Alternative cytoskeletal landscapes: cytoskeletal novelty and evolution in basal excavate protists

Abstract

Microbial eukaryotes encompass the majority of eukaryotic evolutionary and cytoskeletal diversity. The cytoskeletal complexity observed in multicellular organisms appears to be an expansion of components present in genomes of diverse microbial eukaryotes such as the basal lineage of flagellates, the Excavata. Excavate protists have complex and diverse cytoskeletal architectures and life cycles-essentially alternative cytoskeletal 'landscapes'-yet still possess conserved microtubule-associated and actin-associated proteins. Comparative genomic analyses have revealed that a subset of excavates, however, lack many canonical actin-binding proteins central to actin cytoskeleton function in other eukaryotes. Overall, excavates possess numerous uncharacterized and 'hypothetical' genes, and may represent an undiscovered reservoir of novel cytoskeletal genes and cytoskeletal mechanisms. The continued development of molecular genetic tools in these complex microbial eukaryotes will undoubtedly contribute to our overall understanding of cytoskeletal diversity and evolution.

Figure 1. Evolutionary relationships of the Excavata

Diagram highlighting major groups within the Excavata [3-5] as well as major primary eukaryotic lineages: Opisthokonts (e.g., metazoans and fungi), Archaeplastida (e.g., plants), and groups composed primarily of protists (Amoebozoa, Chromalveolata, and Rhizaria). Representative images (right) of excavates and asterisks indicate those excavates with genomes discussed in this review. Scale bars = 1μm.

Figure 2. Cytoskeletal complexity of the Giardia ventral disc

Schematic of the Giardia microtubule cytoskeleton (A) indicating the median body (mb), the ventral disc (vdMTs) and supernumerary (snMTs) microtubule spiral arrays, the overlap zone (oz) of the vdMTs, the lateral crest (lc), the eight basal bodies (bb), and the four flagellar pairs – ventral flagella, vfl; caudal flagella, cfl; posteriolateral flagella, pfl; and anterior flagella, afl. Actin localizes primarily to the axonemes and the cell periphery. The detergent extracted cytoskeleton SEM (B) highlights the spiral vdMT array, and the lateral crest (lc) as viewed from the ventral side. Associated with the ventral plasma membrane (pm), the ventral disc microtubules (mt), trilaminar microribbons (mr) are seen in cross-section in the TEM (C), provided by Cindi Schwartz (CU-Boulder). Schematic representation of the ventral disc (D) shows the architecture of the primary elements of the ventral disc including the curved MTs with the associated microribbons (MR) and linked crossbridges (CB).