An Anomalous Type IV Secretion System in Rickettsia Is Evolutionarily Conserved

Gillespie, Joseph J.; Ammerman, Nicole C.; Dreher-Lesnick, Sheila M.; Rahman, M. Sayeedur; Worley, Micah J.; Setúbal, João Carlos; Sobral, Bruno W. S.; Azad, Abdu F.

doi:10.1371/journal.pone.0004833

Cited by 91 publications

(164 citation statements)

References 220 publications

(410 reference statements)

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“…In this context, it is intriguing that these pathogens often possess T4SS gene clusters bearing duplications of certain virB-like genes. Homologs of most of the VirB/ VirD4 genes were identified in all species of the Anaplasmataceae (Ehrlichia chaffeensis, Ehrlichia ruminantium, Anaplasma phagocytophilum, Anaplasma marginale, Wolbachia spp., Neorickettsia sennetsu) as well as the Rickettsiaceae (Rickettsia typhi, Rickettsia prowazekii, and Rickettsia conorii) (7,61,106,108,136,140,188,205,206).…”

Section: More Gram-negative Systemsmentioning

confidence: 99%

“…6, the T4SS genes generally cluster into two or three groups (95,106,136,207). One group codes for proteins resembling A. tumefaciens VirB3, VirB4, and VirB6.…”

Section: More Gram-negative Systemsmentioning

confidence: 99%

“…codes for several copies of VirB2 orthologs and VirB4 (Fig. 6) (106,199). In view of the proposed role for VirB4 in mediating the assembly of conjugative pili, the preservation of the virB2-virB4 gene arrangement suggests that these proteins might assemble as an antigenically variable surface organelle in intracellular bacteria either independently of or in conjunction with the other VirB subunits.…”

Section: More Gram-negative Systemsmentioning

confidence: 99%

“…For example, the Bartonella Trw system possesses tandem copies of VirB2-and VirB5-like genes and is thought to be specifically adapted for the production of antigenically variable pili through intergenic recombination (75). Among Rickettsia species, the presence of tandem virB2-like genes often adjacent to a virB4-like gene suggests that these organisms similarly display surface-variable pilin or pili as a result of recombination or differential gene expression (106). H. pylori does not encode multiple copies of pilin subunits but rather evolved a novel VirB5-like CagL subunit with an RGD motif (Fig.…”

Section: Evolution Of T4ss-associated Surface Structuresmentioning

confidence: 99%

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Biological Diversity of Prokaryotic Type IV Secretion Systems

Martı́nez

Christie

2009

Microbiol Mol Biol Rev

623

780

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SUMMARY Type IV secretion systems (T4SS) translocate DNA and protein substrates across prokaryotic cell envelopes generally by a mechanism requiring direct contact with a target cell. Three types of T4SS have been described: (i) conjugation systems, operationally defined as machines that translocate DNA substrates intercellularly by a contact-dependent process; (ii) effector translocator systems, functioning to deliver proteins or other macromolecules to eukaryotic target cells; and (iii) DNA release/uptake systems, which translocate DNA to or from the extracellular milieu. Studies of a few paradigmatic systems, notably the conjugation systems of plasmids F, R388, RP4, and pKM101 and the Agrobacterium tumefaciens VirB/VirD4 system, have supplied important insights into the structure, function, and mechanism of action of type IV secretion machines. Information on these systems is updated, with emphasis on recent exciting structural advances. An underappreciated feature of T4SS, most notably of the conjugation subfamily, is that they are widely distributed among many species of gram-negative and -positive bacteria, wall-less bacteria, and the Archaea. Conjugation-mediated lateral gene transfer has shaped the genomes of most if not all prokaryotes over evolutionary time and also contributed in the short term to the dissemination of antibiotic resistance and other virulence traits among medically important pathogens. How have these machines adapted to function across envelopes of distantly related microorganisms? A survey of T4SS functioning in phylogenetically diverse species highlights the biological complexity of these translocation systems and identifies common mechanistic themes as well as novel adaptations for specialized purposes relating to the modulation of the donor-target cell interaction.

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Section: More Gram-negative Systemsmentioning

confidence: 99%

“…6, the T4SS genes generally cluster into two or three groups (95,106,136,207). One group codes for proteins resembling A. tumefaciens VirB3, VirB4, and VirB6.…”

Section: More Gram-negative Systemsmentioning

confidence: 99%

Section: More Gram-negative Systemsmentioning

confidence: 99%

Section: Evolution Of T4ss-associated Surface Structuresmentioning

confidence: 99%

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Biological Diversity of Prokaryotic Type IV Secretion Systems

Martı́nez

Christie

2009

Microbiol Mol Biol Rev

623

780

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“…Default matrix parameters (BLOSUM62) and gap costs (existence, 11; extension, 1) were implemented, with an inclusion threshold of 0.005. The taxonomic distributions of blastp hits were graphically depicted as previously described (46). In some instances, all sequences within alignments were screened for possible signal peptides using SignalP v.3.0 (10) and LipoP v.1.0 (65) servers.…”

Section: Genome Reconstruction (I) Summarymentioning

confidence: 99%

A Rickettsia Genome Overrun by Mobile Genetic Elements Provides Insight into the Acquisition of Genes Characteristic of an Obligate Intracellular Lifestyle

et al. 2012

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We present the draft genome for the Rickettsia endosymbiont of Ixodes scapularis (REIS), a symbiont of the deer tick vector of Lyme disease in North America. Among Rickettsia species (Alphaproteobacteria: Rickettsiales), REIS has the largest genome sequenced to date (>2 Mb) and contains 2,309 genes across the chromosome and four plasmids (pREIS1 to pREIS4). The most remarkable finding within the REIS genome is the extraordinary proliferation of mobile genetic elements (MGEs), which contributes to a limited synteny with other Rickettsia genomes. In particular, an integrative conjugative element named RAGE (for Rickettsiales amplified genetic element), previously identified in scrub typhus rickettsiae (Orientia tsutsugamushi) genomes, is present on both the REIS chromosome and plasmids. Unlike the pseudogene-laden RAGEs of O. tsutsugamushi, REIS encodes nine conserved RAGEs that include F-like type IV secretion systems similar to that of the tra genes encoded in the Rickettsia bellii and R. massiliae genomes. An unparalleled abundance of encoded transposases (>650) relative to genome size, together with the RAGEs and other MGEs, comprise ϳ35% of the total genome, making REIS one of the most plastic and repetitive bacterial genomes sequenced to date. We present evidence that conserved rickettsial genes associated with an intracellular lifestyle were acquired via MGEs, especially the RAGE, through a continuum of genomic invasions. Robust phylogeny estimation suggests REIS is ancestral to the virulent spotted fever group of rickettsiae. As REIS is not known to invade vertebrate cells and has no known pathogenic effects on I. scapularis, its genome sequence provides insight on the origin of mechanisms of rickettsial pathogenicity.

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