Novel Surface Structures Are Associated with the Adhesion of Actinobacillus actinomycetemcomitans to Collagen

Abstract

Actinobacillus actinomycetemcomitans is a gram-negative, facultative, anaerobic bacterium that colonizes the human oral cavity and the upper respiratory tract. This bacterium is strongly associated with localized aggressive periodontitis and adult periodontitis and is the causative agent for other serious systemic infections. Recently, we have identified a protein, EmaA (extracellular matrix protein adhesin A), that mediates the adhesion of A. actinomycetemcomitans to collagen. The conserved sequence and predicted secondary structure suggest that EmaA is an orthologue of the Yersinia enterocolitica adhesin YadA. Electron microscopy examinations of A. actinomycetemcomitans have identified antenna-like protrusions associated with the surface of the bacterium. These structures are absent on emaA mutant strains and can be restored by transformation of the mutant strain with emaA in trans. The loss of these structures is associated with a decrease in the binding of this bacterium to collagen. The antenna-like structures are composed of a long rod that terminates in an ellipsoidal head region. The analysis of these structures using image processing techniques has provided an initial estimate of the overall dimensions, which suggests that the appendages are oligomeric structures formed by either three or four subunits. Together, the data suggest that emaA is required for the expression of novel appendages on the surface of A. actinomycetemcomitans that mediate the adhesion of the bacterium to collagen.

Stick to Your Gums

“…EmaA is structurally distinct from the other two auto-transporters, with coiled-coil, glycosylated monomers trimerizing to form antenna-like protrusions on the bacterial cell surface. These comprise a stalk of approximately 150 nm that terminates in an ellipsoidal cap, within which the collagenbinding domain is located (Ruiz et al, 2006;Yu et al, 2008;Tang and Mintz, 2010). Specific amino acid residues within the stalk have been shown to introduce bends within the structure, conferring flexibility to ensure optimal adhesion to collagen (Yu et al, 2009).…”

Ultrastructural Analysis of the Rugose Cell Envelope of a Member of the Pasteurellaceae Family

“…However, the loss of the rugosity does not seem to influence the presentation of all virulence determinants on the outer bacterial surface. EmaA (extracellular matrix adhesin A), a trimeric autotransporter collagen binding adhesin that forms antenna-like appendages on the surface of the bacterium (13,22,30,31), is present in both wild-type and morC mutant strains, thus indicating that not all outer membrane transport systems are affected. All of these observations raise fundamental questions about the specific role of the outer membrane morphology and the spatial relationship between outer and inner membranes in bacteria with a native rugose phenotype.…”

“…Interestingly, a number of Gram-negative bacteria naturally show convoluted or rugose surfaces (22)(23)(24). This phenotype is most prominent in the Pasteurellaceae family, which includes Pasteurella multocida, Haemophilus influenzae, and the periodontal pathogen, Aggregatibacter actinomycetemcomitans (22). However, the function and physiological relevance of the membrane convolutions in the native state of these bacteria is unknown.…”

“…This treatment resulted in an originally smooth surface changing to a wrinkled or rugose phenotype (20). Interestingly, a number of Gram-negative bacteria naturally show convoluted or rugose surfaces (22)(23)(24). This phenotype is most prominent in the Pasteurellaceae family, which includes Pasteurella multocida, Haemophilus influenzae, and the periodontal pathogen, Aggregatibacter actinomycetemcomitans (22).…”

Structure Analysis of a Sugar-moiety Chimera of EmaA, a Collagen Adhesin of a Gram-negative Bacterial Pathogen

“…Multiple virulence factors are involved in the infective process, and EmaA (extracellular matrix adhesin A) is one of the important virulence determinants in the early stage of infection. EmaA is a trimeric autotransporter adhesin, composed of three 202 kDa monomers, and forms antenna-like appendages extending more than 150 nm from the bacterial surface [1]. The functional Nterminus, encompasses approximately 30 nm from the distal end, and comprises three subdomains (SI, SII and SIII), with a linker region between subdomains SII and SIII [2].…”