Trimeric autotransporter adhesins: variable structure, common function

Linke, Dirk; Rieß, Tanja; Autenrieth, Ingo B.; Lupas, Andrei N.; Kempf, Volkhard A. J.

doi:10.1016/j.tim.2006.04.005

Cited by 274 publications

(308 citation statements)

References 52 publications

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“…T4Ps are known to play central roles in host colonization for other proteobacterial taxa, including close relatives of Snodgrassella such as Neisseria meningitidis and N. gonorrheae, via surface adhesion and motility, and are thus fundamental to biofilm organization and attachment to the host epithelium (19). Two other major cell surface components, trimeric autotransporters and LPS O antigens, are also likely candidates for participation in adhesion, as well as in specific interactions with host receptors or evasion of host immune mechanisms (16,17). These latter functions may give rise to the observed host specificity of particular S. alvi strains to particular host species (14).…”

Section: Discussionmentioning

confidence: 99%

“…Two of the three trimeric autotransporter adhesin (TAA) genes in S. alvi, staA and staB, appear crucial for gut colonization. TAAs are a family of diverse, but structurally similar, adhesion factors that are widespread in bacteria, including human-associated Yersinia, Neisseria, and Bartonella (17). Consisting of a sticky head for adhering to host cells or extracellular matrices, and connected to the outer membrane by a lengthy stalk, these proteins are encoded by some of the largest S. alvi genes (∼10 kb).…”

Section: Significancementioning

confidence: 99%

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Genome-wide screen identifies host colonization determinants in a bacterial gut symbiont

Powell

Leonard

Kwong

et al. 2016

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

139

152

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Animal guts are often colonized by host-specialized bacterial species to the exclusion of other transient microorganisms, but the genetic basis of colonization ability is largely unknown. The bacterium Snodgrassella alvi is a dominant gut symbiont in honey bees, specialized in colonizing the hindgut epithelium. We developed methods for transposon-based mutagenesis in S. alvi and, using high-throughput DNA sequencing, screened genome-wide transposon insertion (Tnseq) and transcriptome (RNA-seq) libraries to characterize both the essential genome and the genes facilitating host colonization. Comparison of Tn-seq results from laboratory cultures and from monoinoculated worker bees reveal that 519 of 2,226 protein-coding genes in S. alvi are essential in culture, whereas 399 are not essential but are beneficial for gut colonization. Genes facilitating colonization fall into three broad functional categories: extracellular interactions, metabolism, and stress responses. Extracellular components with strong fitness benefits in vivo include trimeric autotransporter adhesins, O antigens, and type IV pili (T4P). Experiments with T4P mutants establish that T4P in S. alvi likely function in attachment and biofilm formation, with knockouts experiencing a competitive disadvantage in vivo. Metabolic processes promoting colonization include essential amino acid biosynthesis and iron acquisition pathways, implying nutrient scarcity within the hindgut environment. Mechanisms to deal with various stressors, such as for the repair of double-stranded DNA breaks and protein quality control, are also critical in vivo. This genome-wide study identifies numerous genetic networks underlying colonization by a gut commensal in its native host environment, including some known from more targeted studies in other hostmicrobe symbioses.type IV pilus | transposon mutagenesis | microbiota | symbiosis | Neisseriaceae

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Section: Discussionmentioning

confidence: 99%

Section: Significancementioning

confidence: 99%

Genome-wide screen identifies host colonization determinants in a bacterial gut symbiont

Powell

Leonard

Kwong

et al. 2016

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

139

152

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“…Bioinformatic analysis of BCAM0224 predicts that this protein is an orthologue of the surface-attached collagen-binding protein YadA from Yersinia species, the best characterized member of the TAAs (Tamm et al, 1993;Koretke et al, 2006). Other members of this class, namely NadA from Neisseria meningitidis (Comanducci et al, 2002), UspA-1 and -2 from Moraxella catarrhalis (Lafontaine et al, 2000) and BadA from Bartonella henselae (Riess et al, 2004) are important pathogenicity factors, playing critical roles in processes such as bacterial adherence, biofilm formation, serum resistance and invasion of host cells (Linke et al, 2006). They represent one of the major families of surfaceexposed proteins in Gram-negative bacteria and are organized in a modular fashion, i.e.…”

Section: Discussionmentioning

confidence: 99%

Genome-wide analysis of DNA repeats in Burkholderia cenocepacia J2315 identifies a novel adhesin-like gene unique to epidemic-associated strains of the ET-12 lineage

2010

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Members of the Burkholderia cepacia complex (Bcc) are respiratory pathogens in patients with cystic fibrosis (CF). Close repetitive DNA sequences often associate with surface antigens to promote genetic variability in pathogenic bacteria. The genome of Burkholderia cenocepacia J2315, a CF isolate belonging to the epidemic lineage Edinburgh-Toronto (ET-12), was analysed for the presence of close repetitive DNA sequences. Among the 422 DNA close repeats, 45 genes potentially involved in virulence were identified and grouped into 12 classes; of these, 13 genes were included in the antigens class. Two trimeric autotransporter adhesins (TAA) among the 13 putative antigens are absent from the other Burkholderia genomes and are clustered downstream of the cci island that is a marker for transmissible B. cenocepacia strains. This cluster contains four adhesins, one outer-membrane protein, one sensor histidine kinase and two transcriptional regulators. By using PCR, we analysed three genes among 47 Bcc isolates to determine whether the cluster was conserved. These three genes were present in the isolates of the ET-12 lineage but absent in all the other members. Furthermore, the BCAM0224 gene was exclusively detected in this epidemic lineage and may serve as a valuable new addition to the field of Bcc diagnostics. The BCAM0224 gene encodes a putative TAA that demonstrates adhesive properties to the extracellular matrix protein collagen type I. Quantitative real-time PCR analysis indicated that BCAM0224 gene expression occurred preferentially for cells grown under high osmolarity, oxygen-limited conditions and oxidative stress. Inactivation of BCAM0224 in B. cenocepacia attenuates the ability of the mutant to promote cell adherence in vitro and impairs the overall bacterial virulence against Galleria mellonella as a model of infection. Together, our data show that BCAM0224 from B. cenocepacia J2315 represents a new collagen-binding TAA with no bacterial orthologues which has an important role in cellular adhesion and virulence.

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“…Adhesion to host cells is a key event during the onset of infection; the mediators of this process, called adhesins, are a heterogeneous group of bacterial surface proteins, which vary in architecture, domain content, and mode of binding. One distinct class of adhesins are the trimeric autotransporter adhesins (TAAs) (2,3), also referred to as type Vc secretion systems (4). TAAs are important virulence factors of many well-studied pathogens: Examples include YadA of Yersinia enterocolitica, a species causing enteritis, mesenteric lymphadenitis, and reactive arthritis (5); NadA of Neisseria meningitidis (6), an agent of meningitis and sepsis; BadA of Bartonella henselae (7), which is the agent of cat scratch disease; UspA1 and A2 of Moraxella catarrhalis (8), a prominent species in respiratory tract infections, and Hia of Haemophilus influenza (9), an organism causing meningitis and respiratory tract infections.…”

mentioning

confidence: 99%

“…TAAs are important virulence factors of many well-studied pathogens: Examples include YadA of Yersinia enterocolitica, a species causing enteritis, mesenteric lymphadenitis, and reactive arthritis (5); NadA of Neisseria meningitidis (6), an agent of meningitis and sepsis; BadA of Bartonella henselae (7), which is the agent of cat scratch disease; UspA1 and A2 of Moraxella catarrhalis (8), a prominent species in respiratory tract infections, and Hia of Haemophilus influenza (9), an organism causing meningitis and respiratory tract infections. Despite their role in the context of unrelated diseases, these TAAs always fulfill similar functions-adhesion to host cells, autoagglutination, and biofilm formation (3).…”

mentioning

confidence: 99%

Complete fiber structures of complex trimeric autotransporter adhesins conserved in enterobacteria

Hartmann

Grin

Dunin-Horkawicz

et al. 2012

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

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Trimeric autotransporter adhesins (TAAs) are modular, highly repetitive surface proteins that mediate adhesion to host cells in a broad range of Gram-negative pathogens. Although their sizes may differ by more than one order of magnitude, they all follow the same basic head-stalk-anchor architecture, where the head mediates adhesion and autoagglutination, the stalk projects the head from the bacterial surface, and the anchor provides the export function and attaches the adhesin to the bacterial outer membrane after export is complete. In complex adhesins, head and stalk domains may alternate several times before the anchor is reached. Despite extensive sequence divergence, the structures of TAA domains are highly constrained, due to the tight interleaving of their constituent polypeptide chains. We have therefore taken a "domain dictionary" approach to characterize representatives for each domain type by X-ray crystallography and use these structures to reconstruct complete TAA fibers. With SadA from Salmonella enterica, EhaG from enteropathogenic Escherichia coli (EHEC), and UpaG from uropathogenic E. coli (UPEC), we present three representative structures of a complex adhesin that occur in a conserved genomic context in Enterobacteria and is essential in the infection process of uropathogenic E. coli. Our work proves the applicability of the dictionary approach to understanding the structure of a class of proteins that are otherwise poorly tractable by high-resolution methods and provides a basis for the rapid and detailed annotation of newly identified TAAs.coiled coil | β-layer

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Trimeric autotransporter adhesins: variable structure, common function

Cited by 274 publications

References 52 publications

Genome-wide screen identifies host colonization determinants in a bacterial gut symbiont

Genome-wide screen identifies host colonization determinants in a bacterial gut symbiont

Genome-wide analysis of DNA repeats in Burkholderia cenocepacia J2315 identifies a novel adhesin-like gene unique to epidemic-associated strains of the ET-12 lineage

Complete fiber structures of complex trimeric autotransporter adhesins conserved in enterobacteria

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