N. elongata Produces Type IV Pili That Mediate Interspecies Gene Transfer with N. gonorrhoeae

Higashi, Dustin L.; Biais, Nicolas; Weyand, Nathan J.; Agellon, Al; Sisko, Jennifer L.; Brown, Lewis M.; So, Magdalene

doi:10.1371/journal.pone.0021373

Cited by 35 publications

(45 citation statements)

References 48 publications

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“…The expression of BFP is associated with a distinctive pattern of three-dimensional clusters when incubated with cells, termed "localized adherence" (67), and the formation of dynamic autoaggregates of bacteria in liquid culture (3). T4Ps mediate diverse cellular processes in a broad range of bacteria, including adhesion and colonization (15,25,86), twitching and social motility (10,41), and horizontal gene transfer (5,36).…”

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confidence: 99%

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Outer Membrane Targeting, Ultrastructure, and Single Molecule Localization of the Enteropathogenic Escherichia coli Type IV Pilus Secretin BfpB

et al. 2012

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Type IV pili (T4P) are filamentous surface appendages required for tissue adherence, motility, aggregation, and transformation in a wide array of bacteria and archaea. The bundle-forming pilus (BFP) of enteropathogenic Escherichia coli (EPEC) is a prototypical T4P and confirmed virulence factor. T4P fibers are assembled by a complex biogenesis machine that extrudes pili through an outer membrane (OM) pore formed by the secretin protein. Secretins constitute a superfamily of proteins that assemble into multimers and support the transport of macromolecules by four evolutionarily ancient secretion systems: T4P, type II secretion, type III secretion, and phage assembly. Here, we determine that the lipoprotein transport pathway is not required for targeting the BfpB secretin protein of the EPEC T4P to the OM and describe the ultrastructure of the single particle averaged structures of the assembled complex by transmission electron microscopy. Furthermore, we use photoactivated localization microscopy to determine the distribution of single BfpB molecules fused to photoactivated mCherry. In contrast to findings in other T4P systems, we found that BFP components predominantly have an uneven distribution through the cell envelope and are only found at one or both poles in a minority of cells. In addition, we report that concurrent mutation of both the T4bP secretin and the retraction ATPase can result in viable cells and found that these cells display paradoxically low levels of cell envelope stress response activity. These results imply that secretins can direct their own targeting, have complex distributions and provide feedback information on the state of pilus biogenesis.

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“…Although T4Ps in Myxococcus xanthus and Pseudomonas aeruginosa have been shown by transmission electron microscopy (TEM) and fluorescence microscopy to exit the cell primarily at the pole (13,20,36,56), the case is much less clear for other T4Ps. Moreover, Cowles and Gitai (20) detected T4Ps with nonpolar origins in P. aeruginosa.…”

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Outer Membrane Targeting, Ultrastructure, and Single Molecule Localization of the Enteropathogenic Escherichia coli Type IV Pilus Secretin BfpB

et al. 2012

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“…Scanning electron microscopy was performed on AP2031 T cells as described by Higashi et al (2011). Biofilms formed by the rough variant were taller and contained multiple layers of cells (Fig.…”

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Isolation and characterization of Neisseria musculi sp. nov., from the wild house mouse

Weyand

Phifer‐Rixey

et al. 2016

International Journal of Systematic and Evolutionary Microbiology

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“…Cluster one isolates were closely related to N. macacae and human commensals N. sicca and N. mucosa. Cluster two isolates fall between the cluster one strains and N. elongata, a human commensal distantly related to human pathogens N. meningitidis and N. gonorrhoeae (4,11,18). These results suggest that multiple species of Neisseria colonize RMs.…”

Section: Rm Neisseria Encodes Orthologs Of Virulence Factors and Vaccinementioning

confidence: 99%

“…These species are highly related: >40% of the genes in pathogenic species are also present in commensals, and many of these encode virulence genes and antibiotic resistance alleles. The species are naturally competent and transfer genetic information to each other in vitro (3,4). HGT is widely assumed to play an important role in the spread of antibiotic resistance among pathogenic Neisseria; however, there is little information on the extent to which HGT occurs in vivo.…”

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Neisseria infection of rhesus macaques as a model to study colonization, transmission, persistence, and horizontal gene transfer

Weyand

Wertheimer

Hobbs

et al. 2013

Proc. Natl. Acad. Sci. U.S.A.

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The strict tropism of many pathogens for man hampers the development of animal models that recapitulate important microbehost interactions. We developed a rhesus macaque model for studying Neisseria-host interactions using Neisseria species indigenous to the animal. We report that Neisseria are common inhabitants of the rhesus macaque. Neisseria isolated from the rhesus macaque recolonize animals after laboratory passage, persist in the animals for at least 72 d, and are transmitted between animals. Neisseria are naturally competent and acquire genetic markers from each other in vivo, in the absence of selection, within 44 d after colonization. Neisseria macacae encodes orthologs of known or presumed virulence factors of human-adapted Neisseria, as well as current or candidate vaccine antigens. We conclude that the rhesus macaque model will allow studies of the molecular mechanisms of Neisseria colonization, transmission, persistence, and horizontal gene transfer. The model can potentially be developed further for preclinical testing of vaccine candidates.commensal Neisseria | nonhuman primate model | type IV pili M icrobe-host interactions are often refractory to investigation because of the exquisite tropism of many bacteria for the human host. Host-restriction has prevented the development of animal models that recapitulate colonization, transmission, and persistence; hampered studies of horizontal gene transfer (HGT); and prevented preclinical testing of vaccine candidates. One means to circumvent host restrictions is to develop an animal model of infection using a related species indigenous to that animal. For example, infections by human pathogens, such as Bordetella pertussis and Chlamydia trachomatis, have been effectively modeled in animals with Bordetella bronchiseptica and Chlamydia muridarum, respectively (1, 2).The genus Neisseria and the rhesus macaque provide us with this opportunity. Neisseria are Gram-negative, diplococcal β-Proteobacteria. This genus includes >10 human-adapted species, two of which are pathogens, and an unknown number of species that naturally colonize animals. These species are highly related: >40% of the genes in pathogenic species are also present in commensals, and many of these encode virulence genes and antibiotic resistance alleles. The species are naturally competent and transfer genetic information to each other in vitro (3, 4). HGT is widely assumed to play an important role in the spread of antibiotic resistance among pathogenic Neisseria; however, there is little information on the extent to which HGT occurs in vivo.Pathogens Neisseria meningitidis and Neisseria gonorrhoeae have an exquisite tropism for man. These pathogens do not naturally infect animals; inoculated into nonhuman hosts, the pathogens will colonize only for brief periods (5, 6). Neisseria species have been isolated from a number of animals (7-10), suggesting it may be possible to develop a model for studying Neisseria-host interactions in which there are no host-restriction barriers to overcome.The ...

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N. elongata Produces Type IV Pili That Mediate Interspecies Gene Transfer with N. gonorrhoeae

Cited by 35 publications

References 48 publications

Outer Membrane Targeting, Ultrastructure, and Single Molecule Localization of the Enteropathogenic Escherichia coli Type IV Pilus Secretin BfpB

Outer Membrane Targeting, Ultrastructure, and Single Molecule Localization of the Enteropathogenic Escherichia coli Type IV Pilus Secretin BfpB

Isolation and characterization of Neisseria musculi sp. nov., from the wild house mouse

Neisseria infection of rhesus macaques as a model to study colonization, transmission, persistence, and horizontal gene transfer

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