Protease-associated import systems are widespread in Gram-negative bacteria

English version

Autoři: Rhys Grinter ^aff001; Pok Man Leung ^aff001; Lakshmi C. Wijeyewickrema ^aff004; Dene Littler ^aff002; Simone Beckham ^aff002; Robert N. Pike ^aff004; Daniel Walker ^aff006; Chris Greening ^aff001; Trevor Lithgow ^aff002
Působiště autorů: School of Biological Sciences, Monash University, Clayton, Victoria, Australia ^aff001; Infection and Immunity Program, Biomedicine Discovery Institute and Department of Microbiology, Monash University, Clayton, Australia ^aff002; Institute of Microbiology and Infection, School of Immunity and Infection, University of Birmingham, Birmingham, England, United Kingdom ^aff003; Department of Biochemistry and Genetics, La Trobe Institute of Molecular Sciences, La Trobe University, Melbourne, Victoria, Australia ^aff004; La Trobe Rural Health School, College of Science, Health and Engineering, La Trobe University, Bendigo, Australia ^aff005; Institute of Infection, Immunity, and Inflammation, College of Medical, Veterinary, and Life Sciences, University of Glasgow, Glasgow, United Kingdom ^aff006
Vyšlo v časopise: Protease-associated import systems are widespread in Gram-negative bacteria. PLoS Genet 15(10): e32767. doi:10.1371/journal.pgen.1008435
Kategorie: Research Article
prolekare.web.journal.doi_sk: https://doi.org/10.1371/journal.pgen.1008435

Souhrn

Bacteria have evolved sophisticated uptake machineries in order to obtain the nutrients required for growth. Gram-negative plant pathogens of the genus Pectobacterium obtain iron from the protein ferredoxin, which is produced by their plant hosts. This iron-piracy is mediated by the ferredoxin uptake system (Fus), a gene cluster encoding proteins that transport ferredoxin into the bacterial cell and process it proteolytically. In this work we show that gene clusters related to the Fus are widespread in bacterial species. Through structural and biochemical characterisation of the distantly related Fus homologues YddB and PqqL from Escherichia coli, we show that these proteins are analogous to components of the Fus from Pectobacterium. The membrane protein YddB shares common structural features with the outer membrane ferredoxin transporter FusA, including a large extracellular substrate binding site. PqqL is an active protease with an analogous periplasmic localisation and iron-dependent expression to the ferredoxin processing protease FusC. Structural analysis demonstrates that PqqL and FusC share specific features that distinguish them from other members of the M16 protease family. Taken together, these data provide evidence that protease associated import systems analogous to the Fus are widespread in Gram-negative bacteria.

Klíčová slova:

Outer membrane proteins – Crystal structure – Sequence databases – Proteases – Glycerol – Sequence similarity searching – Crystals – Operons

Zdroje

1. Pekkonen M, Ketola T, Laakso JT. Resource Availability and Competition Shape the Evolution of Survival and Growth Ability in a Bacterial Community. PLoS ONE. 2013;8(9):e76471. doi: 10.1371/journal.pone.0076471 24098791

2. Hibbing ME, Fuqua C, Parsek MR, Peterson SB. Bacterial competition: surviving and thriving in the microbial jungle. Nature Reviews Microbiology. 2010;8(1):15. doi: 10.1038/nrmicro2259 19946288

3. Barber MF, Elde NC. Buried treasure: evolutionary perspectives on microbial iron piracy. Trends in Genetics. 2015;31(11):627–36. doi: 10.1016/j.tig.2015.09.001 26431675

4. Grinter R, Milner J, Walker D. Ferredoxin containing bacteriocins suggest a novel mechanism of iron uptake in Pectobacterium spp. PLoS ONE. 2012;7(3):e33033. doi: 10.1371/journal.pone.0033033 22427936

5. Grinter R, Milner J, Walker D. Beware of proteins bearing gifts: protein antibiotics that use iron as a Trojan horse. FEMS Microbiol Lett. 2013;338(1):1–9. doi: 10.1111/1574-6968.12011 22998625

6. Grinter R, Hay ID, Song J, Wang J, Teng D, Dhanesakaran V, et al. FusC, a member of the M16 protease family acquired by bacteria for iron piracy against plants. PLoS Biol. 2018;16(8):e2006026. doi: 10.1371/journal.pbio.2006026 30071011

7. Grinter R, Josts I, Mosbahi K, Roszak AW, Cogdell RJ, Bonvin AM, et al. Structure of the bacterial plant-ferredoxin receptor FusA. Nat Commun. 2016;7.

8. Mosbahi K, Wojnowska M, Albalat A, Walker D. Bacterial iron acquisition mediated by outer membrane translocation and cleavage of a host protein. Proceedings of the National Academy of Sciences. 2018:201800672.

9. Grinter R, Josts I, Zeth K, Roszak AW, McCaughey LC, Cogdell RJ, et al. Structure of the atypical bacteriocin pectocin M2 implies a novel mechanism of protein uptake. Mol Microbiol. 2014;93(2):234–46. doi: 10.1111/mmi.12655 24865810

10. Noinaj N, Easley NC, Oke M, Mizuno N, Gumbart J, Boura E, et al. Structural basis for iron piracy by pathogenic Neisseria. Nature. 2012;483(7387):53–8. http://www.nature.com/nature/journal/v483/n7387/abs/nature10823.html-supplementary-information. doi: 10.1038/nature10823 22327295

11. Huang W, Wilks A. Extracellular Heme Uptake and the Challenge of Bacterial Cell Membranes. Annu Rev Biochem. 2017;(0).

12. Finn RD, Clements J, Eddy SR. HMMER web server: interactive sequence similarity searching. Nucleic Acids Res. 2011;39(Web Server issue):W29–W37. doi: 10.1093/nar/gkr367 PMC3125773. 21593126

13. Frickey T, Lupas A. CLANS: a Java application for visualizing protein families based on pairwise similarity. Bioinformatics. 2004;20(18):3702–4. doi: 10.1093/bioinformatics/bth444 15284097

14. Schütz B, Seidel J, Sturm G, Einsle O, Gescher J. Investigation of the electron transport chain to and the catalytic activity of the diheme cytochrome c peroxidase CcpA of Shewanella oneidensis. Appl Environ Microbiol. 2011;77(17):6172–80. doi: 10.1128/AEM.00606-11 21742904

15. Fülöp V, Ridout CJ, Greenwood C, Hajdu J. Crystal structure of the di-haem cytochrome c peroxidase from Pseudomonas aeruginosa. Structure. 1995;3(11):1225–33. doi: 10.1016/s0969-2126(01)00258-1 8591033

16. Martorana AM, Motta S, Di Silvestre D, Falchi F, Dehò G, Mauri P, et al. Dissecting Escherichia coli outer membrane biogenesis using differential proteomics. PLoS ONE. 2014;9(6):e100941. doi: 10.1371/journal.pone.0100941 24967819

17. Vertommen D, Ruiz N, Leverrier P, Silhavy TJ, Collet JF. Characterization of the role of the Escherichia coli periplasmic chaperone SurA using differential proteomics. Proteomics. 2009;9(9):2432–43. doi: 10.1002/pmic.200800794 19343722

18. Lee EY, Bang JY, Park GW, Choi DS, Kang JS, Kim HJ, et al. Global proteomic profiling of native outer membrane vesicles derived from Escherichia coli. Proteomics. 2007;7(17):3143–53. doi: 10.1002/pmic.200700196 17787032

19. Scorza FB, Doro F, Rodríguez-Ortega MJ, Stella M, Liberatori S, Taddei AR, et al. Proteomics characterization of outer membrane vesicles from the extraintestinal pathogenic Escherichia coli ΔtolR IHE3034 mutant. Molecular & Cellular Proteomics. 2008;7(3):473–85.

20. Wurpel DJ, Moriel DG, Totsika M, Easton DM, Schembri MA. Comparative analysis of the uropathogenic Escherichia coli surface proteome by tandem mass-spectrometry of artificially induced outer membrane vesicles. Journal of proteomics. 2015;115:93–106. doi: 10.1016/j.jprot.2014.12.005 25534882

21. Subashchandrabose S, Smith SN, Spurbeck RR, Kole MM, Mobley HLT. Genome-Wide Detection of Fitness Genes in Uropathogenic Escherichia coli during Systemic Infection. PLoS Pathog. 2013;9(12):e1003788. doi: 10.1371/journal.ppat.1003788 24339777

22. Seo SW, Kim D, Latif H, O’Brien EJ, Szubin R, Palsson BO. Deciphering Fur transcriptional regulatory network highlights its complex role beyond iron metabolism in Escherichia coli. Nature communications. 2014;5:4910. doi: 10.1038/ncomms5910 25222563

23. McHugh JP, Rodríguez-Quiñones F, Abdul-Tehrani H, Svistunenko DA, Poole RK, Cooper CE, et al. Global iron-dependent gene regulation in Escherichia coli A new mechanism for iron homeostasis. J Biol Chem. 2003;278(32):29478–86. doi: 10.1074/jbc.M303381200 12746439

24. Holm L, Laakso LM. Dali server update. Nucleic Acids Res. 2016;44(W1):W351–W5. doi: 10.1093/nar/gkw357 27131377

25. Grinter R, Lithgow T. Determination of the Molecular Basis for Coprogen Import by Gram Negative Bacteria. IUCrJ. 2019;In Press.

26. Garcia EC, Brumbaugh AR, Mobley HL. Redundancy and specificity of Escherichia coli iron acquisition systems during urinary tract infection. Infect Immun. 2011;79(3):1225–35. doi: 10.1128/IAI.01222-10 21220482

27. Sklar JG, Wu T, Kahne D, Silhavy TJ. Defining the roles of the periplasmic chaperones SurA, Skp, and DegP in Escherichia coli. Genes Dev. 2007;21(19):2473–84. doi: 10.1101/gad.1581007 17908933

28. Noinaj N, Kuszak AJ, Gumbart JC, Lukacik P, Chang H, Easley NC, et al. Structural insight into the biogenesis of β-barrel membrane proteins. Nature. 2013;501(7467):385–90. doi: 10.1038/nature12521 http://www.nature.com/nature/journal/v501/n7467/abs/nature12521.html-supplementary-information. 23995689

29. Selkrig J, Mosbahi K, Webb CT, Belousoff MJ, Perry AJ, Wells TJ, et al. Discovery of an archetypal protein transport system in bacterial outer membranes. Nat Struct Mol Biol. 2012;19(5):506–10. http://www.nature.com/nsmb/journal/v19/n5/abs/nsmb.2261.html-supplementary-information. doi: 10.1038/nsmb.2261 22466966

30. King JV, Liang WG, Scherpelz KP, Schilling AB, Meredith SC, Tang W-J. Molecular basis of substrate recognition and degradation by human presequence protease. Structure. 2014;22(7):996–1007. doi: 10.1016/j.str.2014.05.003 24931469

31. Aleshin AE, Gramatikova S, Hura GL, Bobkov A, Strongin AY, Stec B, et al. Crystal and Solution Structures of a Prokaryotic M16B Peptidase: an Open and Shut Case. Structure. 17(11):1465–75. doi: 10.1016/j.str.2009.09.009 19913481

32. Johnson KA, Bhushan S, Ståhl A, Hallberg BM, Frohn A, Glaser E, et al. The closed structure of presequence protease PreP forms a unique 10 000 Å3 chamber for proteolysis. The EMBO Journal. 2006;25(9):1977–86. doi: 10.1038/sj.emboj.7601080 16601675

33. Wei Q, Ran T, Ma C, He J, Xu D, Wang W. Crystal structure and function of PqqF protein in the pyrroloquinoline quinone biosynthetic pathway. J Biol Chem. 2016;291(30):15575–87. doi: 10.1074/jbc.M115.711226 27231346

34. Tria G, Mertens HD, Kachala M, Svergun DI. Advanced ensemble modelling of flexible macromolecules using X-ray solution scattering. IUCrJ. 2015;2(2):207–17.

35. Noinaj N, Guillier M, Barnard, Travis J., Buchanan SK. TonB-Dependent Transporters: Regulation, Structure, and Function. Annu Rev Microbiol. 2010;64(1):43–60. doi: 10.1146/annurev.micro.112408.134247 20420522

36. Cascales E, Buchanan SK, Duché D, Kleanthous C, Lloubes R, Postle K, et al. Colicin biology. Microbiol Mol Biol Rev. 2007;71(1):158–229. doi: 10.1128/MMBR.00036-06 17347522

37. Grinter R, Roszak AW, Cogdell RJ, Milner JJ, Walker D. The Crystal Structure of the Lipid II-degrading Bacteriocin Syringacin M Suggests Unexpected Evolutionary Relationships between Colicin M-like Bacteriocins. J Biol Chem. 2012;287(46):38876–88. doi: 10.1074/jbc.M112.400150 22995910

38. Gómez-Santos N, Glatter T, Koebnik R, Świątek-Połatyńska MA, Søgaard-Andersen L. A TonB-dependent transporter is required for secretion of protease PopC across the bacterial outer membrane. Nature Communications. 2019;10(1):1360. doi: 10.1038/s41467-019-09366-9 30911012

39. Bolam DN, van den Berg B. TonB-dependent transport by the gut microbiota: novel aspects of an old problem. Curr Opin Struct Biol. 2018;51:35–43. doi: 10.1016/j.sbi.2018.03.001 29550504

40. Glenwright AJ, Pothula KR, Bhamidimarri SP, Chorev DS, Baslé A, Firbank SJ, et al. Structural basis for nutrient acquisition by dominant members of the human gut microbiota. Nature. 2017;541(7637):407. doi: 10.1038/nature20828 28077872

41. Meyer J. Iron–sulfur protein folds, iron–sulfur chemistry, and evolution. JBIC Journal of Biological Inorganic Chemistry. 2008;13(2):157–70. doi: 10.1007/s00775-007-0318-7 17992543

42. Munro AW, Girvan HM, McLean KJ, Cheesman MR, Leys D. Heme and Hemoproteins. Tetrapyrroles: Birth, Life and Death. New York, NY: Springer New York; 2009. p. 160–83.

43. Chen C, Natale DA, Finn RD, Huang H, Zhang J, Wu CH, et al. Representative Proteomes: A Stable, Scalable and Unbiased Proteome Set for Sequence Analysis and Functional Annotation. PLoS ONE. 2011;6(4):e18910. doi: 10.1371/journal.pone.0018910 21556138

44. Li W, Godzik A. Cd-hit: a fast program for clustering and comparing large sets of protein or nucleotide sequences. Bioinformatics. 2006;22(13):1658–9. doi: 10.1093/bioinformatics/btl158 16731699

45. Hubbard T, Barker D, Birney E, Cameron G, Chen Y, Clark L, et al. The Ensembl genome database project. Nucleic Acids Res. 2002;30(1):38–41. doi: 10.1093/nar/30.1.38 11752248

46. Apweiler R, Bairoch A, Wu CH, Barker WC, Boeckmann B, Ferro S, et al. UniProt: the universal protein knowledgebase. Nucleic Acids Res. 2004;32(suppl_1):D115–D9.

47. Miroux B, Walker JE. Over-production of proteins in Escherichia coli: mutant hosts that allow synthesis of some membrane proteins and globular proteins at high levels. Journal of molecular biology. 1996;260(3):289–98. doi: 10.1006/jmbi.1996.0399 8757792

48. Emsley P, Lohkamp B, Scott WG, Cowtan K. Features and development of Coot. Acta Crystallogr Sect D. 2010;66(4):486–501. doi: 10.1107/S0907444910007493 20383002

49. Adams PD, Afonine PV, Bunkoczi G, Chen VB, Davis IW, Echols N, et al. PHENIX: a comprehensive Python-based system for macromolecular structure solution. Acta Crystallogr Sect D. 2010;66(2):213–21. doi: 10.1107/S0907444909052925 20124702

50. Smart OS, Womack TO, Flensburg C, Keller P, Paciorek W, Sharff A, et al. Exploiting structure similarity in refinement: automated NCS and target-structure restraints in BUSTER. Acta Crystallographica Section D: Biological Crystallography. 2012;68(4):368–80.

51. Thomas DA, Francis P, Smith C, Ratcliffe S, Ede NJ, Kay C, et al. A broad‐spectrum fluorescence‐based peptide library for the rapid identification of protease substrates. Proteomics. 2006;6(7):2112–20. doi: 10.1002/pmic.200500153 16479534

52. Kirby N, Cowieson N, Hawley AM, Mudie ST, McGillivray DJ, Kusel M, et al. Improved radiation dose efficiency in solution SAXS using a sheath flow sample environment. Acta Crystallographica Section D: Structural Biology. 2016;72(12):1254–66.

53. Kirby NM, Mudie ST, Hawley AM, Cookson DJ, Mertens HD, Cowieson N, et al. A low-background-intensity focusing small-angle X-ray scattering undulator beamline. J Appl Crystallogr. 2013;46(6):1670–80.

54. Konarev PV, Volkov VV, Sokolova AV, Koch MH, Svergun DI. PRIMUS: a Windows PC-based system for small-angle scattering data analysis. J Appl Crystallogr. 2003;36(5):1277–82.

55. Datsenko KA, Wanner BL. One-step inactivation of chromosomal genes in Escherichia coli K-12 using PCR products. Proceedings of the National Academy of Sciences. 2000;97(12):6640–5.

56. Baba T, Ara T, Hasegawa M, Takai Y, Okumura Y, Baba M, et al. Construction of Escherichia coli K‐12 in‐frame, single‐gene knockout mutants: the Keio collection. Molecular systems biology. 2006;2(1).

57. Tu Q, Yin J, Fu J, Herrmann J, Li Y, Yin Y, et al. Room temperature electrocompetent bacterial cells improve DNA transformation and recombineering efficiency. Scientific reports. 2016;6:24648. doi: 10.1038/srep24648 27095488

58. Doublet B, Douard G, Targant H, Meunier D, Madec J-Y, Cloeckaert A. Antibiotic marker modifications of λ Red and FLP helper plasmids, pKD46 and pCP20, for inactivation of chromosomal genes using PCR products in multidrug-resistant strains. J Microbiol Methods. 2008;75(2):359–61. doi: 10.1016/j.mimet.2008.06.010 18619499

59. Guyer DM, Kao J-S, Mobley HL. Genomic analysis of a pathogenicity island in uropathogenic Escherichia coli CFT073: distribution of homologous sequences among isolates from patients with pyelonephritis, cystitis, and catheterassociated bacteriuria and from fecal samples. Infection and Immunity. 1998;66(9):4411–7. 9712795

60. Quan S, Hiniker A, Collet J-F, Bardwell JC. Isolation of bacteria envelope proteins. Bacterial Cell Surfaces: Springer; 2013. p. 359–66.

61. Schneider CA, Rasband WS, Eliceiri KW. NIH Image to ImageJ: 25 years of image analysis. Nature methods. 2012;9(7):671. doi: 10.1038/nmeth.2089 22930834