Bacterial Pili and Fimbriae

Abstract

Bacterial proteinaceous filaments termed pili or fimbriae are nonflagellar, hair‐like structures protruding from the cell surface that are critical for bacterial virulence and fitness. Present in both Gram‐negative and Gram‐positive bacteria, pili are involved in many processes such as conjugation, adherence, twitching motility, biofilm formation and immunomodulation. Considerably diverse and complex, Gram‐negative pili are formed by noncovalent polymerisation of various pilin subunits; many of these pili require chaperones and usher proteins for their assembly. In contrast, fewer pilus systems have been described for the Gram‐positive counterparts; notably well studied are the heterotrimeric or ‐dimeric pili that are covalently assembled by a transpeptidase enzyme called sortase. Here we review the current knowledge of assembly pathways, structure and function of these pili in Gram‐negative and Gram‐positive pathogens.

Key Concepts:

  • Noncovalent pilus polymerisation is a general mechanism of pilus assembly in Gram‐negative bacteria, including the chaperon‐usher assembly pathway and type IV pilus pathway, which generates noncovalent pilus polymers.

  • Sortase‐mediated pilus assembly is a general mechanism of pilus assembly in Gram‐positive bacteria that involves a transpeptidase enzyme named sortase, which cleaves pilin precursors at sorting signals between threonine and glycine and involve the side‐chain amino groups of pilin motif sequences to generate covalent links between pilin subunits.

  • The sorting signal is consisted of an LPXTG motif followed by a hydrophobic domain and a positively charged tail.

  • The pilin motif is an 11 amino acid sequence of WxxxVxVYPKN located near the N‐terminus of major pilin subunits, in which the electron donating lysine residue forms an isopeptide bond with the threonine residue generated from the cleavage of the LPXTG motif of adjacent pilin subunits.

  • Tissue tropism is referred to as the ability of a pathogen to adhere specifically to some particular epithelial cells.

  • Phase variation involves switching of surface antigens such as pili that allows a pathogen to evade the host immune system.

  • Immunomodulation is a process of changing the host's immune system by certain molecules known as immunomodulators including pili that can activate or suppress immune cells.

  • Dental plaque is one of the most complex bacterial biofilms that is formed by sequential colonisation of initial colonisers such as Actinomyces spp. and oral streptococci and late colonisers; this process involves Actinomyces fimbriae.

  • Twitching motility mediated by pili allows translocation between mucosal surfaces, colonisation of host tissues and establishment of biofilms by a pathogen.

Keywords: pili; fimbriae; adhesion; polymerisation; sortase

Figure 1.

Assembly mechanisms of Gram‐negative pili. Examples are P pili assembled by the chaperone‐usher pathway (reproduced with permission from Li and Thanassi, ; Thanassi and Hultgren, ) and type IV pili (reproduced with permission from Mattick, ). P subunits (PapA, E, F, G, H, K) are translocated across the cytoplasmic membrane by the Sec machinery and they interact sequentially with the periplasmic disulfide isomerase DsbA and the chaperone PapD. DsbA mediates disulfide bond formation in the subunits and PapD, and it is required for the correct folding of PapD. PapD is needed for the release of subunits from the cytoplasmic membrane and for the proper folding of the subunits via donor strain complementation. In the absence of PapD, subunits enter into nonproductive aggregations that are sensed by the Cpx and σE signal transduction pathways (not shown). Chaperone–subunit complexes are targeted to PapC in the outer membrane, where subunit–subunit interactions lead to the formation and translocation of a linear pilus fibre across the outer membrane through the usher channel. Once on the cell surface, the pilus rod can twist into its final helical conformation, which may facilitate secretion of the pilus. For the assembly and retraction of type IV pili, prepilin leader sequences are cleaved and N‐methylated by prepilin peptidasePilD. PilA is assembled on a base of PilE, V, W, X and FimU by the cytoplasmic membrane protein PilC and the NTP‐binding protein PilB. The pilus grows through the outer membrane pore composed of multimeric PilQ, which is stabilised by the lipoprotein PilP. Pili are retracted by ATPase PilT that is aided by PilU.

Figure 2.

A biphasic model of sortase‐mediated pilus assembly in Gram‐positive bacteria with the prototype SpaA pili of Corynebacterium diphtheriae. Spa pilin precursors (SpaA, SpaB and SpaC) are translocated across the membrane by the Sec machinery with the removal of their leader peptide sequences. The cleaved pilins are anchored to the cytoplasmic membrane by the sorting signal, which is compromised of an LPXTG sequence motif, followed by a hydrophobic domain and tail of positively charged residues (+). Sortases cleave the LPXTG motif between threonine and glycine, forming acyl–enzyme intermediates with the pilin substrates. Pilus polymerisation occurs by lysine‐mediated transpeptidation reactions catalysed by pilus‐specific sortase. This polymerisation is terminated when SpaB is attached to the pilus base by the housekeeping sortase. The housekeeping sortase catalyses cell wall anchoring of pilus polymers. Reproduced with permission from Mandlik et al. . Copyright 2008 National Academy of Sciences, USA.

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References

Abbot EL, Smith WD, Siou GP et al. (2007) Pili mediate specific adhesion of Streptococcus pyogenes to human tonsil and skin. Cell Microbiology 9(7): 1822–1833.

Aguiar SI, Serrano I, Pinto FR, Melo‐Cristino J and Ramirez M (2008) The presence of the pilus locus is a clonal property among pneumococcal invasive isolates. BMC Microbiology 8: 41.

Bagnoli F, Moschioni M, Donati C et al. (2008) A second pilus type in Streptococcus pneumoniae is prevalent in emerging serotypes and mediates adhesion to host cells. Journal of Bacteriology 190(15): 5480–5492.

Barnhart MM and Chapman MR (2006) Curli biogenesis and function. Annual Review of Microbiology 60: 131–147.

Barocchi MA, Ries J, Zogaj X et al. (2006) A pneumococcal pilus influences virulence and host inflammatory responses. Proceedings of the National Academy of Sciences of the U S A 103(8): 2857–2862.

Beachey EH (1981) Bacterial adherence: adhesin‐receptor interactions mediating the attachment of bacteria to mucosal surface. Journal of Infectious Diseases 143(3): 325–345.

Brinton CC Jr (1965) The structure, function, synthesis and genetic control of bacterial pili and a molecular model for DNA and RNA transport in Gram‐negative bacteria. Transactions of the New York Academy of Sciences 27(8): 1003–1054.

Budzik JM, Marraffini LA and Schneewind O (2007) Assembly of pili on the surface of Bacillus cereus vegetative cells. Molecular Microbiology 66(2): 495–510.

Cobo Molinos A, Abriouel H, Omar NB, Lopez RL and Galvez A (2008) Detection of ebp (endocarditis‐ and biofilm‐associated pilus) genes in enterococcal isolates from clinical and non‐clinical origin. International Journal of Food Microbiology 126(1–2): 123–126.

Coureuil M, Mikaty G, Miller F et al. (2009) Meningococcal type IV pili recruit the polarity complex to cross the brain endothelium. Science 325(5936): 83–87.

Duguid JP, Smith IW, Dempster G and Edmunds PN (1955) Non‐flagellar filamentous appendages (fimbriae) and haemagglutinating activity in Bacterium coli. Journal of Pathology and Bacteriology 70(2): 335–348.

Falugi F, Zingaretti C, Pinto V et al. (2008) Sequence variation in group A Streptococcus pili and association of pilus backbone types with lancefield T serotypes. Journal of Infectious Diseases 198(12): 1834–1841.

Girard AE and Jacius BH (1974) Ultrastructure of Actinomyces viscosus and Actinomyces naeslundii. Archives of Oral Biology 19(1): 71–79.

Henderson IR, Owen P and Nataro JP (1999) Molecular switches: the ON and OFF of bacterial phase variation. Molecular Microbiology 33(5): 919–932.

Ippen‐Ihler KA and Minkley EG Jr (1986) The conjugation system of F, the fertility factor of E. coli. Annual Review of Genetics 20: 593–624.

Kang HJ, Coulibaly F, Clow F, Proft T and Baker EN (2007) Stabilizing isopeptide bonds revealed in Gram‐positive bacterial pilus structure. Science 318(5856): 1625–1628.

Krishnan V, Gaspar AH, Ye N et al. (2007) An IgG‐like domain in the minor pilin GBS52 of Streptococcus agalactiae mediates lung epithelial cell adhesion. Structure 15(8): 893–903.

Lancefield RC and Dole VP (1946) The properties of T antigens extracted from group A hemolytic streptococci. Journal of Experimental Medicine 84: 449–471.

Li H and Thanassi DG (2009) Use of a combined cryo‐EM and X‐ray crystallography approach to reveal molecular details of bacterial pilus assembly by the chaperone/usher pathway. Current Opinion in Microbiology 12(3): 326–332.

Maisey HC, Hensler M, Nizet V and Doran KS (2007) Group B streptococcal pilus proteins contribute to adherence to and invasion of brain microvascular endothelial cells. Journal of Bacteriology 189(4): 1464–1467.

Mandlik A, Das A and Ton‐That H (2008a) The molecular switch that activates the cell wall anchoring step of pilus assembly in Gram‐positive bacteria. Proceedings of the National Academy of Sciences of the USA 105(37): 14147–14152.

Mandlik A, Swierczynski A, Das A and Ton‐That H (2008b) Pili in Gram‐positive bacteria: assembly, involvement in colonization and biofilm development. Trends in Microbiology 16(1): 33–40.

Manetti AG, Zingaretti C, Falugi F et al. (2007) Streptococcus pyogenes pili promote pharyngeal cell adhesion and biofilm formation. Molecular Microbiology 64(4): 968–983.

Margarit I, Rinaudo CD, Galeotti CL et al. (2009) Preventing bacterial infections with pilus‐based vaccines: the group B streptococcus paradigm. Journal of Infectious Diseases 199(1): 108–115.

Marraffini LA, Dedent AC and Schneewind O (2006) Sortases and the art of anchoring proteins to the envelopes of Gram‐positive bacteria. Microbiology and Molecular Biology Reviews 70(1): 192–221.

Mattick JS (2002) Type IV pili and twitching motility. Annual Review of Microbiology 56: 289–314.

Merz AJ, So M and Sheetz MP (2000) Pilus retraction powers bacterial twitching motility. Nature 407(6800): 98–102.

Milgotina E and Donnenberg MS (2009) The bundle‐forming pilus and other type IVb pili. In: Jarrell KF (ed.) Pili and Flagella, Chapter 3, pp. 41–57. Norfolk, UK: Caister Academic Press.

Mishra A, Das A, Cisar JO and Ton‐That H (2007) Sortase‐catalyzed assembly of distinct heteromeric himbriae in Actinomyces naeslundii. Journal of Bacteriology 189(8): 3156–3165.

Nallapareddy SR, Singh KV, Sillanpaa J et al. (2006) Endocarditis and biofilm‐associated pili of Enterococcus faecalis. Journal of Clinical Investigation 116(10): 2799–2807.

Naumann M, Rudel T and Meyer TF (1999) Host cell interactions and signalling with Neisseria gonorrhoeae. Current Opinion in Microbiology 2(1): 62–70.

Newman JV, Burghoff RL, Pallesen L et al. (1994) Stimulation of E. coli F‐18Col‐ type‐1 fimbriae synthesis by leuX. FEMS Microbiological Letters 122(3): 281–287.

Opitz D, Clausen M and Maier B (2009) Dynamics of gonococcal type IV pili during infection. Chemphyschem 10(9–10): 1614–1618.

Periasamy S, Chalmers NI, Du‐Thumm L and Kolenbrander PE (2009) Fusobacterium nucleatum ATCC 10953 requires Actinomyces naeslundii ATCC 43146 for growth on saliva in a three‐species community that includes Streptococcus oralis 34. Applied Environmental Microbiology 75(10): 3250–3257.

Proft T and Baker EN (2009) Pili in Gram‐negative and Gram‐positive bacteria: structure, assembly and their role in disease. Cellular and Molecular Life Sciences 66(4): 613–635.

Rakotoarivonina H, Jubelin G, Hebraud M et al. (2002) Adhesion to cellulose of the Gram‐positive bacterium Ruminococcus albus involves type IV pili. Microbiology 148(part 6): 1871–1880.

Sauer FG, Mulvey MA, Schilling JD, Martinez JJ and Hultgren SJ (2000) Bacterial pili: molecular mechanisms of pathogenesis. Current Opinion in Microbiology 3(1): 65–72.

Schneewind O, Model P and Fischetti VA (1992) Sorting of protein A to the staphylococcal cell wall. Cell 70(2): 267–281.

Scott JR and Zahner D (2006) Pili with strong attachments: Gram‐positive bacteria do it differently. Molecular Microbiology 62(2): 320–330.

Seifert HS (1996) Questions about gonococcal pilus phase‐ and antigenic variation. Molecular Microbiology 21(3): 433–440.

Sillanpaa J, Prakash VP, Nallapareddy SR and Murray BE (2009) Distribution of genes encoding MSCRAMMs and pili in clinical and natural populations of Enterococcus faecium. Journal of Clinical Microbiology 47(4): 896–901.

Sjoquist J, Meloun B and Hjelm H (1972) Protein A isolated from Staphylococcus aureus after digestion with lysostaphin. European Journal of Biochemistry 29(3): 572–578.

Skerker JM and Berg HC (2001) Direct observation of extension and retraction of type IV pili. Proceedings of the National Academy of Sciences of the USA 98(12): 6901–6904.

Strom MS and Lory S (1993) Structure‐function and biogenesis of the type IV pili. Annual Review of Microbiology 47: 565–596.

Swaminathan A, Mandlik A, Swierczynski A et al. (2007) Housekeeping sortase facilitates the cell wall anchoring of pilus polymers in Corynebacterium diphtheriae. Molecular Microbiology 66(4): 961–974.

Telford JL, Barocchi MA, Margarit I, Rappuoli R and Grandi G (2006) Pili in Gram‐positive pathogens. Nature Reviews of Microbiology 4(7): 509–519.

Thanassi DG and Hultgren SJ (2000) Assembly of complex organelles: pilus biogenesis in Gram‐negative bacteria as a model system. Methods 20(1): 111–126.

Thanassi DG, Saulino ET and Hultgren SJ (1998) The chaperone/usher pathway: a major terminal branch of the general secretory pathway. Current Opinion in Microbiology 1(2): 223–231.

Tomich M, Planet PJ and Figurski DH (2007) The tad locus: postcards from the widespread colonization island. Nature Reviews of Microbiology 5(5): 363–375.

Ton‐That H, Marraffini LA and Schneewind O (2004) Protein sorting to the cell wall envelope of Gram‐positive bacteria. Biochimica et Biophysica Acta 1694(1–3): 269–278.

Ton‐That H and Schneewind O (2003) Assembly of pili on the surface of Corynebacterium diphtheriae. Molecular Microbiology 50(4): 1429–1438.

Ton‐That H and Schneewind O (2004) Assembly of pili in Gram‐positive bacteria. Trends in Microbiology 12(5): 228–234.

Underhill DM (2004) Toll‐like receptors and microbes take aim at each other. Current Opinion in Immunology 16(4): 483–487.

van der Woude MW and Baumler AJ (2004) Phase and antigenic variation in bacteria. Clinical Microbiology Review 17(3): 581–611 table of contents.

Varga JJ, Nguyen V, O'Brien DK et al. (2006) Type IV pili‐dependent gliding motility in the Gram‐positive pathogen Clostridium perfringens and other clostridia. Molecular Microbiology 62(3): 680–694.

Yanagawa R, Otsuki K and Tokui T (1968) Electron microscopy of fine structure of Corynebacterium renale with special reference to pili. Japan Journal of Veterinary Research 16(1): 31–37.

Yeung MK (1999) Molecular and genetic analyses of Actinomyces spp. Critical Reviews in Oral Biology and Medicine 10(2): 120–138.

Further Reading

Jarrell KF (2009) Pili and Flagella: Current Research and Future Trends. Wymondham: Caister Academic.

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Huang, I‐Hsiu, Dwivedi, Prabhat, and Ton‐That, Hung(Apr 2010) Bacterial Pili and Fimbriae. In: eLS. John Wiley & Sons Ltd, Chichester. http://www.els.net [doi: 10.1002/9780470015902.a0000304.pub2]