Stepwise formation of the bacterial flagellar system

Abstract

Elucidating the origins of complex biological structures has been one of the major challenges of evolutionary studies. The bacterial flagellum is a primary example of a complex apparatus whose origins and evolutionary history have proven difficult to reconstruct. The gene clusters encoding the components of the flagellum can include >50 genes, but these clusters vary greatly in their numbers and contents among bacterial phyla. To investigate how this diversity arose, we identified all homologs of all flagellar proteins encoded in the complete genome sequences of 41 flagellated species from 11 bacterial phyla. Based on the phylogenetic occurrence and histories of each of these proteins, we could distinguish an ancient core set of 24 structural genes that were present in the common ancestor to all Bacteria. Within a genome, many of these core genes show sequence similarity only to other flagellar core genes, indicating that they were derived from one another, and the relationships among these genes suggest the probable order in which the structural components of the bacterial flagellum arose. These results show that core components of the bacterial flagellum originated through the successive duplication and modification of a few, or perhaps even a single, precursor gene.

Type III secretion systems: the bacterial flagellum and the injectisome

“…However, early phylogenetic studies suggested that both systems share a common ancestor, and have since evolved differently from each other [55]. With the evergrowing number of genome sequences [56,57], it became clear that flagellar components are almost always encoded on the bacterial chromosome and co-evolved with the rest of the genome to a certain degree [58,59], while the genes coding for the injectisome are often encoded on virulence plasmids or pathogenicity islands, and are more closely related to each other than their flagellar counterparts. They are distributed independently of the phylogeny of the respective species, and have probably been frequently transferred between species [38,55,60].…”

Nematogalectin, a nematocyst protein with GlyXY and galectin domains, demonstrates nematocyte-specific alternative splicing in Hydra

“…Taken together, the results on nematogalectins and minicollagen-15 support the idea that the more complex nematocyst repertoire in medusozoans compared with anthozoans is attributable, in part, to a diversification of tubule proteins by tandem exon duplication. The bacterial flagellum and the eukaryotic cilium are similarly complex structures, which, like the nematocyst, appear to have evolved by a series of gene duplication events and associated sequence evolution to yield a variety of proteins from a limited number of starting domain motifs (31,32).…”

Break on through to the other side: outer membrane penetration of the nascent flagellum by a stop-polymerization mechanism: Figure 1.

“…Conservation of signaling events based on mechanical effects in seemingly diverse proteins could be extremely relevant considering the recent unveiling of evolutionary relationships between members of the core flagellum gene repertoire (Liu and Ochman 2007). Meta-genome and phylogenetic analyses indicate a gradual invention, starting from a single ancestral gene that duplicated and diversified (Liu and Ochman 2007). Addition of novel components allowed extension of the structure outward, eventually resulting in the extracellular flagellum.…”

“…Thus, it is conceivable that different stop-polymerization mechanisms act on distinct conformational states of a given protein to modulate the overall structure and, thus, impart specialized function on such protein assemblages. Conservation of signaling events based on mechanical effects in seemingly diverse proteins could be extremely relevant considering the recent unveiling of evolutionary relationships between members of the core flagellum gene repertoire (Liu and Ochman 2007). Meta-genome and phylogenetic analyses indicate a gradual invention, starting from a single ancestral gene that duplicated and diversified (Liu and Ochman 2007).…”

“…Yet, despite these deficiencies, the assembly program continues unabated and succeeds in forming the hook and the flagellar filament structures in the periplasm. Toward elucidating the molecular basis of these stop-polymerization effects, the FlgG* mutations were modeled onto the structure of the FlgE hook protein, which exhibits a high degree of sequence similarity to FlgG (Liu and Ochman 2007). This comparison indicated that most of the FlgG* mutations fall into exposed regions (one at the top and one at the bottom of the FlgE structural model), where two symmetrical FlgG-FlgG interfaces could interact.…”