The major subunit of widespread competence (pseudo)pili exhibits a novel and conserved type IV pilin fold

Type IV filaments (Tff) - a superfamily of filamentous nanomachines virtually ubiquitous in prokaryotes - are helical assemblies of type IV pilins that mediate a wide variety of functions. The competence (Com) (pseudo)pilus is a widespread Tff mediating DNA uptake in bacteria with one membrane (monoderms), which is the first step in natural transformation, an important mechanism of horizontal gene transfer. Here, we report the genomic, phylogenetic and structural analysis of ComGC, the major pilin subunit of Com (pseudo)pili. By performing a global comparative analysis, we show that Com (pseudo)pili are virtually ubiquitous in Bacilli, a major monoderm class of Firmicutes, and ComGC displays extensive sequence conservation, defining a monophyletic group among type IV pilins. We also report two ComGC solution structures from two naturally competent human pathogens, Streptococcus sanguinis (ComGCSS) and Streptococcus pneumoniae (ComGCSP), revealing that this pilin displays extensive structural conservation. Strikingly, ComGCSS and ComGCSP exhibit a novel type IV pilin fold, which is purely helical. Modelling of ComGC packing into Tff confirms that its unusual structure is compatible with helical filament assembly. Owing to the widespread distribution of ComGC, these results have implications for hundreds of monoderm species.