Abstract
Natural transformation is the widespread biological process by which “competent” bacteria take up free DNA, incorporate it into their genomes, and become genetically altered or “transformed”. To curb often deleterious transformation by foreign DNA, several competent species preferentially take up their own DNA that contains specific DUS (DNA uptake sequence) watermarks. Our recent finding that ComP is the long sought DUS receptor in Neisseria species paves the way for the functional analysis of the DUS-ComP interdependence which is reported here. By abolishing/modulating ComP levels in Neisseria meningitidis, we show that the enhancement of transformation seen in the presence of DUS is entirely dependent on ComP, which also controls transformation in the absence of DUS. While peripheral bases in the DUS were found to be less important, inner bases are essential since single base mutations led to dramatically impaired interaction with ComP and transformation. Strikingly, naturally occurring DUS variants in the genomes of human Neisseria commensals differing from DUS by only one or two bases were found to be similarly impaired for transformation of N. meningitidis. By showing that ComPsub from the N. subflava commensal specifically binds its cognate DUS variant and mediates DUS-enhanced transformation when expressed in a comP mutant of N. meningitidis, we confirm that a similar mechanism is used by all Neisseria species to promote transformation by their own, or closely related DNA. Together, these findings shed new light on the molecular events involved in the earliest step in natural transformation, and reveal an elegant mechanism for modulating horizontal gene transfer between competent species sharing the same niche.
Highlights
Natural transformation is a widespread biological property shared by dozens of bacterial species which plays a key role in evolution by generating genetic diversity through horizontal gene transfer [1]
Meningococci protect themselves from uncontrolled transformation by foreign DNA by preferentially taking up their own DNA through specific recognition of motifs known as DUS (DNA uptake sequence) by the ComP receptor
We show here that (i) ComP controls transformation in the meningococcus both in the presence and in the absence of DUS, (ii) some bases of DUS are more important for recognition by ComP and transformation, (iii) DUS variants in other human Neisseria commensals are impaired for transformation of N. meningitidis, and (iv) ComP homologs in these commensals are able to bind their cognate DUS variant and mediate DUSspecific transformation
Summary
Natural transformation is a widespread biological property shared by dozens of bacterial species which plays a key role in evolution by generating genetic diversity through horizontal gene transfer [1]. The meningococcus acquires DNA mainly from other meningococci but there is ample evidence for horizontal gene transfer from other bacteria sharing the same ecological niche, i.e. the human nasopharynx, such as other Neisseria species [3] or Haemophilus species [4]. This astonishing genome plasticity is a key virulence property of N. meningitidis, which contributes markedly to its success as a pathogen [5]. Incoming DNA can be used as a template for the repair of DNA damage (when donor is identical), or as a source of food (when donor is too different) [8]
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