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Native and Foreign Proteins Secreted by the Cupriavidus metallidurans Type II System and an Alternative Mechanism

  • Xu, Houjuan (College of Plant Protection, Shandong Agricultural University) ;
  • Denny, Timothy P. (Department of Plant Pathology, The University of Georgia)
  • 투고 : 2016.11.01
  • 심사 : 2017.01.24
  • 발행 : 2017.04.28

초록

The type II secretion system (T2SS), which transports selected periplasmic proteins across the outer membrane, has rarely been studied in nonpathogens or in organisms classified as Betaproteobacteria. Therefore, we studied Cupriavidus metallidurans (Cme), a facultative chemilithoautotroph. Gel analysis of extracellular proteins revealed no remarkable differences between the wild type and the T2SS mutants. However, enzyme assays revealed that native extracellular alkaline phosphatase is a T2SS substrate, because activity was 10-fold greater for the wild type than a T2SS mutant. In Cme engineered to produce three Ralstonia solanacearum (Rso) exoenzymes, at least 95% of their total activities were extracellular, but unexpectedly high percentages of these exoenzymes remained extracellular in T2SS mutants cultured in rich broth. These conditions appear to permit an alternative secretion process, because neither cell lysis nor periplasmic leakage was observed when Cme produced a Pectobacterium carotovorum exoenzyme, and wild-type Cme cultured in minimal medium secreted 98% of Rso polygalacturonase, but 92% of this exoenzyme remained intracellular in T2SS mutants. We concluded that Cme has a functional T2SS despite lacking any abundant native T2SS substrates. The efficient secretion of three foreign exoenzymes by Cme is remarkable, but so too is the indication of an alternative secretion process in rich culture conditions. When not transiting the T2SS, we suggest that Rso exoenzymes are probably selectively packaged into outer membrane vesicles. Phylogenetic analysis of T2SS proteins supports the existence of at least three T2SS subfamilies, and we propose that Cme, as a representative of the Betaproteobacteria, could become a new useful model system for studying T2SS substrate specificity.

키워드

참고문헌

  1. Wooldridge K. 2009. Bacterial Secreted Proteins: Secretory Mechanisms and Role in Pathogenesis. Caister Academic Press, Poole, UK.
  2. Kostakioti M, Newman CL, Thanassi DG, Stathopoulos C. 2005. Mechanisms of protein export across the bacterial outer membrane. J. Bacteriol. 187: 4306-4314. https://doi.org/10.1128/JB.187.13.4306-4314.2005
  3. Bleves S, Viarre V, Salacha R, Michel GP, Filloux A, Voulhoux R. 2010. Protein secretion systems in Pseudomonas aeruginosa: a wealth of pathogenic weapons. Int. J. Med. Microbiol. 300: 534-543. https://doi.org/10.1016/j.ijmm.2010.08.005
  4. Beckwith J. 2013. The Sec-dependent pathway. Res. Microbiol. 164: 497-504. https://doi.org/10.1016/j.resmic.2013.03.007
  5. Palmer T, Berks BC. 2012. The twin-arginine translocation (Tat) protein export pathway. Nat. Rev. Microbiol. 10: 483-496. https://doi.org/10.1038/nrmicro2814
  6. Douzi B, Filloux A, Voulhoux R. 2012. On the path to uncover the bacterial type II secretion system. Phil. Trans. R. Soc. Lond. B Biol. Sci. 367: 1059-1072. https://doi.org/10.1098/rstb.2011.0204
  7. Korotkov KV, Sandkvist M, Hol WGJ. 2012. The type II secretion system: biogenesis, molecular architecture and mechanism. Nat. Rev. Microbiol. 10: 336-351. https://doi.org/10.1038/nrmicro2762
  8. Cianciotto NP. 2005. Type II secretion: a protein secretion system for all seasons. Trends Microbiol. 13: 581-588. https://doi.org/10.1016/j.tim.2005.09.005
  9. Berry JL, Pelicic V. 2015. Exceptionally widespread nanomachines composed of type IV pilins: the prokaryotic Swiss Army knives. FEMS Microbiol. Rev. 39: 134-154. https://doi.org/10.1093/femsre/fuu001
  10. McLaughlin LS, Haft RJF, Forest KT. 2012. Structural insights into the type II secretion nanomachine. Curr. Opin. Struct. Biol. 22: 208-216. https://doi.org/10.1016/j.sbi.2012.02.005
  11. Jha G, Rajeshwari R, Sonti RV. 2005. Bacterial type two secretion system secreted proteins: double-edged swords for plant pathogens. Mol. Plant Microbe Interact. 18: 891-898. https://doi.org/10.1094/MPMI-18-0891
  12. Peabody CR, Chung YJ, Yen MR, Vidal-Ingigliardi D, Pugsley AP, Saier MH. 2003. Type II protein secretion and its relationship to bacterial type IV pili and archaeal flagella. Microbiology 149: 3051-3072. https://doi.org/10.1099/mic.0.26364-0
  13. Sandkvist M. 2001. Type II secretion and pathogenesis. Infect. Immun. 69: 3523-3535. https://doi.org/10.1128/IAI.69.6.3523-3535.2001
  14. Vignon G, Kohler R, Larquet E, Giroux S, Prevost MC, Roux P, Pugsley AP. 2003. Type IV-like pili formed by the type II secreton: specificity, composition, bundling, polar localization, and surface presentation of peptides. J. Bacteriol. 185: 3416-3428. https://doi.org/10.1128/JB.185.11.3416-3428.2003
  15. 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. https://doi.org/10.1038/nsmb.1426
  16. Douzi B, Durand E, Bernard C, Alphonse S, Cambillau C, Filloux A, et al. 2009. The XcpV/GspI pseudopilin has a central role in the assembly of a quaternary complex within the T2SS pseudopilus. J. Biol. Chem. 284: 34580-34589. https://doi.org/10.1074/jbc.M109.042366
  17. Nivaskumar M, Francetic O. 2014. Type II secretion system: a magic beanstalk or a protein escalator. Biochim. Biophys. Acta 1843: 1568-1577. https://doi.org/10.1016/j.bbamcr.2013.12.020
  18. Korotkov KV, Gonen T, Hol WGJ. 2011. Secretins: dynamic channels for protein transport across membranes. Trends Biochem. Sci. 36: 433-443. https://doi.org/10.1016/j.tibs.2011.04.002
  19. Login FH, Fries M, Wang X, Pickersgill RW, Shevchik VE. 2010. A 20-residue peptide of the inner membrane protein OutC mediates interaction with two distinct sites of the outer membrane secretin OutD and is essential for the functional type II secretion system in Erwinia chrysanthemi. Mol. Microbiol. 76: 944-955. https://doi.org/10.1111/j.1365-2958.2010.07149.x
  20. Korotkov KV, Johnson TL, Jobling MG, Pruneda J, Pardon E, Heroux A, et al. 2011. Structural and functional studies on the interaction of GspC and GspD in the type II secretion system. PLoS Pathog. 7: e1002228. https://doi.org/10.1371/journal.ppat.1002228
  21. Wang X, Pineau C, Gu S, Guschinskaya N, Pickersgill RW, Shevchik VE. 2012. Cysteine scanning mutagenesis and disulfide mapping analysis of arrangement of GspC and GspD protomers within the type 2 secretion system. J. Biol. Chem. 287: 19082-19093. https://doi.org/10.1074/jbc.M112.346338
  22. Gu S, Kelly G, Wang XH, Frenkiel T, Shevchik VE, Pickersgill RW. 2012. Solution structure of homology region (HR) domain of type II secretion system. J. Biol. Chem. 287: 9072-9080. https://doi.org/10.1074/jbc.M111.300624
  23. Douzi B, Ball G, Cambillau C, Tegoni M, Voulhoux R. 2011. Deciphering the Xcp Pseudomonas aeruginosa type II secretion machinery through multiple interactions with substrates. J. Biol. Chem. 286: 40792-40801. https://doi.org/10.1074/jbc.M111.294843
  24. Denny TP. 2006. Plant pathogenic Ralstonia species, pp. 573-644. In Gnanamanickam SS (ed.). Plant-Associated Bacteria. Springer, Dordrecht, The Netherlands.
  25. Liu H, Zhang S, Schell MA, Denny TP. 2005. Pyramiding unmarked mutations in Ralstonia solanacearum shows that secreted proteins in addition to plant cell wall degrading enzymes contribute to virulence. Mol. Plant Microbe Interact. 18: 1296-1305. https://doi.org/10.1094/MPMI-18-1296
  26. Tsujimoto S, Nakaho K, Adachi M, Ohnishi K, Kiba A, Hikichi Y. 2008. Contribution of the type II secretion system in systemic infectivity of Ralstonia solanacearum through xylem vessels. J. Gen. Plant Pathol. 74: 71-75. https://doi.org/10.1007/s10327-007-0061-5
  27. Poueymiro M, Genin S. 2009. Secreted proteins from Ralstonia solanacearum: a hundred tricks to kill a plant. Curr. Opin. Microbiol. 12: 44-52. https://doi.org/10.1016/j.mib.2008.11.008
  28. Evans FF, Egan S, Kjelleberg S. 2008. Ecology of type II secretion in marine Gammaproteobacteria. Environ. Microbiol. 10: 1101-1107. https://doi.org/10.1111/j.1462-2920.2007.01545.x
  29. Silver S, Mergeay M. 2009. Introduction to a special Festschrift issue celebrating the microbiology of Cupriavidus metallidurans strain CH34. Antonie Van Leeuwenhoek 96: 113-114. https://doi.org/10.1007/s10482-009-9357-0
  30. von Rozycki T, Nies DH. 2009. Cupriavidus metallidurans: evolution of a metal-resistant bacterium. Antonie Van Leeuwenhoek 96: 115-139. https://doi.org/10.1007/s10482-008-9284-5
  31. Janssen PJ, Van Houdt R, Moors H, Monsieurs P, Morin N, Michaux A, et al. 2010. The complete genome sequence of Cupriavidus metallidurans strain CH34, a master survivalist in harsh and anthropogenic environments. PLoS One 5: e10433. https://doi.org/10.1371/journal.pone.0010433
  32. Monsieurs P, Provoost A, Mijnendonckx K, Leys N, Gaudreau C, Van HR. 2013. Genome sequence of Cupriavidus metallidurans strain H1130, isolated from an invasive human infection. Genome Announc. 1: e01051-13.
  33. Mergeay M, Nies D, Schlegel HG, Gerits J, Charles P, Vangijsegem F. 1985. Alcaligenes eutrophus CH34 is a facultative chemolithotroph with plasmid-bound resistance to heavy metals. J. Bacteriol. 162: 328-334.
  34. Mergeay M, Monchy S, Vallaeys T, Auquier V, Benotmane A, Bertin P, et al. 2003. Ralstonia metallidurans, a bacterium specifically adapted to toxic metals: towards a catalogue of metal-responsive genes. FEMS Microbiol. Rev. 27: 385-410. https://doi.org/10.1016/S0168-6445(03)00045-7
  35. Garg RP, Yindeeyoungyeon W, Gilis A, Denny TP, van der Lelie D, Schell MA. 2000. Evidence that Ralstonia eutropha (Alcaligenes eutrophus) contains a functional homologue of the Ralstonia solanacearum Phc cell density sensing system. Mol. Microbiol. 38: 359-367. https://doi.org/10.1046/j.1365-2958.2000.02131.x
  36. Miller JH. 1972. Experiments in Molecular Genetics. Cold Spring Harbor Laboratory Press, Cold Spring Harbor, NY. USA.
  37. Clough SJ, Schell MA, Denny TP. 1994. Evidence for involvement of a volatile extracellular factor in Pseudomonas solanacearum virulence gene expression. Mol. Plant Microbe Interact. 7: 621-630. https://doi.org/10.1094/MPMI-7-0621
  38. Cote RJ, Gherna RL. 1994. Nutrition and media, pp. 155-178. In Gerhardt P, Murray RGE, Woodard S, Krimm U (eds.). Methods for General and Molecular Bacteriology. American Society for Microbiology, Washington, DC. USA.
  39. Manoil C. 1991. Analysis of membrane protein topology using alkaline phosphatase and beta-galactosidase gene fusions. Methods Cell Biol. 34: 61-75.
  40. Denny TP, Makini FW, Brumbley SM. 1988. Characterization of Pseudomonas solanacearum Tn5 mutants deficient in extracellular polysaccharide. Mol. Plant Microbe Interact. 1: 215-223. https://doi.org/10.1094/MPMI-1-215
  41. Mukasa H, Tsumori H, Takeda H. 1994. Renaturation and activity staining of glycosidases and glycosyltransferases in gels after sodium dodecyl sulfate-electrophoresis. Electrophoresis 15: 911-915. https://doi.org/10.1002/elps.11501501131
  42. Altschul SF, Madden TL, Schäffer AA, Zhang J, Zhang Z, Webb M, Lipman DJ. 1997. Gapped BLAST and PSI-BLAST: a new generation of protein database search programs. Nucleic Acids Res. 25: 3389-3402. https://doi.org/10.1093/nar/25.17.3389
  43. Gerard-Vincent M, Robert V, Ball G, Bleves S, Michel GP, Lazdunski A, Filloux A. 2002. Identification of XcpP domains that confer functionality and specificity to the Pseudomonas aeruginosa type II secretion apparatus. Mol. Microbiol. 44: 1651-1665. https://doi.org/10.1046/j.1365-2958.2002.02991.x
  44. Korotkov KV, Krumm B, Bagdasarian M, Hol WGJ. 2006. Structural and functional studies of EpsC, a crucial component of the type 2 secretion system from Vibrio cholerae. J. Mol. Biol. 363: 311-321. https://doi.org/10.1016/j.jmb.2006.08.037
  45. Marchler-Bauer A, Lu SN, Anderson JB, Chitsaz F, Derbyshire MK, DeWeese-Scott C, et al. 2011. CDD: a Conserved Domain Database for the functional annotation of proteins. Nucleic Acids Res. 39: D225-D229. https://doi.org/10.1093/nar/gkq1189
  46. Cole C, Barber JD, Barton GJ. 2008. The Jpred 3 secondary structure prediction server. Nucleic Acids Res. 36: W197-W201. https://doi.org/10.1093/nar/gkn238
  47. Login FH, Shevchik VE. 2006. The single transmembrane segment drives self-assembly of OutC and the formation of a functional type II secretion system in Erwinia chrysanthemi. J. Biol. Chem. 281: 33152-33162. https://doi.org/10.1074/jbc.M606245200
  48. Lupas A, Vandyke M, Stock J. 1991. Predicting coiled coils from protein sequences. Science 252: 1162-1164. https://doi.org/10.1126/science.252.5009.1162
  49. Bleves S, Gerard-Vincent M, Lazdunski A, Filloux A. 1999. Structure-function analysis of XcpP, a component involved in general secretory pathway-dependent protein secretion in Pseudomonas aeruginosa. J. Bacteriol. 181: 4012-4019.
  50. Lee H-M, Chen JR, Lee HL, Leu W-M, Chen L-Y, Hu N-T. 2004. Functional dissection of the XpsN (GspC) protein of the Xanthomonas campestris pv. campestris type II secretion machinery. J. Bacteriol. 186: 2946-2955. https://doi.org/10.1128/JB.186.10.2946-2955.2004
  51. Corbett M, Virtue S, Bell K, Birch P, Burr T, Hyman L, et al. 2005. Identification of a new quorum-sensing-controlled virulence factor in Erwinia carotovora subsp. atroseptica secreted via the type II targeting pathway. Mol. Plant Microbe Interact. 18: 334-342. https://doi.org/10.1094/MPMI-18-0334
  52. DebRoy S, Dao J, Soderberg M, Rossier O, Cianciotto NP. 2006. Legionella pneumophila type II secretome reveals unique exoproteins and a chitinase that promotes bacterial persistence in the lung. Proc. Natl. Acad. Sci. USA 103: 19146-19151. https://doi.org/10.1073/pnas.0608279103
  53. Harding CM, Kinsella RL, Palmer LD, Skaar EP, Feldman MF. 2016. Medically relevant Acinetobacter species require a type II secretion system and specific membrane-associated chaperones for the export of multiple substrates and full virulence. PLoS. Pathog. 12: e1005391. https://doi.org/10.1371/journal.ppat.1005391
  54. Michel GPF, Durand E, Filloux A. 2007. XphA/XqhA, a novel GspCD subunit for type II secretion in Pseudomonas aeruginosa. J. Bacteriol. 189: 3776-3783. https://doi.org/10.1128/JB.00205-07
  55. Ball G, Durand E, Lazdunski A, Filloux A. 2002. A novel type II secretion system in Pseudomonas aeruginosa. Mol. Microbiol. 43: 475-485. https://doi.org/10.1046/j.1365-2958.2002.02759.x
  56. de Groot A, Krijger JJ, Filloux A, Tommassen J. 1996. Characterization of type II protein secretion (xcp) genes in the plant growth-stimulating Pseudomonas putida, strain WCS358. Mol. Gen. Genet. 250: 491-504.
  57. Putker F, Tommassen-van BR, Stork M, Rodriguez-Herva JJ, Koster M, Tommassen J. 2013. The type II secretion system (Xcp) of Pseudomonas putida is active and involved in the secretion of phosphatases. Environ. Microbiol. 15: 2658-2671.
  58. d'Enfert C, Pugsley AP. 1989. Klebsiella pneumoniae pulS gene encodes an outer membrane lipoprotein required for pullulanase secretion. J. Bacteriol. 171: 3673-3679. https://doi.org/10.1128/jb.171.7.3673-3679.1989
  59. Cadoret F, Ball G, Douzi B, Voulhoux R. 2014. Txc, a new type II secretion system of Pseudomonas aeruginosa strain PA7, is regulated by the TtsS/TtsR two-component system and directs specific secretion of the CbpE chitin-binding protein. J. Bacteriol. 196: 2376-2386. https://doi.org/10.1128/JB.01563-14
  60. Ball G, Viarre V, Garvis S, Voulhoux R, Filloux A. 2012. Type II-dependent secretion of a Pseudomonas aeruginosa DING protein. Res. Microbiol. 163: 457-469. https://doi.org/10.1016/j.resmic.2012.07.007
  61. Ferrandez Y, Condemine G. 2008. Novel mechanism of outer membrane targeting of proteins in gram-negative bacteria. Mol. Microbiol. 69: 1349-1357. https://doi.org/10.1111/j.1365-2958.2008.06366.x
  62. Mulcahy H, Charron-Mazenod L, Lewenza S. 2010. Pseudomonas aeruginosa produces an extracellular deoxyribonuclease that is required for utilization of DNA as a nutrient source. Environ. Microbiol. 12: 1621-1629.
  63. Py B, Salmond GPC, Chippaux M, Barras F. 1991. Secretion of cellulases in Erwinia chrysanthemi and E. carotovora is species-specific. FEMS Microbiol. Lett. 79: 315-322. https://doi.org/10.1111/j.1574-6968.1991.tb04548.x
  64. Lindeberg M, Salmond GPC, Collmer A. 1996. Complementation of deletion mutations in a cloned functional cluster of Erwinia chrysanthemi out genes with Erwinia carotovora out homologues reveals OutC and OutD as candidate gatekeepers of species-specific secretion of proteins via the type II pathway. Mol. Microbiol. 20: 175-190. https://doi.org/10.1111/j.1365-2958.1996.tb02499.x
  65. Lindeberg M, Boyd CM, Keen NT, Collmer A. 1998. External loops at the C terminus of Erwinia chrysanthemi pectate lyase C are required for species-specific secretion through the Out type II pathway. J. Bacteriol. 180: 1431-1437.
  66. Bouley J, Condemine G, Shevchik VE. 2001. The PDZ domain of OutC and the N-terminal region of OutD determine the secretion specificity of the type II Out pathway of Erwinia chrysanthemi. J. Mol. Biol. 308: 205-219. https://doi.org/10.1006/jmbi.2001.4594
  67. Pineau C, Guschinskaya N, Robert X, Gouet P, Ballut L, Shevchik VE. 2014. Substrate recognition by the bacterial type II secretion system: more than a simple interaction. Mol. Microbiol. 94: 126-140. https://doi.org/10.1111/mmi.12744
  68. Michel LO, Sandkvist M, Bagdasarian M. 1995. Specificity of the protein secretory apparatus: secretion of the heat-labile enterotoxin-B subunit pentamers by different species of gram-bacteria. Gene 152: 41-45. https://doi.org/10.1016/0378-1119(94)00691-K
  69. de Groot A, Koster M, Gerard-Vincent M, Gerritse G, Lazdunski A, Tommassen J, Filloux A. 2001. Exchange of Xcp (Gsp) secretion machineries between Pseudomonas aeruginosa and Pseudomonas alcaligenes: species specificity unrelated to substrate recognition. J. Bacteriol. 183: 959-967. https://doi.org/10.1128/JB.183.3.959-967.2001
  70. Connell TD, Metzger DJ, Wang M, Jobling MG, Holmes RK. 1995. Initial studies of the structural signal for extracellular transport of cholera toxin and other proteins recognized by Vibrio cholerae. Infect. Immun. 63: 4091-4098.
  71. Palomaki T, Pickersgill R, Riekki R, Romantschuk M, Saarilahti HT. 2002. A putative three-dimensional targeting motif of polygalacturonase (PehA), a protein secreted through the type II (GSP) pathway in Erwinia carotovora. Mol. Microbiol. 43: 585-596. https://doi.org/10.1046/j.1365-2958.2002.02793.x
  72. Ried JL, Collmer A. 1986. Comparison of pectic enzymes produced by Erwinia chrysanthemi, Erwinia carotovora subsp. carotovora, and Erwinia carotovora subsp. atroseptica. Appl. Environ. Microbiol. 52: 305-310.
  73. Staskawicz B, Dahlbeck D, Keen N, Napoli C. 1987. Molecular characterization of cloned avirulence genes from race 0 and race 1 of Pseudomonas syringae pv. glycinea. J. Bacteriol. 169: 5789-5794. https://doi.org/10.1128/jb.169.12.5789-5794.1987
  74. Ditta G, Stanfield S, Corbin D, Helinski DR. 1980. Broad host range DNA cloning system for gram-negative bacteria: construction of a gene bank of Rhizobium meliloti. Proc. Natl. Acad. Sci. USA 77: 7347-7351. https://doi.org/10.1073/pnas.77.12.7347
  75. Vanbleu E, Marchal K, Vanderleyden J. 2004. Genetic and physical map of the pLAFR1 vector. DNA Seq. 15: 225-227. https://doi.org/10.1080/10425170410001723949
  76. Possot OM, Vignon G, Bomchil N, Ebel F, Pugsley AP. 2000. Multiple interactions between pullulanase secreton components involved in stabilization and cytoplasmic membrane association of PulE. J. Bacteriol. 182: 2142-2152. https://doi.org/10.1128/JB.182.8.2142-2152.2000
  77. DeShazer D, Brett PJ, Burtnick MN, Woods DE. 1999. Molecular characterization of genetic loci required for secretion of exoproducts in Burkholderia pseudomallei. J. Bacteriol. 181: 4661-4664.
  78. Fehlner-Gardiner CC, Hopkins TMH, Valvano MA. 2002. Identification of a general secretory pathway in a human isolate of Burkholderia vietnamiensis (formerly B. cepacia complex genomovar V) that is required for the secretion of hemolysin and phospholipase C activities. Microb. Pathogo. 32: 249-254. https://doi.org/10.1006/mpat.2002.0503
  79. Somvanshi VS, Viswanathan P, Jacobs JL, Mulks MH, Sundin GW, Ciche TA. 2010. The type 2 secretion pseudopilin, gspJ, is required for multihost pathogenicity of Burkholderia cenocepacia AU1054. Infect. Immun. 78: 4110-4121. https://doi.org/10.1128/IAI.00558-10
  80. Chowdhury PR, Heinemann JA. 2006. The general secretory pathway of Burkholderia gladioli pv. agaricicola BG164R is necessary for cavity disease in white button mushrooms. Appl. Environ. Microbiol. 72: 3558-3565. https://doi.org/10.1128/AEM.72.5.3558-3565.2006
  81. Durand E, Alphonse S, Brochier-Armanet C, Ball G, Douzi B, Filloux A, et al. 2011. The assembly mode of the pseudopilus: a hallmark to distinguish a novel secretion system subtype. J. Biol. Chem. 286: 24407-24416. https://doi.org/10.1074/jbc.M111.234278
  82. Rossier O, Starkenburg SR, Cianciotto NP. 2004. Legionella pneumophila type II protein secretion promotes virulence in the A/J mouse model of Legionnaires' disease pneumonia. Infect. Immun. 72: 310-321. https://doi.org/10.1128/IAI.72.1.310-321.2004
  83. Luo H, Benner R, Long RA, Hu J. 2009. Subcellular localization of marine bacterial alkaline phosphatases. Proc. Natl. Acad. Sci. USA 106: 21219-21223. https://doi.org/10.1073/pnas.0907586106
  84. Ragot SA, Kertesz MA, Bunemann EK. 2015. phoD alkaline phosphatase gene diversity in soil. Appl. Environ. Microbiol. 81: 7281-7289. https://doi.org/10.1128/AEM.01823-15
  85. Tan H, Barret M, Mooij MJ, Rice O, Morrissey JP, Dobson A, et al. 2013. Long-term phosphorus fertilisation increased the diversity of the total bacterial community and the phoD phosphorus mineraliser group in pasture soils. Biol. Fert. Soils 49: 661-672. https://doi.org/10.1007/s00374-012-0755-5
  86. Sole M, Scheibner F, Hoffmeister AK, Hartmann N, Hause G, Rother A, et al. 2015. Xanthomonas campestris pv. vesicatoria secretes proteases and xylanases via the Xps type II secretion system and outer membrane vesicles. J. Bacteriol. 197: 2879-2893. https://doi.org/10.1128/JB.00322-15
  87. Tseng H-T. 2010. Evaluating the GspC protein in substrate specificity of Ralstonia solanacearum type II secretion. Dissertation for the University of Georgia, Athens, GA, USA.
  88. Huang J, Schell MA. 1990. Evidence that extracellular export of the endoglucanase encoded by egl of Pseudomonas solanacearum occurs by a two-step process involving a lipoprotein intermediate. J. Biol. Chem. 265: 11628-11632.
  89. East A, Mechaly AE, Huysmans GH, Bernarde C, Tello-Manigne D, Nadeau N, et al. 2016. Structural basis of pullulanase membrane binding and secretion revealed by X-ray crystallography, molecular dynamics and biochemical analysis. Structure 24: 92-104. https://doi.org/10.1016/j.str.2015.10.023
  90. Szczesny R, Jordan M, Schramm C, Schulz S, Cogez V, Bonas U, Buttner D. 2010. Functional characterization of the Xcs and Xps type II secretion systems from the plant pathogenic bacterium Xanthomonas campestris pv. vesicatoria. New Phytol. 187: 983-1002. https://doi.org/10.1111/j.1469-8137.2010.03312.x
  91. Martinez A, Ostrovsky P, Nunn DN. 1998. Identification of an additional member of the secretin superfamily of proteins in Pseudomonas aeruginosa that is able to function in type II protein secretion. Mol. Microbiol. 28: 1235-1246. https://doi.org/10.1046/j.1365-2958.1998.00888.x
  92. Kulp A, Kuehn MJ. 2010. Biological functions and biogenesis of secreted bacterial outer membrane vesicles. Annu. Rev. Microbiol. 64: 163-184. https://doi.org/10.1146/annurev.micro.091208.073413
  93. Schwechheimer C, Kulp A, Kuehn MJ. 2014. Modulation of bacterial outer membrane vesicle production by envelope structure and content. BMC. Microbiol. 14: 324. https://doi.org/10.1186/s12866-014-0324-1
  94. Allan ND, Kooi C, Sokol PA, Beveridge TJ. 2003. Putative virulence factors are released in association with membrane vesicles from Burkholderia cepacia. Can. J. Microbiol. 49: 613-624. https://doi.org/10.1139/w03-078
  95. Altindis E, Fu Y, Mekalanos JJ. 2014. Proteomic analysis of Vibrio cholerae outer membrane vesicles. Proc. Natl. Acad. Sci. USA 111: E1548-E1556. https://doi.org/10.1073/pnas.1403683111
  96. Chapon V, Czjzek M, El Hassouni M, Py B, Juy M, Barras F. 2001. Type II protein secretion in gram-negative pathogenic bacteria: the study of the structure/secretion relationships of the cellulase Cel5 (formerly EGZ) from Erwinia chrysanthemi. J. Mol. Biol. 310: 1055-1066. https://doi.org/10.1006/jmbi.2001.4787
  97. Francetic O, Pugsley AP. 2005. Towards the identification of type II secretion signals in a nonacylated variant of pullulanase from Klebsiella oxytoca. J. Bacteriol. 187: 7045-7055. https://doi.org/10.1128/JB.187.20.7045-7055.2005
  98. Yanisch-Perron C, Vieira J, Messing J. 1985. Improved M13 phage cloning vectors and host strains: nucleotide sequences of the M13mp18 and pUC19 vectors. Gene 33: 103-119. https://doi.org/10.1016/0378-1119(85)90120-9
  99. Kovach ME, Elzer PH, Hill DS, Robertson GT, Farris MA, Roop RM, II, Peterson KM. 1995. Four new derivatives of the broad-host-range cloning vector pBBR1MCS, carrying different antibiotic-resistance cassettes. Gene 166: 175-176. https://doi.org/10.1016/0378-1119(95)00584-1
  100. Cardona ST, Valvano MA. 2005. An expression vector containing a rhamnose-inducible promoter provides tightly regulated gene expression in Burkholderia cenocepacia. Plasmid 54: 219-228. https://doi.org/10.1016/j.plasmid.2005.03.004
  101. Muyrers JPP, Zhang Y, Stewart AF. 2001. Techniques: recombinogenic engineering - new options for cloning and manipulating DNA. Trends. Biochem. Sci. 26: 325-331. https://doi.org/10.1016/S0968-0004(00)01757-6
  102. Garcia-Pedrajas MD, Nadal M, Denny T, Baeza-Montanez L, Paz Z, Gold SE. 2010. DelsGate: a robust and rapid method for gene deletion, pp. 55-76. In Sharon A (ed.). Molecular and Cell Biology Methods for Fungi. Humana Press, New York.
  103. Kitten T, Willis DK. 1996. Suppression of a sensor kinase-dependent phenotype in Pseudomonas syringae by ribosomal proteins L35 and L20. J. Bacteriol. 178: 1548-1555. https://doi.org/10.1128/jb.178.6.1548-1555.1996
  104. Schell MA, Roberts DP, Denny TP. 1988. Analysis of the Pseudomonas solanacearum polygalacturonase encoded by pglA and its involvement in phytopathogenicity. J. Bacteriol. 170: 4501-4508. https://doi.org/10.1128/jb.170.10.4501-4508.1988
  105. Brumbley SM, Carney BF, Denny TP. 1993. Phenotype conversion in Pseudomonas solanacearum due to spontaneous inactivation of PhcA, a putative LysR transcriptional activator. J. Bacteriol. 175: 5477-5487. https://doi.org/10.1128/jb.175.17.5477-5487.1993
  106. Saitou N, Nei M. 1987. The neighbor-joining method: a new method for reconstructing phylogenetic trees. Mol. Biol. Evol. 4: 406-425.
  107. Felsenstein J. 1988. Phylogenies from molecular sequences: inference and reliability. Annu. Rev. Genet. 22: 521-565. https://doi.org/10.1146/annurev.ge.22.120188.002513
  108. Nei M, Kumar S. 2000. Molecular Evolution and Phylogenetics. Oxford University Press, New York.
  109. Tamura K, Stecher G, Peterson D, Filipski A, Kumar S. 2013. MEGA6: Molecular Evolutionary Genetics Analysis version 6.0. Mol. Biol. Evol. 30: 2725-2729. https://doi.org/10.1093/molbev/mst197

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