The Myxococcus xanthus pilQ(sglA) Gene Encodes a Secretin Homolog Required for Type IV Pilus Biogenesis, Social Motility, and Development

In response to starvation, the gram-negative bacterium Myxococcus xanthus initiates a multicellular developmental program that culminates in cells aggregating and forming a fruiting body (19). Within this structure vegetative cells differentiate into spores. This process depends on gliding motility. Gliding is controlled by two distinct genetic systems called adventurous (A)-motility and social (S)-motility (22). S-motility, but not A-motility, depends on polar type IV pili (58, 61). Most of the M. xanthus pil genes are homologous to type IV pil genes found in Pseudomonas aeruginosa and Neisseria gonorrhoeae, which are also required for a type of motility called twitching and for pathogenesis (33, 53). These pili may retract, as well as polymerize, and they may provide the force for movement by pushing and pulling cells (2, 53). Many type IV pil genes are homologous to type II secretion genes (general secretion pathway) (42). In the type IV system, pilin (PilA) is the only known secretion product (33). Pili and fibrils have been shown to mediate cohesion among cells and adhesion to substrates (4, 49, 61). Cohesive cells clump or aggregate in suspension, and their clumps stick to the walls of culture flasks. Native cultures of M. xanthus isolated from soil fail to suspend in liquid culture. To obtain dispersed growth in liquid medium, a spontaneous mutant which retained the ability to form fruiting bodies was isolated after continuous selection; it was named strain FB (15). This mutant of M. xanthus was amenable to necessary microbiological manipulations, such as dilutions, and as a result most laboratory strains were derived from strain FB. Later work showed that this mutation was in a social gliding motility gene, named sglA (22). Unlike other sgl mutations, the sglA1 mutant retains some S-motility and expresses pili at reduced levels, suggesting that sglA1 is a hypomorphic allele (23). Strains which carry sglA1 can form fruiting bodies on agar but not in submerged culture (27). This quality is associated with the decreased cohesiveness of sglA1 mutants, which consequently are unable to form a mat of cells (biofilm) within which fruiting bodies can develop. Strain DK1622 was constructed from strain FB; DK1622 is sglA+, fully S-motile, and capable of developing in submerged culture. Type IV pili are required by P. aeruginosa to form a biofilm (40), a process that resembles the formation of fruiting bodies (12). Here we report the mapping and cloning and the sequence of the sglA locus. SglA is found to belong to a large family of proteins called secretins (33), which include PilQ proteins from P. aeruginosa and N. gonorrhoeae. To indicate the molecular nature of sglA, we have changed its name to pilQ, as has been done for other sgl genes in M. xanthus when their functions were recognized. In-frame deletions in pilQ and its downstream gene orfL were constructed. pilQ is shown to be essential for the biogenesis of pili and for S-motility, while orfL is not. The origin of the pilQ+ DK1622 strain and the role of PilQ in M. xanthus are discussed.