Chapter 11 : Gram-Positive Type IV Pili and Competence

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Gram-Positive Type IV Pili and Competence, Page 1 of 2

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In recent years, numerous complete bacterial genome sequences became available and led to the identification of surprisingly diverse type IV pili (T4P) across a broad range of Gram-positive bacteria. The genes encoding T4P components cluster together in distinct loci, and three subsets of T4P loci present in Gram-positive bacteria have been described: (in) loci, (petence) loci, and (ight herence) loci ( ). Interestingly, they are not mutually exclusive. In fact, many Gram-positive bacteria harbor a combination of , , and loci, suggesting diverse functional roles for T4P in Gram-positive bacteria ( ). loci are commonly found in spp., and clostridial T4P are best studied for and ( ). loci are widespread in Firmicutes, among Bacillales and Lactobacillales. loci are present in archaea and Gram-negative and Gram-positive bacteria. Proteins of the system assemble adhesive fimbrial low-molecular-weight protein (Flp) pili that are largely unexplored in Gram-positive bacteria ( ). and loci are not extensively discussed here. Instead we focus on the operon present in the human respiratory pathogen and containing the genes involved in the formation of the pneumococcal type IV pilus, also referred to as competence pilus or transformation pilus.

Citation: Muschiol S, Aschtgen M, Nannapaneni P, Henriques-Normark B. 2019. Gram-Positive Type IV Pili and Competence, p 129-135. In Sandkvist M, Cascales E, Christie P (ed), Protein Secretion in Bacteria. ASM Press, Washington, DC. doi: 10.1128/microbiolspec.PSIB-0011-2018
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Figure 1

Type IV competence pilus produced by R6. The pilus was visualized by transmission electron microscopy after negative staining with uranyl acetate. Scale bar, 100 nm.

Citation: Muschiol S, Aschtgen M, Nannapaneni P, Henriques-Normark B. 2019. Gram-Positive Type IV Pili and Competence, p 129-135. In Sandkvist M, Cascales E, Christie P (ed), Protein Secretion in Bacteria. ASM Press, Washington, DC. doi: 10.1128/microbiolspec.PSIB-0011-2018
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Image of Figure 2
Figure 2

Schematic representation of the DNA uptake machinery in competent . Upon competence induction, the pneumococcal competence pilus composed of ComGC is made and captures extracellular, transforming DNA ( ). Captured DNA is passed to the DNA receptor ComEA and the transmembrane channel protein ComEC. This step is possibly mediated by an unknown retraction ATPase and subsequent pilus retraction or yet another undescribed mechanism. Double-stranded DNA (dsDNA) is cleaved by the endonuclease EndA and single-stranded DNA (ssDNA) enters the cytoplasm through the ComEC pore driven by the DNA-dependent ATPase ComFA ( ). ComFA forms a complex with ComFC and DprA ( ) and together with SsbB and RecA help in stabilization and processing of internalized ssDNA to facilitate genetic exchange ( ).

Citation: Muschiol S, Aschtgen M, Nannapaneni P, Henriques-Normark B. 2019. Gram-Positive Type IV Pili and Competence, p 129-135. In Sandkvist M, Cascales E, Christie P (ed), Protein Secretion in Bacteria. ASM Press, Washington, DC. doi: 10.1128/microbiolspec.PSIB-0011-2018
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1. Imam S,, Chen Z,, Roos DS,, Pohlschröder M . 2011. Identification of surprisingly diverse type IV pili, across a broad range of gram-positive bacteria. PLoS One 6 : e28919.[CrossRef][PubMed]
2. Melville S,, Craig L . 2013. Type IV pili in Gram-positive bacteria. Microbiol Mol Biol Rev 77 : 323 341.[CrossRef][PubMed]
3. Piepenbrink KH,, Sundberg EJ . 2016. Motility and adhesion through type IV pili in Gram-positive bacteria. Biochem Soc Trans 44 : 1659 1666.[CrossRef][PubMed]
4. Tomich M,, Planet PJ,, Figurski DH . 2007. The tad locus: postcards from the widespread colonization island. Nat Rev Microbiol 5 : 363 375.[CrossRef][PubMed]
5. Craig L,, Pique ME,, Tainer JA . 2004. Type IV pilus structure and bacterial pathogenicity. Nat Rev Microbiol 2 : 363 378.[CrossRef][PubMed]
6. Berry JL,, Pelicic V . 2015. Exceptionally widespread nanomachines composed of type IV pilins: the prokaryotic Swiss Army knives. FEMS Microbiol Rev 39 : 134 154.[CrossRef][PubMed]
7. Chung YS,, Breidt F,, Dubnau D . 1998. Cell surface localization and processing of the ComG proteins, required for DNA binding during transformation of Bacillus subtilis. Mol Microbiol 29 : 905 913.[CrossRef][PubMed]
8. Chung YS,, Dubnau D . 1995. ComC is required for the processing and translocation of comGC, a pilin-like competence protein of Bacillus subtilis. Mol Microbiol 15 : 543 551.[CrossRef][PubMed]
9. Chung YS,, Dubnau D . 1998. All seven comG open reading frames are required for DNA binding during transformation of competent Bacillus subtilis. J Bacteriol 180 : 41 45.[PubMed]
10. Chen I,, Provvedi R,, Dubnau D . 2006. A macromolecular complex formed by a pilin-like protein in competent Bacillus subtilis. J Biol Chem 281 : 21720 21727.[CrossRef][PubMed]
11. Varga JJ,, Nguyen V,, O’Brien DK,, Rodgers K,, Walker RA,, Melville SB . 2006. Type IV pili-dependent gliding motility in the Gram-positive pathogen Clostridium perfringens and other clostridia. Mol Microbiol 62 : 680 694.[CrossRef][PubMed]
12. Piepenbrink KH,, Maldarelli GA,, de la Peña CF,, Mulvey GL,, Snyder GA,, De Masi L,, von Rosenvinge EC,, Günther S,, Armstrong GD,, Donnenberg MS,, Sundberg EJ . 2014. Structure of Clostridium difficile PilJ exhibits unprecedented divergence from known type IV pilins. J Biol Chem 289 : 4334 4345.[CrossRef][PubMed]
13. Piepenbrink KH,, Maldarelli GA,, Martinez de la Peña CF,, Dingle TC,, Mulvey GL,, Lee A,, von Rosenvinge E,, Armstrong GD,, Donnenberg MS,, Sundberg EJ . 2015. Structural and evolutionary analyses show unique stabilization strategies in the type IV pili of Clostridium difficile. Structure 23 : 385 396.[CrossRef][PubMed]
14. Rakotoarivonina H,, Jubelin G,, Hebraud M,, Gaillard-Martinie B,, Forano E,, Mosoni P . 2002. Adhesion to cellulose of the Gram-positive bacterium Ruminococcus albus involves type IV pili. Microbiology 148 : 1871 1880.[CrossRef][PubMed]
15. Laurenceau R,, Péhau-Arnaudet G,, Baconnais S,, Gault J,, Malosse C,, Dujeancourt A,, Campo N,, Chamot-Rooke J,, Le Cam E,, Claverys JP,, Fronzes R . 2013. A type IV pilus mediates DNA binding during natural transformation in Streptococcus pneumoniae. PLoS Pathog 9 : e1003473.[CrossRef][PubMed]
16. Muschiol S,, Erlendsson S,, Aschtgen MS,, Oliveira V,, Schmieder P,, de Lichtenberg C,, Teilum K,, Boesen T,, Akbey U,, Henriques-Normark B . 2017. Structure of the competence pilus major pilin ComGC in Streptococcus pneumoniae. J Biol Chem 292 : 14134 14146.[CrossRef][PubMed]
17. Gurung I,, Berry JL,, Hall AMJ,, Pelicic V . 2017. Cloning-independent markerless gene editing in Streptococcus sanguinis: novel insights in type IV pilus biology. Nucleic Acids Res 45 : e40.[CrossRef][PubMed]
18. Gurung I,, Spielman I,, Davies MR,, Lala R,, Gaustad P,, Biais N,, Pelicic V . 2016. Functional analysis of an unusual type IV pilus in the Gram-positive Streptococcus sanguinis. Mol Microbiol 99 : 380 392.[CrossRef][PubMed]
19. Angelov A,, Bergen P,, Nadler F,, Hornburg P,, Lichev A,, Übelacker M,, Pachl F,, Kuster B,, Liebl W . 2015. Novel Flp pilus biogenesis-dependent natural transformation. Front Microbiol 6 : 84.[CrossRef][PubMed]
20. Pegden RS,, Larson MA,, Grant RJ,, Morrison M . 1998. Adherence of the gram-positive bacterium Ruminococcus albus to cellulose and identification of a novel form of cellulose-binding protein which belongs to the Pil family of proteins. J Bacteriol 180 : 5921 5927.[PubMed]
21. Håvarstein LS,, Coomaraswamy G,, Morrison DA . 1995. An unmodified heptadecapeptide pheromone induces competence for genetic transformation in Streptococcus pneumoniae. Proc Natl Acad Sci U S A 92 : 11140 11144.[CrossRef][PubMed]
22. Moreno-Gámez S,, Sorg RA,, Domenech A,, Kjos M,, Weissing FJ,, van Doorn GS,, Veening JW . 2017. Quorum sensing integrates environmental cues, cell density and cell history to control bacterial competence. Nat Commun 8 : 854.[CrossRef][PubMed]
23. Johnsborg O,, Eldholm V,, Håvarstein LS . 2007. Natural genetic transformation: prevalence, mechanisms and function. Res Microbiol 158 : 767 778.[CrossRef][PubMed]
24. Johnston C,, Martin B,, Fichant G,, Polard P,, Claverys JP . 2014. Bacterial transformation: distribution, shared mechanisms and divergent control. Nat Rev Microbiol 12 : 181 196.[CrossRef][PubMed]
25. Lee MS,, Morrison DA . 1999. Identification of a new regulator in Streptococcus pneumoniae linking quorum sensing to competence for genetic transformation. J Bacteriol 181 : 5004 5016.[PubMed]
26. Peterson SN,, Sung CK,, Cline R,, Desai BV,, Snesrud EC,, Luo P,, Walling J,, Li H,, Mintz M,, Tsegaye G,, Burr PC,, Do Y,, Ahn S,, Gilbert J,, Fleischmann RD,, Morrison DA . 2004. Identification of competence pheromone responsive genes in Streptococcus pneumoniae by use of DNA microarrays. Mol Microbiol 51 : 1051 1070.[CrossRef][PubMed]
27. Briley K Jr,, Dorsey-Oresto A,, Prepiak P,, Dias MJ,, Mann JM,, Dubnau D . 2011. The secretion ATPase ComGA is required for the binding and transport of transforming DNA. Mol Microbiol 81 : 818 830.[CrossRef][PubMed]
28. Giltner CL,, Nguyen Y,, Burrows LL . 2012. Type IV pilin proteins: versatile molecular modules. Microbiol Mol Biol Rev 76 : 740 772.[CrossRef][PubMed]
29. Sandkvist M . 2001. Biology of type II secretion. Mol Microbiol 40 : 271 283.[CrossRef][PubMed]
30. Makarova KS,, Koonin EV,, Albers SV . 2016. Diversity and evolution of type IV pili systems in Archaea. Front Microbiol 7 : 667.[CrossRef][PubMed]
31. Albers SV,, Jarrell KF . 2018. The archaellum: an update on the unique archaeal motility structure. Trends Microbiol 26 : 351 362.[CrossRef][PubMed]
32. Korotkov KV,, Hol WG . 2008. Structure of the GspK-GspI-GspJ complex from the enterotoxigenic Escherichia coli type 2 secretion system. Nat Struct Mol Biol 15 : 462 468.[CrossRef][PubMed]
33. Wolfgang M,, Lauer P,, Park HS,, Brossay L,, Hébert J,, Koomey M . 1998. PilT mutations lead to simultaneous defects in competence for natural transformation and twitching motility in piliated Neisseria gonorrhoeae. Mol Microbiol 29 : 321 330.[CrossRef][PubMed]
34. Obergfell KP,, Seifert HS . 2015. Mobile DNA in the pathogenic Neisseria. Microbiol Spectr 3 : MDNA3-0015-2014.
35. Matthey N,, Blokesch M . 2016. The DNA-uptake process of naturally competent Vibrio cholerae. Trends Microbiol 24 : 98 110.[CrossRef][PubMed]
36. Ellison CK,, Dalia TN,, Vidal Ceballos A,, Wang JC,, Biais N,, Brun YV,, Dalia AB . 2018. Retraction of DNA-bound type IV competence pili initiates DNA uptake during natural transformation in Vibrio cholerae. Nat Microbiol 3 : 773 780.[CrossRef][PubMed]
37. Cowley LA,, Petersen FC,, Junges R,, Jimson D,, Jimenez M,, Morrison DA,, Hanage WP . 2018. Evolution via recombination: cell-to-cell contact facilitates larger recombination events in Streptococcus pneumoniae. PLoS Genet 14 : e1007410.[CrossRef][PubMed]
38. Kolappan S,, Ng D,, Yang G,, Harn T,, Craig L . 2015. Crystal structure of the minor pilin CofB, the initiator of CFA/III pilus assembly in enterotoxigenic Escherichia coli. J Biol Chem 290 : 25805 25818.[CrossRef][PubMed]
39. Ng D,, Harn T,, Altindal T,, Kolappan S,, Marles JM,, Lala R,, Spielman I,, Gao Y,, Hauke CA,, Kovacikova G,, Verjee Z,, Taylor RK,, Biais N,, Craig L . 2016. The Vibrio cholerae minor pilin TcpB initiates assembly and retraction of the toxin-coregulated pilus. PLoS Pathog 12 : e1006109.[CrossRef][PubMed]
40. Giltner CL,, Habash M,, Burrows LL . 2010. Pseudomonas aeruginosa minor pilins are incorporated into type IV pili. J Mol Biol 398 : 444 461.[CrossRef][PubMed]
41. Nguyen Y,, Sugiman-Marangos S,, Harvey H,, Bell SD,, Charlton CL,, Junop MS,, Burrows LL . 2015. Pseudomonas aeruginosa minor pilins prime type IVa pilus assembly and promote surface display of the PilY1 adhesin. J Biol Chem 290 : 601 611.[CrossRef][PubMed]
42. Marko VA,, Kilmury SLN,, MacNeil LT,, Burrows LL . 2018. Pseudomonas aeruginosa type IV minor pilins and PilY1 regulate virulence by modulating FimS-AlgR activity. PLoS Pathog 14 : e1007074.[CrossRef][PubMed]
43. Kuchma SL,, Griffin EF,, O’Toole GA . 2012. Minor pilins of the type IV pilus system participate in the negative regulation of swarming motility. J Bacteriol 194 : 5388 5403.[CrossRef][PubMed]
44. Cehovin A,, Simpson PJ,, McDowell MA,, Brown DR,, Noschese R,, Pallett M,, Brady J,, Baldwin GS,, Lea SM,, Matthews SJ,, Pelicic V . 2013. Specific DNA recognition mediated by a type IV pilin. Proc Natl Acad Sci U S A 110 : 3065 3070.[CrossRef][PubMed]
45. Cisneros DA,, Bond PJ,, Pugsley AP,, Campos M,, Francetic O . 2012. Minor pseudopilin self-assembly primes type II secretion pseudopilus elongation. EMBO J 31 : 1041 1053.[CrossRef][PubMed]
46. Cisneros DA,, Pehau-Arnaudet G,, Francetic O . 2012. Heterologous assembly of type IV pili by a type II secretion system reveals the role of minor pilins in assembly initiation. Mol Microbiol 86 : 805 818.[CrossRef][PubMed]
47. Burrows LL . 2012. Prime time for minor subunits of the type II secretion and type IV pilus systems. Mol Microbiol 86 : 765 769.[CrossRef][PubMed]
48. Johnston C,, Campo N,, Bergé MJ,, Polard P,, Claverys JP . 2014. Streptococcus pneumoniae, le transformiste. Trends Microbiol 22 : 113 119.[CrossRef][PubMed]
49. Diallo A,, Foster HR,, Gromek KA,, Perry TN,, Dujeancourt A,, Krasteva PV,, Gubellini F,, Falbel TG,, Burton BM,, Fronzes R . 2017. Bacterial transformation: ComFA is a DNA-dependent ATPase that forms complexes with ComFC and DprA. Mol Microbiol 105 : 741 754.[CrossRef][PubMed]

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