DNA transformation is a widespread process allowing bacteria to capture free DNA by using filamentous nano-machines composed of type IV pilins. These proteins can act as DNA receptors as demonstrated by the finding that Neisseria meningitidis ComP minor pilin has intrinsic DNA-binding ability. ComP binds DNA better when it contains the DNA-uptake sequence (DUS) motif abundant in this species genome, playing a role in its trademark ability to selectively take up its own DNA. Here, we report high-resolution structures for meningococcal ComP and Neisseria subflava ComPsub, which recognize different DUS motifs. We show that they are structurally identical type IV pilins that pack readily into filament models and display a unique DD region delimited by two disulfide bonds. Functional analysis of ComPsub defines a new mode of DNA binding involving the DD region, adapted for exported DNA receptors. Display omitted •ComP orthologs are type IV pilins binding DNA, key for natural transformation•Two high-resolution structures reveal a unique pilin fold•DNA binding involves a novel motif ComP is the first type IV pilin with DNA-binding ability, key for natural transformation in Neisseriaceae. By reporting high-resolution structures for two ComP orthologs, Berry et al. shed light on a novel mode of DNA binding.