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The peritrichous flagella of Rhizobium meliloti rotate only clockwise and control directional changes of swimming cells by modulating flagellar rotary speed. Using Tn5 insertions, we have identified and sequenced a motility (mot) operon containing three genes, motB, motC, and motD, that are translationally coupled. The motB gene (and an unlinked motA) has been assigned by similarity to the Escherichia coli and Bacillus subtilis homologs, whereas motC and motD are new and without known precedents in other bacteria. In-frame deletions introduced in motB, motC, or motD each result in paralysis. MotD function was fully restored by complementation with the wild-type motD gene. By contrast, deletions in motB or motC required the native combination of motB and motC in trans for restoring normal flagellar rotation, whereas complementation with motB or motC alone led to uncoordinated (jiggly) swimming. Similarly, a motB-motC gene fusion and a Tn5 insertion intervening between motB and motC resulted in jiggly swimming as a consequence of large fluctuations in flagellar rotary speed. We conclude that MotC biosynthesis requires coordinate expression of motB and motC and balanced amounts of the two gene products. The MotC polypeptide contains an N-terminal signal sequence for export, and Western blots have confirmed its location in the periplasm of the R. meliloti cell. A working model suggests that interactions between MotB and MotC at the periplasmic surface of the motor control the energy flux or the energy coupling that drives flagellar rotation.

Three genes of a motility operon and their role in flagellar rotary speed variation in Rhizobium meliloti