A mutant in one of two exbD loci of a TonB system in Flavobacterium psychrophilum shows attenuated virulence and confers protection against cold water disease

Álvarez, Beatriz; Álvarez, Javier Fernández; Menéndez, Aurora; Guijarro, José A.

doi:10.1099/mic.0.2007/010900-0

Cited by 63 publications

(52 citation statements)

References 50 publications

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“…To our knowledge, only two reports have previously described two ExbD proteins encoded within the same TonB cluster in other Gram-negative microorganisms (43,44). In both cases, it was found that only one of the two ExbD proteins was involved in iron uptake functions, an observation that contrasts with our results showing that both exbD products are required for iron acquisition.…”

Section: Discussioncontrasting

confidence: 57%

Functional Features of TonB Energy Transduction Systems of Acinetobacter baumannii

et al. 2013

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Acinetobacter baumannii is an opportunistic pathogen that causes severe nosocomial infections. Strain ATCC 19606 T utilizes the siderophore acinetobactin to acquire iron under iron-limiting conditions encountered in the host. Accordingly, the genome of this strain has three tonB genes encoding proteins for energy transduction functions needed for the active transport of nutrients, including iron, through the outer membrane. Phylogenetic analysis indicates that these tonB genes, which are present in the genomes of all sequenced A. baumannii strains, were acquired from different sources. Two of these genes occur as components of tonB-exbB-exbD operons and one as a monocistronic copy; all are actively transcribed in ATCC 19606T . The abilities of components of these TonB systems to complement the growth defect of Escherichia coli W3110 mutants KP1344 (tonB) and RA1051 (exbBD) under iron-chelated conditions further support the roles of these TonB systems in iron acquisition. Mutagenesis analysis of ATCC 19606 T tonB 1 (subscripted numbers represent different copies of genes or proteins) and tonB 2 supports this hypothesis: their inactivation results in growth defects in iron-chelated media, without affecting acinetobactin biosynthesis or the production of the acinetobactin outer membrane receptor protein BauA. In vivo assays using Galleria mellonella show that each TonB protein is involved in, but not essential for, bacterial virulence in this infection model. Furthermore, we observed that TonB 2 plays a role in the ability of bacteria to bind to fibronectin and to adhere to A549 cells by uncharacterized mechanisms. Taken together, these results indicate that A. baumannii ATCC 19606 T produces three independent TonB proteins, which appear to provide the energy-transducing functions needed for iron acquisition and cellular processes that play a role in the virulence of this pathogen.

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Section: Discussioncontrasting

confidence: 57%

Functional Features of TonB Energy Transduction Systems of Acinetobacter baumannii

et al. 2013

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“…Some bacteria have more than one tonB or tonB-like gene, and in all cases, the connection between TonB-ExbBD and iron acquisition, when examined, has been clear (1,4,10,29,39,58,59,64,93,97,121,126,139). But recently, it has become apparent that some bacteria that contain an OM and IM, including L. pneumophila, and species of Chlamydia, Chlamydophila, Coxiella, Ehrlichia, Francisella, and Rickettsia do not have TonB-ExbBD (29,74).…”

Section: Discussionmentioning

confidence: 99%

Legionella pneumophila LbtU Acts as a Novel, TonB-Independent Receptor for the Legiobactin Siderophore

et al. 2011

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Gram-negative Legionella pneumophila produces a siderophore (legiobactin) that promotes lung infection. We previously determined that lbtA and lbtB are required for the synthesis and secretion of legiobactin. DNA sequence and reverse transcription-PCR (RT-PCR) analyses now reveal the presence of an iron-repressed gene (lbtU) directly upstream of the lbtAB-containing operon. In silico analysis predicted that LbtU is an outer membrane protein consisting of a 16-stranded transmembrane ␤-barrel, multiple extracellular domains, and short periplasmic tails. Immunoblot analysis of cell fractions confirmed an outer membrane location for LbtU. Although replicating normally in standard media, lbtU mutants, like lbtA mutants, were impaired for growth on iron-depleted agar media. While producing typical levels of legiobactin, lbtU mutants were unable to use supplied legiobactin to stimulate growth on iron-depleted media and displayed an inability to take up iron. Complemented lbtU mutants behaved as the wild type did. The lbtU mutants were also impaired for infection in a legiobactin-dependent manner. Together, these data indicate that LbtU is involved in the uptake of legiobactin and, based upon its location, is most likely the Legionella siderophore receptor. The sequence and predicted two-dimensional (2D) and 3D structures of LbtU were distinct from those of all known siderophore receptors, which generally contain a 22-stranded ␤-barrel and an extended N terminus that binds TonB in order to transduce energy from the inner membrane. This observation coupled with the fact that L. pneumophila does not encode TonB suggests that LbtU is a new type of receptor that participates in a form of iron uptake that is mechanistically distinct from the existing paradigm.

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“…As an important component of the iron uptake system, several TonB-dependent receptors were reported to have relevance in pathogen pathogenicity (Alvarez et al 2008, Tauseef et al 2011. In a comparative study of Flavobacterium columnare strains with high and low virulence, Li et al (2010) identified 3 tdr genes in the high virulence strain but not in the low virulence strain.…”

Section: Discussionmentioning

confidence: 99%

“…Binding of the Fe 3+ -siderophore complex triggers conformational change in the receptor, which induces the passage of the ligand (Braun 2006, Krewulak & Vogel 2011. As a result, TDRs are associated with bacterial pathogenicity in species such as Flavobacterium psychrophilum, Escherichia coli, Riemerella anatipestifer, and Neisseria meningitides (Alvarez et al 2008, Hagan & Mobley 2009, Tauseef et al 2011, Lu et al 2013. However, the potential importance of TDRs in pathogenic P. fluorescens remains largely unknown.…”

Section: Introductionmentioning

confidence: 99%

Identification and analysis of three virulence-associated TonB-dependent outer membrane receptors of Pseudomonas fluorescens

Zhang

Lu²,

Sun³

2014

Dis. Aquat. Org.

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Pseudomonas fluorescens is a Gram-negative bacterium that can infect a wide range of farmed fish. However, very little is known about the virulence mechanism of P. fluorescens as a fish pathogen. In this study, we identified and analyzed 3 TonB-dependent outer membrane receptors (TDRs) from a pathogenic P. fluorescens strain isolated from fish. In silico analysis revealed that all 3 proteins (named Tdr1 to 3) possess structural domains typical of TDRs. Quantitative real time RT-PCR analysis showed that tdr1, tdr2, and tdr3 expressions were upregulated under iron-depleted conditions. Compared to the wild type, mutants defective in tdr1, tdr2, and tdr3 were retarded in growth to different extents. Infection in a turbot Scophthalmus maximus model showed that all 3 mutants were impaired in their ability to desseminate into and colonize host tissues. In addition, the tdr1 and tdr3 mutants exhibited significantly reduced virulence. When used as subunit vaccines, purified recombinant proteins of Tdr1, Tdr2, and, in particular, Tdr3 elicited significant protection in turbot against lethal P. fluorescens challenge. The vaccinated fish produced specific serum antibodies, which, when incubated with P. fluorescens, blocked infection of P. fluorescens in fish cells. Together these results indicate that Tdr1, Tdr2, and Tdr3 are iron-regulated factors that participate in bacterial virulence and induce protective immunity as subunit vaccines.

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A mutant in one of two exbD loci of a TonB system in Flavobacterium psychrophilum shows attenuated virulence and confers protection against cold water disease

Cited by 63 publications

References 50 publications

Functional Features of TonB Energy Transduction Systems of Acinetobacter baumannii

Functional Features of TonB Energy Transduction Systems of Acinetobacter baumannii

Legionella pneumophila LbtU Acts as a Novel, TonB-Independent Receptor for the Legiobactin Siderophore

Identification and analysis of three virulence-associated TonB-dependent outer membrane receptors of Pseudomonas fluorescens

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