frustules. Colchicine inhibits the formation of connecting spines, whereas paclitaxel causes spines to form a complex, branching shape. At the same time, inhibitors do not affect the formation of areolae (openings) in the frustule. We discuss the possibility that various processes of the diatom frustule morphogenesis are controlled by two different mechanisms: membrane-related micromorphogenesis and cytoskeleton-mediated macromorphogenesis.

Revealing the static and dynamic nanomechanical properties of diatom frustules—Nature's glass lace

“…The cross-sectional view of a diatom frustule after FIB (Fig. 2b,c) demonstrates the multi-layered hierarchical structure of the cell wall, formed by orthosilicic acid in silica deposition vesicle 36,48 . The wall thickness is in the 0.3-1.5 µm range.…”

Looking back, looking forward: a review of the new literature on diatom teratological forms (2010–2020)

“…SDV are strictly associated to the cytoskeleton, which provides a rigid path for SDV expansion and defines the correct positioning of the components within the valve. It has been hypothesized that SDV are kept in position not only through microtubules connections, but also to the participation of transmembrane proteins called cingulins (Tesson et al, 2017;Bedoshvili et al, 2018). Valve morphogenesis is a complex process, which can be described as a combination of micro-and macromorphogenesis.…”

“…However, the role of cytoskeleton in the valve morphogenesis has been highlighted by many experiments conducted with microtubule inhibitors, which generally impede macromorphogenesis (Bedoshvili & Likhoshway, 2019). Cells treated with microtubule inhibitors, such as colchicine, showed abnormal ornamentation patterns, anomalies in the valve outline, curved or displaced raphe, and unusual raphe channel (see Bedoshvili et al, 2018;Bedoshvili & Likhoshway, 2019 and references within). Cytoskeleton inhibitors can also affect finer structures of the valve such as fultoportulae or areolae.…”

Molecular Evolution of Tubulins in Diatoms

“…Earlier studies have shown that this group of organisms expresses α-, β-, and γ-tubulins [ 8 , 47 , 48 , 49 ]. Exposure to microtubule inhibitors causes a variety of structural anomalies in diatom valves [ 50 , 51 , 52 , 53 , 54 , 55 , 56 , 57 , 58 , 59 ]. In other studies, tubulin has been shown to be involved during morphogenesis, and microtubules appear to form underlying layers during the formation of valves [ 60 , 61 ] and other specialized structures [ 56 , 57 ].…”

“…In other studies, tubulin has been shown to be involved during morphogenesis, and microtubules appear to form underlying layers during the formation of valves [ 60 , 61 ] and other specialized structures [ 56 , 57 ]. The role of microtubules is likely not limited to defining formations of structure; they are also likely to be involved in intracellular vesicular transport [ 50 , 62 , 63 ]. A hypothesis was put forward about the specific localization of aquaporins in silicalemma by MTs during the morphogenesis of silica structures [ 64 ].…”