A Complete Set of Flagellar Genes Acquired by Horizontal Transfer Coexists with the Endogenous Flagellar System inRhodobacter sphaeroides

Abstract

Bacteria swim in liquid environments by means of a complex rotating structure known as the flagellum. Approximately 40 proteins are required for the assembly and functionality of this structure. Rhodobacter sphaeroides has two flagellar systems. One of these systems has been shown to be functional and is required for the synthesis of the well-characterized single subpolar flagellum, while the other was found only after the genome sequence of this bacterium was completed. In this work we found that the second flagellar system of R. sphaeroides can be expressed and produces a functional flagellum. In many bacteria with two flagellar systems, one is required for swimming, while the other allows movement in denser environments by producing a large number of flagella over the entire cell surface. In contrast, the second flagellar system of R. sphaeroides produces polar flagella that are required for swimming. Expression of the second set of flagellar genes seems to be positively regulated under anaerobic growth conditions. Phylogenic analysis suggests that the flagellar system that was initially characterized was in fact acquired by horizontal transfer from a ␥-proteobacterium, while the second flagellar system contains the native genes. Interestingly, other ␣-proteobacteria closely related to R. sphaeroides have also acquired a set of flagellar genes similar to the set found in R. sphaeroides, suggesting that a common ancestor received this gene cluster.The bacterial flagellum is a complex protein structure which consists of a long helical filament that is connected through a flexible linker known as the hook to an H ϩ -or Na ϩ -driven rotary motor (29). Rotation of the filament produces thrust that allows the cell to swim in liquid or semisolid medium (6). Bacteria perform taxis by controlling the frequency of reorientation, which is commonly regulated by a two-component signal transduction system that senses an environmental stimulus (2, 3, 7). Several reorientation mechanisms have been described for different bacteria (35). In Escherichia coli and Salmonella enterica serovar Typhimurium, in which the flagellar system has been studied more extensively, more than 40 proteins are required for flagellar synthesis and functioning (29). Expression of the flagellar genes is regulated in a hierarchical pattern which results from coordination of flagellar gene expression at the transcriptional or posttranscriptional level with one or more structural checkpoints in flagellum biogenesis (31). This tight regulation has probably evolved to avoid unnecessary synthesis of the large number of flagellar protein subunits required for this structure. The high energetic cost required for the synthesis and functioning of the flagellum is compensated for by the selective advantage conferred by motility. Accordingly, motility seems to be important in several processes, such as colonization, pathogenesis, dispersion, and competition for resources (37). When the growth medium is too dense to allow swimming, many bacteria differentiate in...

Genetic Determinants ofSilicibactersp. TM1040 Motility

“…2, is nearly identical to the fla2 locus of R. sphaeroides (Fig. 2B) (30). Recently, Poggio et al (30) noted the similarity of the R. sphaeroides fla2 locus to the While the overall structure and organization is similar, there are localized differences between the major flagellar loci of R. sphaeroides and TM1040.…”

“…2B) (30). Recently, Poggio et al (30) noted the similarity of the R. sphaeroides fla2 locus to the While the overall structure and organization is similar, there are localized differences between the major flagellar loci of R. sphaeroides and TM1040. The most striking example is the insertion of four genes (fliC3, flaF, flbT, and flgF2) in the 35.4-kb flagellar locus nestled between fliI and TM2975 (renamed flaI as shown in Fig.…”

A molecular brake, not a clutch, stops the Rhodobacter sphaeroides flagellar motor

“…Media were supplemented with 25 g/mL kanamycin and 1 mM IPTG (overnight induction) when using pIND4. Although the R. sphaeroides genome encodes 2 sets of fla genes (30), only the fla1 set has ever been observed under these conditions. Bead and Tethered Cell Assay.…”

Origins of Flagellar Gene Operons and Secondary Flagellar Systems

“…A recent study has shown that the alphaproteobacterium Rhodobacter sphaeroides contains two flagellar systems, which encode polar flagella (30). One of these systems is ancestral to Alphaproteobacteria, whereas the other is homologous to the primary system in Z. mobilis, which was shown previously to have originated by lateral gene transfer from Gammaproteobacteria (17).…”