Role of the Cytoskeleton in Choanoflagellate Lorica Assembly

Abstract

Cell division in Acanthoeca spectabilis produces a "naked" motile daughter cell (juvenile) that settles onto a surface and deposits siliceous costal strips that are stored extracellularly in bundles. When complete, the bundles of strips are assembled in a single continuous movement to form a basket-like lorica. Assembly can be divided into four overlapping stages. Stage 1 entails the left-handed rotation of strips at the anterior end while the posterior end remains stationary. Stage 2 includes the posterior protrusion of the cell to form a stalk. Stage 3 involves the anterior extension of the spines, and Stage 4 the dilation of the lorica chamber and deposition of the organic investment. Scanning electron microscopic images reveal a one-to-one association between the moving bundles of strips and the anterior ring of lorica-assembling tentacles. Treatment with microtubule inhibitors produces "dwarf" cells that lack stalks, have their spines extended, and possess collars but lack flagella. Treatment with microfilament (actin) inhibitors prevents extension of the anterior spines. These experiments demonstrate that posterior cell extension is primarily mediated by microtubules whereas extension of the spines is controlled by the actin cytoskeleton. The processes of cytoskeletal rotation and extracellular costal strip movement are compared, respectively, with rotation of nuclei in animal embryos and movement of mammalian cells over surfaces.

Flow-Induced Crystallization of Collagen: A Potentially Critical Mechanism in Early Tissue Formation

“…1 The collagen motif arose in a premetazoan class of protists ( Choanoflagellata ), 2 known for their extracellular structures. 3 Thus, collagen has served as a structural molecule for approximately one billion years. Its amino acid composition has been tuned by retention of numerous, beneficial mutations, duplications, and substitutions 4 to permit entropy-driven fibril assembly.…”

Early evolution of eukaryote feeding modes, cell structural diversity, and classification of the protozoan phyla Loukozoa, Sulcozoa, and Choanozoa

“…The diversity of locomotory pseudopodial form in the walled aciliate Choanofila and their general nonresemblance to the long pointed pseudopodia of Paramycia or the ancestral Sulcozoa suggests that they evolved secondarily to help dispersal after the wall evolved and cilia were lost, and that the ancestral pointed choanozoan/sulcozoan filopodia were converted into non-locomotory filodigits in the common ancestor of all Choanofila. I use the term filodigit to indicate their finger like appearance and function; choanoflagellates use them for multifarious non-locomotory purposes: all use them for making the collar for filtering bacteria for subsequent engulfment by separate pseudopodia; those of order Craspedida also have posterior tentacles of unclear function (possibly attachment); those of order Acanthoecida use them like fingers to hold, manipulate, and move lorica components whilst building their siliceous lorica (Frösler and Leadbeater 2009;Leadbeater 2008;Leadbeater and Cheng 2010); Ministeria may use them for catching bacteria; Capsaspora uses its radiating tentacles for attachment to the substratum (Stibbs et al 1979) and apparently also for moving along by their extension and retraction, though the latter is not adequately described -it makes thicker pseudopodia for penetrating into schistosomes, killing and feeding on their cells (Owczarzak et al 1980). -Smith, 1998em.…”

The Origin of Animal Multicellularity and Cell Differentiation

“…The advantage of such a modular architecture in single-celled organisms might include modulating the total abundancy of a module (depending for example on environmental signals), ensuring stoichiometry between its components, or allowing regeneration of a given part of the cell. For example, choanoflagellates regenerate their flagellum after each division or when recovering from microtubule-depolymerizing treatment (Froesler and Leadbeater 2009). In the unicellular alga Chlamydomonas , flagellum regeneration involves a coordinated rise in flagellar gene transcription (Keller et al 1984) and investigation of promoter motifs suggests shared regulation of these flagellar genes by yet unidentified, specific transcription factors (Stolc et al 2005).…”