Self-assembling enzymes and the origins of the cytoskeleton

Abstract

The bacterial cytoskeleton is composed of a complex and diverse group of proteins that self-assemble into linear filaments. These filaments support and organize cellular architecture and provide a dynamic network controlling transport and localization within the cell. Here, we review recent discoveries related to a newly appreciated class of self-assembling proteins that expand our view of the bacterial cytoskeleton and provide potential explanations for its evolutionary origins. Specifically, several types of metabolic enzymes can form structures similar to established cytoskeletal filaments and, in some cases, these structures have been repurposed for structural uses independent of their normal roles. The behaviors of these enzymes suggest that some modern cytoskeletal proteins may have evolved from dual-role proteins with catalytic and structural functions.

Figure 1

A table of the generalized mechanisms through which higher-order assembly may control enzymatic activity. In the first situation, the conformation of enzymes in filaments may stabilize or destabilize the active form. Second, the filament may assemble active sites in relation to one another such that they promote or inhibit substrate binding. Finally, filaments may make enzymes more or less likely to interact with accessory factors that control activity such as kinases or phosphatases.

Figure 2

A model of cytoskeletal evolution with modern examples of each step. The first event in this process is the evolution of self-assembly as an enzymatic regulatory mechanism. Polymerizing filaments can then be repurposed as dual-role enzymes with both enzymatic and structural functions (such as membrane association, shown here). Eventually dual-role enzymes may have diverged into cytoskeletal filaments that lost catalytic function (bottom) or active enzymes whose regulation by higher-order assembly was replaced by other regulatory mechanisms (top).