Origins of Flagellar Gene Operons and Secondary Flagellar Systems

Abstract

Forty-one flagellated species representing 11 bacterial phyla were used to investigate the origin of secondary flagellar systems and the structure and formation of flagellar gene operons over the course of bacterial evolution. Secondary (i.e., lateral) flagellar systems, which are harbored by five of the proteobacterial species considered, originated twice, once in the alphaproteobacterial lineage and again in the common ancestor of the Beta-and Gammaproteobacteria. The order and organization of flagellar genes have undergone extensive shuffling and rearrangement among lineages, and based on the phylogenetic distributions of flagellar gene complexes, the flagellar gene operons existed as small, usually two-gene units in the ancestor of Bacteria and have expanded through the recruitment of new genes and fusion of gene units. In contrast to the evolutionary trend towards larger flagellar gene complexes, operon structures have been highly disrupted through gene disassociation and rearrangements in the Epsilon-and Alphaproteobacteria. These results demonstrate that the genetic basis of this ancient and structurally conserved organelle has been subject to many lineage-specific modifications.Bacterial flagella are complex organelles whose assembly is dependent on multiple cooperating components. In the wellstudied systems, those of Escherichia coli and Salmonella enterica serovar Typhimurium, approximately 50 genes, distributed in at least 10 operons, contribute to the formation, regulation, and function of the flagella (19,20). About one-half of these genes produce proteins that become part of the physical structure of flagella, whereas other genes have auxiliary or regulatory roles.Although the basic structure of the flagellum is fairly well conserved across bacteria, lineages can vary with respect to the number of flagella per cell and the location of flagella on the cell surface, as well as to the overall number of genes devoted to the synthesis and regulation of flagella (3,29). Among the more notable differences is the difference between the spirochetes, which possess periplasmic flagella whose filaments reside between the outer and cytoplasmic membranes, and other species whose filaments are situated outside the cells (8). In some bacteria, such as Vibrio parahaemolyticus, there are two flagellar systems (a polar system and a lateral system), which are encoded by distinct sets of genes and are responsible for different types of motility (22).The structure, assembly, and function of flagella have been characterized in some detail by molecular, genetic, and biophysical analyses (1,4,19,20,24,36); in contrast, relatively little is known about the evolutionary origins of the genes or gene clusters that specify these complex and diverse organelles (25). There is extensive similarity between flagellar genes and genes dedicated to protein secretion systems, leading to speculation that the flagellum arose from a primitive secretion system that was later adapted to cell motility (5,6,26,27). In addition, some of the fla...

Functional Characterization of EscK (Orf4), a Sorting Platform Component of the Enteropathogenic Escherichia coli Injectisome

“…Moreover, as previously suggested (68,72), it can be speculated that members of the SctK family are evolutionarily related to the flagellar FliG protein, given that its encoding gene is usually located between fliF (encoding an SctJ homolog) and fliH (encoding an SctL homolog) (73) and the fact that FliG interacts with the C-ring component FliM (an SctQ homolog), connecting the cytoplasmic ring to the flagellar basal body (44). Although in our Y2H screening we did not detect any interaction between EscK and a basal body T3SS component, we cannot rule out the possibility that EscK has a FliG-like function, aiding to dock the EscQ cytoplasmic ring to the injectisome base.…”

Structural basis for the molecular evolution of SRP-GTPase activation by protein

“…They always form a transcriptional unit with ylxH being the adjacent downstream open reading frame of flhF ( Supplementary Fig. 8a,b), which is remarkable considering the extensive rearrangements flagellar operons have undergone in evolution 37 . The absence of FlhF and YlxH in motile species most likely reflects the development of more recent regulatory systems, most notably in the -proteobacteria (see refs.…”

Transcriptional Control of the Lateral-Flagellar Genes of Bradyrhizobium diazoefficiens

“…Bradyrhizobium diazoefficiens, the soybean N 2 -fixing symbiont, is a soil alphaproteobacterium that possesses two different flagellar systems with independent evolutionary origins (19,20). One of these systems involves a subpolar flagellum closely related to the one in C. crescentus, while the other is characterized by lateral flagella similar to those in E. meliloti (20).…”