Type II protein secretion and its relationship to bacterial type IV pili and archaeal flagella

Abstract

Homologues of the protein constituents of the Klebsiella pneumoniae (Klebsiella oxytoca) type II secreton (T2S), the Pseudomonas aeruginosa type IV pilus/fimbrium biogenesis machinery (T4P) and the Methanococcus voltae flagellum biogenesis machinery (Fla) have been identified. Known constituents of these systems include (1) a major prepilin (preflagellin), (2) several minor prepilins (preflagellins), (3) a prepilin (preflagellin) peptidase/methylase, (4) an ATPase, (5) a multispanning transmembrane (TM) protein, (6) an outer-membrane secretin (lacking in Fla) and (7) several functionally uncharacterized envelope proteins. Sequence and phylogenetic analyses led to the conclusion that, although many of the protein constituents are probably homologous, extensive sequence divergence during evolution clouds this homology so that a common ancestry can be established for all three types of systems for only two constituents, the ATPase and the TM protein. Sequence divergence of the individual T2S constituents has occurred at characteristic rates, apparently without shuffling of constituents between systems. The same is probably also true for the T4P and Fla systems. The family of ATPases is much larger than the family of TM proteins, and many ATPase homologues function in capacities unrelated to those considered here. Many phylogenetic clusters of the ATPases probably exhibit uniform function. Some of these have a corresponding TM protein homologue although others probably function without one. It is further shown that proteins that compose the different phylogenetic clusters in both the ATPase and the TM protein families exhibit unique structural characteristics that are of probable functional significance. The TM proteins are shown to have arisen by at least two dissimilar intragenic duplication events, one in the bacterial kingdom and one in the archaeal kingdom. The archaeal TM proteins are twice as large as the bacterial TM proteins, suggesting an oligomeric structure for the latter. OverviewThree related types of prokaryotic envelope protein complexes include (putative) prepilin proteins with highly similar hydrophobic N-terminal segments of approximately 20 amino acyl residues. These putative prepilins can assemble into filamentous structures which compose parts of (1) the type II secretion system (T2S), (2) the type IV piliation/fimbriation system (T4P) (both of Gramnegative bacteria) and (3) the flagellar system (Fla) of archaea. T2S, also called the type II secreton or the main terminal branch (MTB; TC #3.A.15) of the general secretory pathway (TC #3.A.5;Cao & Saier, 2003), represents the major pathway for exoprotein transport from the periplasm across the outer membrane in a wide variety of Gramnegative bacteria (Pugsley, 1993a). The type II secreton is composed of a core of around 12 proteins, some of which are not present in all type II secretons and others of which appear to be dispensable for secreton function Pugsley, 1993a;Sandkvist, 2001). In this review, secreton components will be referred to accordi...

Transposon Insertions ofmagellan-4That Impair Social Gliding Motility inMyxococcus xanthus

“…Although social motility appears to be a mechanism conserved among diverse Gram-negative bacteria, very few genetic determinants of this mechanism are conserved in sequence among the bacteria that display social (or ''twitching'') motility, M. xanthus and P. aeruginosa (Peabody et al 2003). The gene encoding glycogen phosphorylase (EC 2.4.1.1), which cleaves polysaccharides with a(1 / 4) glucan linkages, is conserved among M. xanthus, P. aeruginosa, and Haemophilus influenzae, which has been shown recently to display S motility (Bakaletz et al 2005).…”

Interaction domains in the Pseudomonas aeruginosa type II secretory apparatus component XcpS (GspF)

“…The ATPase XcpR (GspE) and the multispanning inner-membrane component XcpS (GspF) show considerable sequence similarity to PilB and PilC, respectively, which are both required for the formation of type IV pili (Peabody et al, 2003). This similarity suggests that XcpR and XcpS may play key roles in the assembly of the pilus-like structure formed by the pseudopilins.…”

Topology of the outer-membrane secretin PilQ from Neisseria meningitidis

“…Neisserial type IV pilus biogenesis represents one of the terminal branches of the type II secretion pathway (Pugsley, 1993), and it requires the complex interactions of 15 proteins (Carbonnelle et al, 2005;Tønjum & Koomey, 1997), which are similar, if not orthologous, to those involved in type II secretion in general (Nunn, 1999;Peabody et al, 2003;Pugsley, 1993). To initiate pilus assembly, the pilin subunit PilE, in its membrane bound state, is processed by the pre-pilin peptidase PilD, removing a short hydrophilic N-terminal peptide, and methylating the N-terminal amino acid (Nunn & Lory, 1991).…”