The role of TonB-dependent receptor TbdR1 in Riemerella anatipestifer in iron acquisition and virulence

Lu, Fengying; Miao, Shuang; Tu, Jing; Ni, Xintao; Xing, Linlin; Yu, Hui; Pan, Ling; Hu, Qinghai

doi:10.1016/j.vetmic.2013.08.020

Cited by 39 publications

(37 citation statements)

References 21 publications

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“…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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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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“…The TonB-dependent receptor TbdR1 (Riean_1607) has been found to be involved in heme acquisition in R. anatipestifer . The median lethal dose of a tbdR1 mutant was approximately 45-fold higher than the wild-type CH-3 strain [20]. Our group has confirmed the functions of TonB and the TonB complex and determined that the ExbB-ExbD-TonB complex is involved in heme uptake in ATCC11845 (unpublished data).…”

Section: Resultsmentioning

confidence: 89%

Comparative genomics of Riemerella anatipestifer reveals genetic diversity

et al. 2014

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BackgroundRiemerella anatipestifer is one of the most important pathogens of ducks. However, the molecular mechanisms of R. anatipestifer infection are poorly understood. In particular, the lack of genomic information from a variety of R. anatipestifer strains has proved severely limiting.ResultsIn this study, we present the complete genomes of two R. anatipestifer strains, RA-CH-1 (2,309,519 bp, Genbank accession CP003787) and RA-CH-2 (2,166,321 bp, Genbank accession CP004020). Both strains are from isolates taken from two different sick ducks in the SiChuang province of China. A comparative genomics approach was used to identify similarities and key differences between RA-CH-1 and RA-CH-2 and the previously sequenced strain RA-GD, a clinical isolate from GuangDong, China, and ATCC11845.ConclusionThe genomes of RA-CH-2 and RA-GD were extremely similar, while RA-CH-1 was significantly different than ATCC11845. RA-CH-1 is 140,000 bp larger than the three other strains and has 16 unique gene families. Evolutionary analysis shows that RA-CH-1 and RA-CH-2 are closed and in a branch with ATCC11845, while RA-GD is located in another branch. Additionally, the detection of several iron/heme-transport related proteins and motility mechanisms will be useful in elucidating factors important in pathogenicity. This information will allow a better understanding of the phenotype of different R. anatipestifer strains and molecular mechanisms of infection.

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“…anatipestifer remain mostly unknown. At present, OmpA [ 5 ], VapD [ 6 ], CAMP cohemolysin [ 7 ], TbdR1 [ 8 ] and siderophore-interacting protein (Sip) [ 9 ] have been identified as potential virulence factors. Among these, it was shown that the sip deletion mutant had significantly impaired iron uptake and reduced toxicity in ducklings compared to the wild type [ 9 ].…”

Section: Introductionmentioning

confidence: 99%

TonB Energy Transduction Systems of Riemerella anatipestifer Are Required for Iron and Hemin Utilization

et al. 2015

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Riemerella anatipestifer (R. anatipestifer) is one of the most important pathogens in ducks. The bacteria causes acute or chronic septicemia characterized by fibrinous pericarditis and meningitis. The R. anatipestifer genome encodes multiple iron/hemin-uptake systems that facilitate adaptation to iron-limited host environments. These systems include several TonB-dependent transporters and three TonB proteins responsible for energy transduction. These three tonB genes are present in all the R. anatipestifer genomes sequenced so far. Two of these genes are contained within the exbB-exbD-tonB1 and exbB-exbD-exbD-tonB2 operons. The third, tonB3, forms a monocistronic transcription unit. The inability to recover derivatives deleted for this gene suggests its product is essential for R. anatipestifer growth. Here, we show that deletion of tonB1 had no effect on hemin uptake of R. anatipestifer, though disruption of tonB2 strongly decreases hemin uptake, and disruption of both tonB1 and tonB2 abolishes the transport of exogenously added hemin. The ability of R. anatipestifer to grow on iron-depleted medium is decreased by tonB2 but not tonB1 disruption. When expressed in an E. coli model strain, the TonB1 complex, TonB2 complex, and TonB3 protein from R. anatipestifer cannot energize heterologous hemin transporters. Further, only the TonB1 complex can energize a R. anatipestifer hemin transporter when co-expressed in an E. coli model strain.

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The role of TonB-dependent receptor TbdR1 in Riemerella anatipestifer in iron acquisition and virulence

Cited by 39 publications

References 21 publications

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

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

Comparative genomics of Riemerella anatipestifer reveals genetic diversity

TonB Energy Transduction Systems of Riemerella anatipestifer Are Required for Iron and Hemin Utilization

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