Functional Analysis of the Gonococcal Genetic Island of Neisseria gonorrhoeae

Pachulec, Emilia; Siewering, Katja; Bender, Tobias; Heller, Eva-Maria; Salgado-Pabón, Wilmara; Schmoller, Shelly K.; Woodhams, Katelynn L.; Dillard, Joseph P.; Does, Chris van der

doi:10.1371/journal.pone.0109613

Cited by 28 publications

(91 citation statements)

References 38 publications

(73 reference statements)

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“…For DNA-secreting gonococci, it was suggested that homologs of ParA and ParB might bind to DNA and bring it to the type IV secretion machinery (T4SS), where it is further processed by a relaxase and a helicase before it is secreted as ssDNA (58,59). Interestingly, deletion mutants of ParA or ParB in Neisseria gonorrhoeae indeed showed strongly reduced DNA secretion (60,61). We could therefore envision that Saci_1498 similarly brings the DNA to the putative transport machinery.…”

Section: Figmentioning

confidence: 99%

DNA Processing Proteins Involved in the UV-Induced Stress Response of Sulfolobales

Wolferen

Albers

2015

J Bacteriol

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The ups operon of Sulfolobus species is highly induced upon UV stress. Previous studies showed that the pili encoded by this operon are involved in cellular aggregation, which is essential for subsequent DNA exchange between cells, resulting in homologous recombination. The presence of this pilus system increases the fitness of Sulfolobus cells under UV light-induced stress conditions, as the transfer of DNA takes place in order to repair UV-induced DNA lesions via homologous recombination. Four conserved genes (saci_1497 to saci_1500) which encode proteins with putative DNA processing functions are present downstream of the ups operon. In this study, we show that after UV treatment the cellular aggregation of strains with saci_1497, saci_1498, and saci_1500 deletions is similar to that of wild-type strains; their survival rates, however, were reduced and similar to or lower than those of the pilus deletion strains, which could not aggregate anymore. DNA recombination assays indicated that saci_1498, encoding a ParB-like protein, plays an important role in DNA transfer. Moreover, biochemical analysis showed that the endonuclease III encoded by saci_1497 nicks UV-damaged DNA. In addition, RecQ-like helicase Saci_1500 is able to unwind homologous recombination intermediates, such as Holliday junctions. Interestingly, a saci_1500 deletion mutant was more sensitive to UV light but not to the replication-stalling agents hydroxyurea and methyl methanesulfonate, suggesting that Saci_1500 functions specifically in the UV damage pathway. Together these results suggest a role of Saci_1497 to Saci_1500 in the repair or transfer of DNA that takes place after UV-induced damage to the genomic DNA of Sulfolobus acidocaldarius. IMPORTANCESulfolobales species increase their fitness after UV stress by a UV-inducible pilus system that enables high rates of DNA exchange between cells. Downstream of the pilus operon, three genes that seem to play a role in the repair or transfer of the DNA between Sulfolobus cells were identified, and their possible functions are discussed. Next to the previously described role of UV-inducible pili in the exchange of DNA, we have thereby increased our knowledge of DNA transfer at the level of DNA processing. This paper therefore contributes to the overall understanding of the DNA exchange mechanism among Sulfolobales cells. In all domains of life, DNA repair is crucial for maintenance of genome integrity upon exposure to intra-or extracellular DNAdamaging threats (1). Unlike DNA repair in bacteria, archaeal DNA repair and its regulation are still far from well understood (1, 2). Homology searches revealed that the proteins in archaeal DNA repair pathways show similarities to both bacterial and eukaryotic proteins. In addition, DNA repair proteins with unique archaeal features exist (3).Previously, it was speculated that archaea might have SOS-like responses similar to those in certain bacteria (4); however, microarray studies revealed that neither Haloarchaea (5, 6) nor Sulfolobus species (7...

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Section: Figmentioning

confidence: 99%

DNA Processing Proteins Involved in the UV-Induced Stress Response of Sulfolobales

Wolferen

Albers

2015

J Bacteriol

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“…The majority of those genes are encoded within the first 27.5 kb of the GGI, the region between yaa and ych , from which many genes were shown to be essential for ssDNA secretion (Hamilton et al 2001, 2005; Pachulec et al 2014). The origin of transfer ( oriT ) was identified between the yaf and ltgX genes (Salgado-Pabón et al 2007).…”

Section: The Gonococcal Genetic Island (Ggi)mentioning

confidence: 99%

“…The exp1-difB region encodes at least 38 ORFs of which several show homology to DNA processing and modifying proteins, including SsbB, TopB, Yea, and CspA. However, most of the genes encode proteins with an unknown function, and only parA and parB encoded within the exp1-difB region are essential for ssDNA secretion (Hamilton et al 2005; Pachulec et al 2014). …”

Section: The Gonococcal Genetic Island (Ggi)mentioning

confidence: 99%

“…The yaa-ych region encodes mostly proteins that show homology with T4SS proteins (Hamilton et al 2005; Pachulec et al 2014). The ltgX-ych region encodes mainly proteins involved in the formation and stabilization of the mating pair complex and proteins involved in the assembly of the pilus (Hamilton et al 2005).…”

Section: Related Type IV Secretion Systemsmentioning

confidence: 99%

“…Close homologs of the TraA pilin and of TrbI, the protein that circularizes pilin subunits are not found in the F-plasmid, but are found in T4SSs that contain an MPF complex that belongs to the MPF T family (Eisenbrandt et al 1999; Hamilton et al 2005; Jain et al 2012). A functional analysis has shown that neither TraA and TrbI, nor Ybe, Ybi, Ycb, or Ych are essential for ssDNA secretion, but all proteins with homology to proteins encoded on the F-plasmid are essential (Hamilton et al 2001, 2005; Pachulec et al 2014). Remarkably, although not found in the F-plasmid, AtlA, Yag, and DsbC encoded in this region are required for DNA secretion (Hamilton et al 2001, 2005; Pachulec et al 2014).…”

Section: Related Type IV Secretion Systemsmentioning

confidence: 99%

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Secretion of Chromosomal DNA by the Neisseria gonorrhoeae Type IV Secretion System

Callaghan

Heilers

Does

et al. 2017

Current Topics in Microbiology and Immunology

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Approximately 80% of Neisseria gonorrhoeae and 17.5% of Neisseria meningitidis clinical isolates carry a ~59 kb genomic island known as the gonococcal genetic island (GGI). About half of the GGI consists of genes encoding a type IV secretion system (T4SS), and most of these genes are clustered in a ~28 kb region at one end of the GGI. Two additional genes (parA and parB) are found at the other end of the island. The remainder of the GGI consists mostly of hypothetical proteins, with several being identified as DNA binding or processing proteins. The T4SS genes show similarity to those of the F-plasmid family of conjugation systems, with similarity in gene order and a low but significant level of sequence identity for the encoded proteins. However, several GGI-encoded proteins are unique from the F-plasmid system, such as AtlA, Yag, and TraA. Interestingly, the gonococcal T4SS does not act as a conjugation system. Instead, this T4SS secretes ssDNA into the extracellular milieu, where it can serve to transform highly competent Neisseria species, thereby increasing the transfer of genetic information. Although many of the T4SS proteins are expressed at low levels, this system has been implicated in several cellular processes. The secreted ssDNA is involved in the initial stages of biofilm formation, and the presence of the T4SS enables TonB-independent intracellular survival of N. gonorrhoeae strains during infection of cervical cells. Other GGI-like T4SS have been identified in several other α-, β- and γ-Proteobacteria, but the function of these GGI-like T4SSs is unknown. Remarkably, the presence of the GGI is related to resistance to several antibiotics. Here we describe our current knowledge about the GGI and its unique ssDNA-secreting T4SS.

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Commensal Neisseria Kill Neisseria gonorrhoeae through a DNA-Dependent Mechanism

Kim

Higashi

Goytia

et al. 2019

Cell Host & Microbe

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Functional Analysis of the Gonococcal Genetic Island of Neisseria gonorrhoeae

Cited by 28 publications

References 38 publications

DNA Processing Proteins Involved in the UV-Induced Stress Response of Sulfolobales

DNA Processing Proteins Involved in the UV-Induced Stress Response of Sulfolobales

Secretion of Chromosomal DNA by the Neisseria gonorrhoeae Type IV Secretion System

Commensal Neisseria Kill Neisseria gonorrhoeae through a DNA-Dependent Mechanism

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