Polymorphism of the Cell Wall-Anchoring Domain of the Autolysin-Adhesin AtlE and Its Relationship to Sequence Type, as Revealed by Multilocus Sequence Typing of Invasive and Commensal Staphylococcus epidermidis Strains

Abstract

We sequenced the adhesin-cell wall-anchoring domain of the atlE gene of 49 invasive and commensal Staphylococcus epidermidis strains. We identified 22 alleles, which could be separated into two main groups: group 1 (alleles 1 and 6 to 16, 32/49 strains) and group 2 (alleles 2 to 5 and 17 to 22, 17/49 strains). Allele 1 (the type strain sequence) was by far the most prevalent (21 of 49 strains). Multilocus sequence typing showed a clear relationship between the atlE allele and the sequence type (ST), with the "nosocomial" ST27 clone and closely related STs expressing group 1 alleles.Staphylococcus epidermidis is a ubiquitous commensal organism of human skin and mucous membranes and is one of the main bacterial agents involved in infections related to the presence of indwelling or implanted foreign bodies (10). AtlE, encoded by the atlE gene (8), is thought to play a key role in the pathogenicity of this bacterium, enabling it to adhere to the surface of implanted medical devices (19). AtlE is a bifunctional autolysin with an N-terminal alanine amidase domain, a central cell wall-anchoring (CWA) domain consisting of three repeats (R1 to R3), each about 165 amino acids long, and a C-terminal glucosaminidase domain. It is secreted as a proenzyme and is cleaved between R2 and R3 at the surface of the bacterium, generating two separate enzymes: a 60-kDa alanine amidase containing R1 and R2 at its C terminus and a 52-kDa glucosaminidase containing R3 at its N terminus. The products of AtlE processing have been shown to have adhesive properties (8), probably involving domains R1, R2, and R3 (9).Other autolysins from gram-positive bacteria able to mediate bacterial adhesion via their CWA domains have been described. These adhesins-autolysins include Aas from Staphylococcus saprophyticus (9), AtlC from Staphylococcus caprae (1, 2), and Ami from Listeria monocytogenes (14). The staphylococcal adhesins-autolysins AtlE, Aas, and AtlC appear to have different adhesion patterns (1, 8, 9). For example, unlike Aas (9), AtlE mediates binding to vitronectin but not to fibronectin (8). Thus, the adhesion patterns mediated by adhesins-autolysins clearly differ between species within the genus Staphylococcus, probably because of differences in the CWA domains of these molecules. We recently showed that the structure and function of the CWA domain of the adhesin-autolysin Ami vary within L. monocytogenes (15). Thus, adhesins-autolysins may also display intraspecific polymorphism, resulting in differences in binding capacity between strains of the same species. To date, atlE has been sequenced in only a few strains (6,8,25). It is therefore unclear whether the CWA domain of AtlE displays polymorphism in invasive and commensal strains. We investigated this possibility by sequencing the DNA region encoding the CWA domain of AtlE (atlE cwa ) in a large panel of S. epidermidis strains.We studied a total of 49 S. epidermidis strains, including 27 clinical strains from 27 individuals (RPC99P332, RPC99P469, RPC99P756, RPC99P1232, RPC99P1478, ...

Type I Signal Peptidase and Protein Secretion inStaphylococcus epidermidis

“…We found that arylomycin C 16 inhibited the secretion of four peptidoglycan hydrolases: AtlE, the SsaA-like protein encoded by SERP0318, SERP2263, and IsaA, making this the major type of protein secreted by S. epidermidis. The autolysin-adhesin AtlE is the major autolysin of S. epidermidis, and it has a well-defined role in virulence (22,49,55) and is also thought to play a role in biofilm formation through its hydrophobicity (22) and its ability to bind various plasma and matrix proteins (22,23,43). The SsaA-like protein encoded by SERP0318 has a C-terminal cysteine-and histidine-dependent aminohydrolase/peptidase (CHAP) domain and two N-terminal LysM peptidoglycan binding domains, which are commonly associated with bacterial cell wall degradation.…”

Genetic Analysis of Glycopeptide-Resistant Staphylococcus epidermidis Strains from Bone and Joint Infections

“…We used both MLST (17)(18)(19) and multilocus variable-number tandem repeat analysis (MLVA) (20)(21)(22) to study S. epidermidis strains from BJIs. We found that the shift of these strains toward greater resistance to glycopeptides is a widespread phenomenon occurring in many STs rather than the result of the spread of a small number of GRSE strains.…”

Characterization of Staphylococcus caprae Clinical Isolates Involved in Human Bone and Joint Infections, Compared with Goat Mastitis Isolates

“…The hypothesis of a parallel but independent evolution of the two lineages is to be considered in accordance with previous studies (22). Compared with the S. epidermidis atlE gene, this gene may display polymorphism in invasive and commensal strains (28). According to our result for the S. caprae atlC gene, it is tempting to speculate that this marker may constitute a major colonization factor mediating the adhesion of bacteria to bone or medical devices and that it constitutes an alternative to screening to determine which population the isolate belongs to.…”