How Did T3S Evolve?

The injectisome has a common evolutionary origin with the bacterial flagellum, as suggested by the fact that the basal bodies of both nanomachines are similar and include many proteins with a significant similarity. Moreover, there are also functional similarities, such as the use of specific chaperones (5, 45, 104, 108, 138) or of molecular systems regulating the size of the external appendage (the hook in the case of flagellum and the needle in the case of the injectisome) (93). Although the flagellum is a motility organelle with a rotary motor powered with the electron-motive force, it contains a built-in secretion apparatus that serves to export its own distal elements such as the hook and filament subunits before they polymerize. Interestingly enough, in some cases, the flagellum has been shown to secrete proteins that are not flagellar, showing that its secretion apparatus can easily be reassigned to pure secretory tasks (83, 85, 142). Like the flagellum, the injectisomes export their own distal components (needle subunits) before they secrete the substrates that represent their raison d’être. Thus the flagellum and the injectisome are evolutionarily related nanomachines sharing a common secretion apparatus and a similar assembly process. In the strictest sense, the secretion pathway that is common to the flagellum and injectisomes is called T3S. However, the term is often used to qualify the injectisome plus its substrates. Here we will refer to the injectisomes and their substrates as “nonflagellar T3S systems” (NFT3S). Since injectisomes are dedicated to trans-kingdom communication, they must have appeared after the first eukaryotes. In contrast, the urge to move toward nutrients in the primitive soup was a more basic need; hence injectisomes are likely to be derived from the flagellum. In phylogenetic studies (49, 56, 96), the flagellar components always cluster on a branch distinct from their homologs from the injectisomes, showing that no exchanges have occurred between the two systems since they diverged.