Neisseria gonorrhoeae secretes chromosomal DNA via a novel type IV secretion system

Abstract

SummaryThe process of DNA donation for natural transformation of bacteria is poorly understood and has been assumed to involve bacterial cell death. Recently in Neisseria gonorrhoeae we found that mutations in three genes in the gonococcal genetic island (GGI) reduced the ability of a strain to act as a donor in transformation and to release DNA into the culture. To better characterize the GGI and the process of DNA donation, the 57 kb genetic island was cloned, sequenced and subjected to insertional mutagenesis. DNA sequencing revealed that the GGI has characteristics of a horizontally acquired genomic island and encodes homologues of type IV secretion system proteins. The GGI was found to be incorporated near the chromosomal replication terminus at the dif site, a sequence targeted by the site-specific recombinase XerCD. Using a plasmid carrying a small region of the GGI and the associated dif site, we demonstrated that this model island could be integrated at the dif site in strains not carrying the GGI and was spontaneously excised from that site. Also, we were able to delete the entire 57 kb region by transformation with DNA from a strain lacking the GGI. Thus the GGI was likely acquired and integrated into the gonococcal chromosome by site-specific recombination and may be lost by site-specific recombination or natural transformation. We made mutations in six putative type IV secretion system genes and assayed these strains for the ability to secrete DNA. Five of the mutations greatly reduced or completely eliminated DNA secretion. Our data indicate that N. gonorrhoeae secretes DNA via a specific process. Donated DNA may be used in natural transformation, contributing to antigenic variation and the spread of antibiotic resistance, and it may modulate the host immune response.

Phage-induced lysis enhances biofilm formation in Shewanella oneidensis MR-1

“…Species such as Neisseria are capable of active DNA export (Hamilton et al, 2005) and also DNA transport through vesiculation has been suggested (Whitchurch et al, 2002;Allesen-Holm et al, 2006). However, as opposed to active transport, several studies provide evidence that, in biofilms of many bacterial species, eDNA rather originates from the lysis of a cellular subpopulation.…”

Bacterial killing via a type IV secretion system

“…T4SSs are perhaps the most versatile of the macromolecular transport systems, being essential for host colonization by many medically important microbes [8][9][10][11][12][13] , the horizontal transfer of genetic material between bacteria and from bacteria to plants 2 as well as the special cases of the Helicobacter pylori DNA uptake 14 and Neisseria gonorrhoeae DNA release 15 systems. The prototypical T4SS is that of the plant pathogen Agrobacterium tumefaciens that uses its Vir system to cause tumours in most dicotyledonous species 16 .…”

FtsK translocation permits discrimination between an endogenous and an imported Xer/ dif recombination complex

“…Neisseria species contain an unusually long IMEX called the gonococcal genomic island (GGI) (8). In Neisseria gonorrheae, the GGI is 57 kb long and encodes a type IV secretion system that exports the chromosomal DNA of its host, rendering it available to neighboring cells for gene exchange by genetic transformation (8,18). The GGI carries a dif site, dif GGI , consisting of a XerC-binding site, a central region homologous to the Neisseria dif site, dif Ng , and a divergent XerD-binding site (Fig.…”