Conserved Spirosomes Suggest a Single Type of Transformation Pilus in Competence
Streptococcus pneumoniae often escapes prevention and treatment through rapid horizontal gene transfer via natural transformation. Uptake of exogenous DNA requires expression of a transformation pilus but two markedly different models for pilus assembly and function have been proposed. We previously reported a long, Type 4 pilus-like appendage on the surface of competent pneumococci that binds extracellular DNA as initial receptor, while a separate study proposed that secreted short, ‘plaited’ transformation pili act simply as peptidoglycan drills to open DNA gateways. Here we show that the ‘plaited’ structures are not competence-specific or related to transformation. We further demonstrate that these are macromolecular assemblies of the metabolic enzyme acetaldehyde-alcohol dehydrogenase—or spirosomes—broadly conserved across the bacterial kingdom.
Vyšlo v časopise:
Conserved Spirosomes Suggest a Single Type of Transformation Pilus in Competence. PLoS Pathog 11(4): e32767. doi:10.1371/journal.ppat.1004835
Kategorie:
Research Article
prolekare.web.journal.doi_sk:
https://doi.org/10.1371/journal.ppat.1004835
Souhrn
Streptococcus pneumoniae often escapes prevention and treatment through rapid horizontal gene transfer via natural transformation. Uptake of exogenous DNA requires expression of a transformation pilus but two markedly different models for pilus assembly and function have been proposed. We previously reported a long, Type 4 pilus-like appendage on the surface of competent pneumococci that binds extracellular DNA as initial receptor, while a separate study proposed that secreted short, ‘plaited’ transformation pili act simply as peptidoglycan drills to open DNA gateways. Here we show that the ‘plaited’ structures are not competence-specific or related to transformation. We further demonstrate that these are macromolecular assemblies of the metabolic enzyme acetaldehyde-alcohol dehydrogenase—or spirosomes—broadly conserved across the bacterial kingdom.
Zdroje
1. Bogaert D, De Groot R, Hermans PW (2004) Streptococcus pneumoniae colonisation: the key to pneumococcal disease. The Lancet Infectious diseases 4: 144–154. 14998500
2. Campbell GD Jr., Silberman R (1998) Drug-resistant Streptococcus pneumoniae. Clinical infectious diseases: an official publication of the Infectious Diseases Society of America 26: 1188–1195.
3. Walker CL, Rudan I, Liu L, Nair H, Theodoratou E, et al. (2013) Global burden of childhood pneumonia and diarrhoea. Lancet 381: 1405–1416. doi: 10.1016/S0140-6736(13)60222-6 23582727
4. Hiller NL, Ahmed A, Powell E, Martin DP, Eutsey R, et al. (2010) Generation of genic diversity among Streptococcus pneumoniae strains via horizontal gene transfer during a chronic polyclonal pediatric infection. PLoS pathogens 6: e1001108. doi: 10.1371/journal.ppat.1001108 20862314
5. Johnston C, Martin B, Fichant G, Polard P, Claverys JP (2014) Bacterial transformation: distribution, shared mechanisms and divergent control. Nature reviews Microbiology 12: 181–196. doi: 10.1038/nrmicro3199 24509783
6. Chen I, Dubnau D (2004) DNA uptake during bacterial transformation. Nature reviews Microbiology 2: 241–249. 15083159
7. Johnston C, Campo N, Berge MJ, Polard P, Claverys JP (2014) Streptococcus pneumoniae, le transformiste. Trends in microbiology 22: 113–119. doi: 10.1016/j.tim.2014.01.002 24508048
8. Balaban M, Battig P, Muschiol S, Tirier SM, Wartha F, et al. (2014) Secretion of a pneumococcal type II secretion system pilus correlates with DNA uptake during transformation. Proceedings of the National Academy of Sciences of the United States of America 111: E758–765. doi: 10.1073/pnas.1313860111 24550320
9. Chen I, Provvedi R, Dubnau D (2006) A macromolecular complex formed by a pilin-like protein in competent Bacillus subtilis. The Journal of biological chemistry 281: 21720–21727. 16751195
10. Laurenceau R, Pehau-Arnaudet G, Baconnais S, Gault J, Malosse C, et al. (2013) A type IV pilus mediates DNA binding during natural transformation in Streptococcus pneumoniae. PLoS pathogens 9: e1003473. doi: 10.1371/journal.ppat.1003473 23825953
11. Dubnau D (1999) DNA uptake in bacteria. Annual review of microbiology 53: 217–244. 10547691
12. Nunn D, Bergman S, Lory S (1990) Products of three accessory genes, pilB, pilC, and pilD, are required for biogenesis of Pseudomonas aeruginosa pili. Journal of bacteriology 172: 2911–2919. 1971619
13. Mann JM, Carabetta VJ, Cristea IM, Dubnau D (2013) Complex formation and processing of the minor transformation pilins of Bacillus subtilis. Molecular microbiology 90: 1201–1215. doi: 10.1111/mmi.12425 24164455
14. Craig L, Pique ME, Tainer JA (2004) Type IV pilus structure and bacterial pathogenicity. Nature reviews Microbiology 2: 363–378. 15100690
15. Campos M, Nilges M, Cisneros DA, Francetic O (2010) Detailed structural and assembly model of the type II secretion pilus from sparse data. Proceedings of the National Academy of Sciences of the United States of America 107: 13081–13086. doi: 10.1073/pnas.1001703107 20616068
16. Nivaskumar M, Bouvier G, Campos M, Nadeau N, Yu X, et al. (2014) Distinct docking and stabilization steps of the Pseudopilus conformational transition path suggest rotational assembly of type IV pilus-like fibers. Structure 22: 685–696. doi: 10.1016/j.str.2014.03.001 24685147
17. Havarstein LS, Martin B, Johnsborg O, Granadel C, Claverys JP (2006) New insights into the pneumococcal fratricide: relationship to clumping and identification of a novel immunity factor. Molecular microbiology 59: 1297–1307. 16430701
18. Altschul SF, Gish W, Miller W, Myers EW, Lipman DJ (1990) Basic local alignment search tool. Journal of molecular biology 215: 403–410. 2231712
19. Extance J, Crennell SJ, Eley K, Cripps R, Hough DW, et al. (2013) Structure of a bifunctional alcohol dehydrogenase involved in bioethanol generation in Geobacillus thermoglucosidasius. Acta crystallographica Section D, Biological crystallography 69: 2104–2115. doi: 10.1107/S0907444913020349 24100328
20. Kawata T, Masuda K, Nomura S (1982) Superprecipitation-like phenomenon and destruction induced by adenosine 5'-triphosphate in spirosomes isolated from Lactobacillus brevis. Microbiology and immunology 26: 979–983. 6298583
21. Kessler D, Herth W, Knappe J (1992) Ultrastructure and pyruvate formate-lyase radical quenching property of the multienzymic AdhE protein of Escherichia coli. The Journal of biological chemistry 267: 18073–18079. 1325457
22. Matayoshi S, Oda H (1985) Detection of fine spiral structures (spirosomes) by weak sonication in some bacterial strains. Microbiology and immunology 29: 13–20. 3990585
23. Matayoshi S, Oda H, Sarwar G (1989) Relationship between the production of spirosomes and anaerobic glycolysis activity in Escherichia coli B. Journal of general microbiology 135: 525–529. 2695595
24. Nomura S, Masuda K, Kawata T (1989) Comparative characterization of spirosomes isolated from Lactobacillus brevis, Lactobacillus fermentum, and Lactobacillus buchneri. Microbiology and immunology 33: 23–34. 2733612
25. Ueki Y, Masuda K, Kawata T (1982) Purification and characterization of spirosomes in Lactobacillus brevis. Microbiology and immunology 26: 199–211. 7109979
26. Yamato M, Takahashi Y, Tomotake H, Ota F, Hirota K, et al. (1994) Monoclonal antibodies to spirosin of Yersinia enterocolitica and analysis of the localization of spirosome by use of them. Microbiology and immunology 38: 177–182. 7521508
27. Burghout P, Bootsma HJ, Kloosterman TG, Bijlsma JJ, de Jongh CE, et al. (2007) Search for genes essential for pneumococcal transformation: the RADA DNA repair protein plays a role in genomic recombination of donor DNA. Journal of bacteriology 189: 6540–6550. 17631629
28. Pettersen EF, Goddard TD, Huang CC, Couch GS, Greenblatt DM, et al. (2004) UCSF Chimera—a visualization system for exploratory research and analysis. Journal of computational chemistry 25: 1605–1612. 15264254
29. Sebaihia M, Wren BW, Mullany P, Fairweather NF, Minton N, et al. (2006) The multidrug-resistant human pathogen Clostridium difficile has a highly mobile, mosaic genome. Nature genetics 38: 779–786. 16804543
30. Xu P, Ge X, Chen L, Wang X, Dou Y, et al. (2011) Genome-wide essential gene identification in Streptococcus sanguinis. Scientific reports 1: 125. doi: 10.1038/srep00125 22355642
31. Krissinel E, Henrick K (2007) Inference of macromolecular assemblies from crystalline state. Journal of molecular biology 372: 774–797. 17681537
32. Zhang YH (2011) Substrate channeling and enzyme complexes for biotechnological applications. Biotechnology advances 29: 715–725. doi: 10.1016/j.biotechadv.2011.05.020 21672618
33. Encheva V, Shah HN, Gharbia SE (2009) Proteomic analysis of the adaptive response of Salmonella enterica serovar Typhimurium to growth under anaerobic conditions. Microbiology 155: 2429–2441. doi: 10.1099/mic.0.026138-0 19389776
34. Eldholm V, Johnsborg O, Haugen K, Ohnstad HS, Havarstein LS (2009) Fratricide in Streptococcus pneumoniae: contributions and role of the cell wall hydrolases CbpD, LytA and LytC. Microbiology 155: 2223–2234. doi: 10.1099/mic.0.026328-0 19389766
35. Gubellini F, Verdon G, Karpowich NK, Luff JD, Boel G, et al. (2011) Physiological response to membrane protein overexpression in E. coli. Molecular & cellular proteomics: MCP 10: M111 007930.
36. Wagner S, Baars L, Ytterberg AJ, Klussmeier A, Wagner CS, et al. (2007) Consequences of membrane protein overexpression in Escherichia coli. Molecular & cellular proteomics: MCP 6: 1527–1550.
37. Okorokov AL, Chaban YL, Bugreev DV, Hodgkinson J, Mazin AV, et al. (2010) Structure of the hDmc1-ssDNA filament reveals the principles of its architecture. PloS one 5: e8586. doi: 10.1371/journal.pone.0008586 20062530
38. Williams RC, Spengler SJ (1986) Fibers of RecA protein and complexes of RecA protein and single-stranded phi X174 DNA as visualized by negative-stain electron microscopy. Journal of molecular biology 187: 109–118. 2937923
39. Yu X, VanLoock MS, Yang S, Reese JT, Egelman EH (2004) What is the structure of the RecA-DNA filament? Current protein & peptide science 5: 73–79.
40. Berge M, Mortier-Barriere I, Martin B, Claverys JP (2003) Transformation of Streptococcus pneumoniae relies on DprA- and RecA-dependent protection of incoming DNA single strands. Molecular microbiology 50: 527–536. 14617176
41. Cox MM (1999) Recombinational DNA repair in bacteria and the RecA protein. Progress in nucleic acid research and molecular biology 63: 311–366. 10506835
42. Mizuno N, Dramicanin M, Mizuuchi M, Adam J, Wang Y, et al. (2013) MuB is an AAA+ ATPase that forms helical filaments to control target selection for DNA transposition. Proceedings of the National Academy of Sciences of the United States of America 110: E2441–2450. doi: 10.1073/pnas.1309499110 23776210
43. Shih YL, Rothfield L (2006) The bacterial cytoskeleton. Microbiology and molecular biology reviews: MMBR 70: 729–754. 16959967
44. Stubbs G, Kendall A (2012) Helical viruses. Advances in experimental medicine and biology 726: 631–658. doi: 10.1007/978-1-4614-0980-9_28 22297534
45. Seitz P, Blokesch M (2013) DNA-uptake machinery of naturally competent Vibrio cholerae. Proceedings of the National Academy of Sciences of the United States of America 110: 17987–17992. doi: 10.1073/pnas.1315647110 24127573
46. Vidal JE, Howery KE, Ludewick HP, Nava P, Klugman KP (2013) Quorum-sensing systems LuxS/autoinducer 2 and Com regulate Streptococcus pneumoniae biofilms in a bioreactor with living cultures of human respiratory cells. Infection and immunity 81: 1341–1353. doi: 10.1128/IAI.01096-12 23403556
47. Berge M, Moscoso M, Prudhomme M, Martin B, Claverys JP (2002) Uptake of transforming DNA in Gram-positive bacteria: a view from Streptococcus pneumoniae. Molecular microbiology 45: 411–421. 12123453
48. Cehovin A, Simpson PJ, McDowell MA, Brown DR, Noschese R, et al. (2013) Specific DNA recognition mediated by a type IV pilin. Proceedings of the National Academy of Sciences of the United States of America 110: 3065–3070. doi: 10.1073/pnas.1218832110 23386723
49. van Schaik EJ, Giltner CL, Audette GF, Keizer DW, Bautista DL, et al. (2005) DNA binding: a novel function of Pseudomonas aeruginosa type IV pili. Journal of bacteriology 187: 1455–1464. 15687210
50. Provvedi R, Dubnau D (1999) ComEA is a DNA receptor for transformation of competent Bacillus subtilis. Molecular microbiology 31: 271–280. 9987128
51. Kurre R, Maier B (2012) Oxygen depletion triggers switching between discrete speed modes of gonococcal type IV pili. Biophysical journal 102: 2556–2563. doi: 10.1016/j.bpj.2012.04.020 22713571
52. Maier B, Chen I, Dubnau D, Sheetz MP (2004) DNA transport into Bacillus subtilis requires proton motive force to generate large molecular forces. Nature structural & molecular biology 11: 643–649.
53. von Hippel PH, Berg OG (1989) Facilitated target location in biological systems. The Journal of biological chemistry 264: 675–678. 2642903
54. Prudhomme M, Camilli A, Claverys J-P (2007) In vitro mariner mutagenesis of Streptococcus pneumoniae: tools and traps. In: Hakenbeck R, Chhatwal GS, editors. The Molecular Biology of Streptococci Norwich, UK: Horizon Scientific Press. pp. 511–517.
55. Wilm M, Shevchenko A, Houthaeve T, Breit S, Schweigerer L, et al. (1996) Femtomole sequencing of proteins from polyacrylamide gels by nano-electrospray mass spectrometry. Nature 379: 466–469. 8559255
56. Cox J, Matic I, Hilger M, Nagaraj N, Selbach M, et al. (2009) A practical guide to the MaxQuant computational platform for SILAC-based quantitative proteomics. Nature protocols 4: 698–705. doi: 10.1038/nprot.2009.36 19373234
57. Mindell JA, Grigorieff N (2003) Accurate determination of local defocus and specimen tilt in electron microscopy. Journal of structural biology 142: 334–347. 12781660
58. Shaikh TR, Gao H, Baxter WT, Asturias FJ, Boisset N, et al. (2008) SPIDER image processing for single-particle reconstruction of biological macromolecules from electron micrographs. Nature protocols 3: 1941–1974. doi: 10.1038/nprot.2008.156 19180078
59. Tang G, Peng L, Baldwin PR, Mann DS, Jiang W, et al. (2007) EMAN2: an extensible image processing suite for electron microscopy. Journal of structural biology 157: 38–46. 16859925
60. Martin B, Granadel C, Campo N, Henard V, Prudhomme M, et al. (2010) Expression and maintenance of ComD-ComE, the two-component signal-transduction system that controls competence of Streptococcus pneumoniae. Molecular microbiology 75: 1513–1528. doi: 10.1111/j.1365-2958.2010.07071.x 20180906
61. Claverys JP, Martin B, Polard P (2009) The genetic transformation machinery: composition, localization, and mechanism. FEMS microbiology reviews 33: 643–656. doi: 10.1111/j.1574-6976.2009.00164.x 19228200
Štítky
Hygiena a epidemiológia Infekčné lekárstvo LaboratóriumČlánok vyšiel v časopise
PLOS Pathogens
2015 Číslo 4
- Parazitičtí červi v terapii Crohnovy choroby a dalších zánětlivých autoimunitních onemocnění
- Očkování proti virové hemoragické horečce Ebola experimentální vakcínou rVSVDG-ZEBOV-GP
- Koronavirus hýbe světem: Víte jak se chránit a jak postupovat v případě podezření?
Najčítanejšie v tomto čísle
- Role of Hypoxia Inducible Factor-1α (HIF-1α) in Innate Defense against Uropathogenic Infection
- Toxin-Induced Necroptosis Is a Major Mechanism of Lung Damage
- Transgenic Fatal Familial Insomnia Mice Indicate Prion Infectivity-Independent Mechanisms of Pathogenesis and Phenotypic Expression of Disease
- A Temporal Gate for Viral Enhancers to Co-opt Toll-Like-Receptor Transcriptional Activation Pathways upon Acute Infection