Assembly of pili in Gram-positive bacteria

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Abstract

The formation of adhesive pili on the surface of Gram-negative bacteria has been studied in detail, whereas the pilus assembly pathways in Gram-positive bacteria remain to be characterized. Gram-positive microbes use the cell wall peptidoglycan as a surface organelle for the covalent attachment of proteins; a strategy that involves sorting signals of surface protein precursors and sortase, a transpeptidase that cleaves sorting signals and links the C-terminus of surface proteins via an amide bond to the peptidoglycan cross-bridge. Recent studies with Actinomyces naeslundii, Corynebacterium diphtheriae and Streptococcus parasanguis suggest that some sortase enzymes catalyze protein polymerization leading to the formation of pili on the surface of Gram-positive bacteria. Arthobacter photogonimos and Ruminococcus albus appear to use different strategies for pilus assembly, consistent with the notion that Gram-positive organisms, similar to Gram-negative bacteria, have evolved multiple molecular strategies for the formation of pili on microbial surfaces.

Section snippets

Assembly of surface proteins in Gram-positive bacteria

More than thirty years ago, Sjöquist and colleagues [16] presented the first evidence that Gram-positive bacterial surface proteins are anchored to the bacterial cell wall. The authors showed that protein A of Staphylococcus aureus could be released from the bacterial surface by treatment with lysostaphin [17]. This glycyl-glycine endopeptidase cleaves the pentaglycine cross-bridge of the staphylococcal cell wall and releases protein A as a fragment with uniform mass [17]. In contrast to

Streptococcal fimbriae

Streptococcal fimbriae were first reported in Streptococcus parasanguis, an organism that colonizes the oral cavity and tooth surface of people and animals [10]. Similar structures with a length of more than 0.6 μm and a diameter of 3–5 nm have been found in Streptococcus faecalis, Streptococcus salivarius and Streptococcus sanguis 11, 33, 34. Using S. parasanguis FW213 as a model system, it was shown that streptococcal fimbriae are composed of a major structural subunit Fap1 and a

Fimbriae of Actinomyces spp

The Gram-positive microbe Actinomyces is a human pathogen that can be isolated from supragingival dental plaque or the oral cavity [39]. These bacteria are the primary colonizers that initiate dental plaque and set the stage for the development of several infectious diseases, ranging from root surface caries and peridontitis to actinomycotic lesions [9]. Colonization of tooth or mucosal surfaces with Actinomyces spp. generates a biofilm substrate for the adherence of other plaque bacteria,

Assembly of Corynebacterium diphtheriae pili

The presence of pili has been reported in several species of corynebacterium, including C. diphtheriae, the causative agent of the human disease diphtheria [8]. C. diphtheriae pili are thin fiber-like structures, 0.2–3.0 μm in length and 2–6 nm in diameter. Surface organelles, such as pili or fimbriae, have been proposed to aid in the adherence of C. diphtheriae to human pharyngeal tissues [55]. Recently, a mechanism for pilus assembly in corynebacteria was described [15]. A search for sortase

Assembly of pili in other Gram-positive bacteria

Ruminococcus albus colonizes the stomach of ruminating animals in a symbiotic relationship, during which bacterial enzymes degrade cellulose of plant cell wall extracts to produce carbohydrate nutrients for both the host and microbe. R. albus and several other closely related microbes bind to cellulose and have been presumed to display cellulosome-like complexes on their bacterial surface, similar to that of the soil-dwelling organism Clostridium thermocellum 57, 58. Further examination of the

Concluding remarks

Adhesive interactions of bacteria with host cells lead to the establishment of commensal or pathogenic relationships. Adhesion of bacteria to host tissues involves several bacterial surface organelles, including pili or fimbriae [6]. The assembly of these structures in Gram-positive bacteria requires sortase, a transpeptidase that cleaves the protein precursors at the LPXTG motif and performs an amide bond exchange between the pilin motif and the sorting signal 14, 15. This mechanism can

Acknowledgements

We thank Luciano Marraffini, Kumaran Ramamurthi and Eric Skaar for critical review of the manuscript and discussion. This work was supported by grants from the United States Public Health Service and the National Institute of Allergy and Infectious Diseases, Infectious Disease Branch, awards AI38897 and AI52474, to Olaf Schneewind.

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