Uptake of extracellular DNA: competence induced pili in natural transformation of Streptococcus pneumoniae

Abstract

Transport of DNA across bacterial membranes involves complex DNA uptake systems. In Gram-positive bacteria, the DNA uptake machinery shares fundamental similarities with type IV pili and type II secretion systems. Although dedicated pilus structures, such as type IV pili in Gram-negative bacteria, are necessary for efficient DNA uptake, the role of similar structures in Gram-positive bacteria is just beginning to emerge. Recently two essentially very different pilus structures composed of the same major pilin protein ComGC were proposed to be involved in transformation of the Gram-positive bacterium Streptococcus pneumoniae - one is a long, thin, type IV pilus-like fiber with DNA binding capacity and the other one is a pilus structure that was thicker, much shorter and not able to bind DNA. Here we discuss how competence induced pili, either by pilus retraction or by a transient pilus-related opening in the cell wall, may mediate DNA uptake in S. pneumoniae.

Keywords: Streptococcus pneumoniae; competence pilus; pneumococci; transformation.

Figure 1

Type IV pili in Neisseria meningitidis. Negatively stained transmission electron micrograph showing the characteristic morphology of type IV pili (courtesy of V. Pelicic).

Figure 2

Competence induced pili in S. pneumoniae. A: EM of a long type IV like pilus (white triangle) emanating from the surface of competent S. pneumoniae R6 (adapted from , reprint from www.plospathogen.org). B: Transformation pilus at higher magnification (adapted from , reprint from www.plospathogen.org). C, D: Short, plaited pili (white triangle) released from competent pneumococci strain T4R.

Figure 3

Retraction or trap model showing key components of the DNA uptake system in S. pneumoniae. A long type IV like transformation pilus is assembled on the surface of bacteria and directly binds exogenous DNA. Captured DNA is pulled through the cell wall by an unknown retraction ATPase (retraction model) to facilitate access of DNA to the DNA receptor ComEA and the transmembrane channel protein ComEC. Alternatively, the flexible pilus directly brings captured DNA in close proximity to cell surface receptors independent of a retraction ATPase (trap model). DsDNA is then cleaved by the EndA nuclease and ssDNA enters the cytoplasm through the ComEC pore.

Figure 4

Hole in the wall model. Upon competence induction a short and rigid pilus structure is assembled at the membrane protein ComGB with energy provided by the ComGA ATPase (Plug ON). The pilus is then rapidly shed from the bacteria, creating an opening through the peptidoglycan cell wall (Plug OFF). This channel facilitates access of exogenous DNA to the DNA receptor ComEA and the transmembrane channel protein ComEC. DsDNA is then cleaved by the endonuclease EndA and ssDNA enters the cytoplasm through the comEC pore.