FİTOPATOJEN BAKTERİLERE AİT SALGI SİSTEMLERİNİN GENEL ÖZELLİKLERİ

Öz

ÖZET

 

Bakteriler çeşitli amaçlara hizmet eden protein/protein benzeri maddeleri kendi hücre membranlarından dış ortama veya direk konukçu hücrelerine aktaracak şekilde çeşitli salgı ve eksport sistemleri geliştirmişlerdir. Bu derleme de mevcut olan salgı sistemlerinin karmaşık yapıları, görevleri, hedefledikleri bölgeleri ve bakteri hücresi zarf yapılarının özellikleriyle beraber ele alınmıştır. Özellikle çok az sayıda çalışması bulunan fitopatojen bakterilerin mevcut olan salgı sistemleriyle ilgili bağlantılarının yanısıra yeni gelişmeler de sunulmuştur.     

Anahtar Kelimeler

• Bakteri,Salgı sistemi,Salgı protein

GENERAL FEATURES OF SECRETION SYSTEMS IN PHTOPATHOGEN BACTERIA

Öz

ABSTRACT

 

Bacteria have developed various secretory and export systems to translocate protein/protein-like sustances performing multiple different functions to extracellular milieu or directly to recipient cells. In this study, it was reviwed complexity of secretion systems, function, in final destination as well as structural features of bacteria cell envelope. Besides to linkage to all known bacteria secretion systems of phytopathogen bacteria, in particular with very insufficient reports, it was introduced also recent findings.    

Anahtar Kelimeler

• Bacterium,Secretion system,Secretory protein

Kaynakça

1. [1] Desvaux M, H´ebraud M, Talon R, Henderson IR. Secretion and subcellular localizations of bacterial proteins: a semantic awareness issue. Trends Microbiol 2009; 17/4: 139-145.
2. [2] Aksoy H, Kara Ç. Bitki Patojeni Bakterilerde Salgı Sistemi. Anadolu Tarım Bilim Derg 2011; 27: 48-54.
3. [3] Braun TF, McBride MJ. Flavobacterium johnsoniae GldJ is a lipoprotein that is required for gliding motility. J Bacteriol 2005; 187:2628–2637.
4. [4] Bitter W, Houben ENG, Luirink J, Appelmelk BJ. Type VII secretion in mycobacteria: classification in line with cell envelope structure. Trends Microbiol 2009; 17/8:337–38.
5. [5] Brown L, Wolf JM, Prados-Rosales R, Casadevall A. Through the wall: extracellular vesicles in Gram-positive bacteria, mycobacteria and fungi. Nat Rev Microbiol 2015; 13/10:620-630. DOI: 10.1038/nrmicro3480.
6. [6] Houben NG, Korotkov KV, Bitter W. Take five — Type VII secretion systems of Mycobacteria. Biochim Biophys Acta 2014; 1843: 1707–1716. http://dx.doi.org/10.1016/j.bbamcr.2013.11.003.
7. [7] Das C, Ghosh TS, Mande SS. Computational analysis of the ESX-1 region of Mycobacterium tuberculosis: insights into the mechanism of type VII secretion system. PLoS ONE 2011; 6/11:e27980.
8. [8] Tseng TT, Tyler BM, Setubal JC. Protein secretion systems in bacterial-host associations, and their description in the Gene Ontology. BMC Microbiol 2009; 9 Suppl 1: S2. doi: 10.1186/1471-2180-9-S1-S2.

9. [9] Natale P, Bruser T, Driessen AJ. Sec- and Tat-mediated protein secretion across the bacterial cytoplasmic membrane--distinct translocases and mechanisms. Biochim Biophys Acta 2008; 1778/9: 1735–1756.
10. [10] Wickner W, Driessen AJM, Hartl FU. The enzymology of protein translocation across the Escherichia coli plasma membrane. Ann Rev Biochem 1991; 60: 101-124.
11. [11] Driessen AJM, Manting EH, Van der Does. The structural basis of protein targeting and translocation in bacteria. Nat Struct Biol 2001; 8: 492-498.
12. [12] Osnorne AR, Rapoport B, Van den Berg. Protein translocation by the Sec61/SecY channel. Annu Rev Cell Dev Biol 2005; 21: 529-550.
13. [13] Berks BC, Palmer T, Sargent F. Protein targeting by the bacterial twin-arginine translocation (Tat) pathway. Curr Opin Microbiol 2005; 8:174-181 DOI 10.1016/j.mib.2005.02.010.
14. [14] Park E, Rapoport TA. Mechanisms of Sec61/SecY-mediated protein translocation across membranes. Annu Rev Biophys 2012; 41:21–40. [15] Palmer T, Berks BC. The twin-arginine translocation (Tat) protein export pathway. Nat Rev Microbiol 2012; 10/7: 483–96.
15. [16] Broedel SE, Papciak SM. ACESTM Signal Sequence and YebF Expression Systems Technical Brief. Athena Environmental Sciences, Inc, Baltimore, MD: 2007.
16. [17] Green ER, Mecsas J. Bacterial Secretion Systems – An overview. Microbiol spectr 2016; 4/1:10.1128/microbiolspec.VMBF-0012-2015.
17. [18] Papanikou E, Karamanou S, Economou A. Bacterial protein secretion through the translocase nanomachine. Nat Rev Microbiol 2007; 5/11: 839-851. DOI:10.1038/nrmicro1771.
18. [19] Hartl FU, Lecker S, Schiebel E, Hendrick JP, Wickner W. The binding cascade of SecB to SecA to SecY/E mediates preprotein targeting to the E. coli plasma membrane. Cell 1990; 63/2: 269–79.
19. [20] Randall LL, Hardy SJ. SecB, one small chaperone in the complex milieu of the cell. Cell Mol Life Sci 2002; 59/10: 1617–1623.
20. [21] Mogensen JE, Otzen DE. Interactions between folding factors and bacterial outer membrane proteins. Mol Microbiol 2005; 57/2: 326–346.
21. [22] Lycklama A, Nijeholt JA, Driessen AJM. The bacterial Sec-translocase: structure and mechanism. Philos Trans R Soc Lond B 2012; 367/1592: 1016–28.
22. [23] Robinson C, Bolhuis A. Tat-dependent protein targeting in prokaryotes and chloroplasts. Biochim Biophys Acta 2004; 1694(1-3): 135-47.
23. [24] Sargent F, Stanley NR, Berks BC, Palmer T. Sec-independent protein translocation in Escherichia coli. A distinct and pivotal role for the TatB protein. J Biol Chem 1999; 274/51: 36073-36082.
24. [25] Pop O, Martin U, Abel C, Müller JP. The twin-arginine signal peptide of PhoD and the TatAd/Cd proteins of Bacillus subtilis form an autonomous Tat translocation system. J Biol Chem 2002; 277/5: 3268-3273.
25. [26] Ochsner UA, Snyder A, Vasil AI, Vasil ML. Effects of the twin-arginine translocase on secretion of virulence factors, stress response, and pathogenesis. Proc Natl Acad Sci U S A 2002; 99/12: 8312-8317.
26. [27] Pradel N, Ye C, Livrelli V, Xu J, Joly B, Wu LF. Contribution of the twin arginine translocation system to the virulence of enterohemorrhagic Escherichia coli O157:H7. Infect Immun 2003; 71/9: 4908-4916.
27. [28] Lavander M, Ericsson SK, Bröms JE, Forsberg A. The twin arginine translocation system is essential for virulence of Yersinia pseudotuberculosis. Infect Immun 2006; 74/3: 1768-76.
28. [29] Thomas S, Holland IB, Schmitt L. The Type 1 secretion pathway - the hemolysin system and beyond. Biochim Biophys Acta 2014; 1843/8: 1629-1641.
29. [30] Rees DC, Johnson E, Lewinson O. ABC transporters: the power to change. Nat Rev Mol Cell Biol 2009; 10/3: 218–227.
30. [31] Jenewein S, Barry Holland I, Schmitt L. Type I Bacterial Secretion Systems. In: Bacterial Secreted Proteins: Secretory Mechanisms and Role in Pathogenesis. 2009; 45-65: Edited by Wooldridge K. Hethersett, Norwich, UK.: Caister Academic Press. [32] da Silva FG, Shen YW, Dardick C, Burdman S, Yadav RC, de Leon AL, Ronald PC. Bacterial genes involved in type I secretion and sulfation are required to elicit the rice Xa21-mediated innate immune response. Mol Plant Microbe Interact 2004; 17/6:593-601.
31. [33] Delepelaire P. Type I secretion in gram-negative bacteria. Biochim Biophys Acta 2004; 1694(1–3):149-161.
32. [34] Reddy JD, Reddy SL, Hopkins DL, Gabriel DW. TolC is required for pathogenicity of Xylella fastidiosa in Vitis vinifera grapevines. Mol Plant Microbe Interact 2007; 20/4: 403-410.
33. [35] Russo DM, Williams A, Edwards A, Posadas DM, Finnie C, Dankert M, Downie JA, Zorreguieta A. Proteins exported via the PrsDPrsE type I secretion system and the acidic exopolysaccharide are involved in biofilm formation by Rhizobium leguminosarum. J Bacteriol 2006, 188/12: 4474-4486.
34. [36] Beeckman DS, Vanrompay DC. Bacterial Secretion Systems with an Emphasis on the Chlamydial Type III Secretion System. Mol Biol 2010; 12: 17-42 doi.org/10.21775/cimb.012.017.
35. [37] Korotkov KV, Sandkvist M, Hol WG. The type II secretion system: biogenesis, molecular architecture and mechanism. Nat Rev Microbiol. 2012; 10/5: 336-51.
36. [38] Kang Y, Huang J, Mao G, He LY, Schell MA. Dramatically reduced virulence of mutants of Pseudomonas solanacearum defective in export of extracellular proteins across the outer membrane. Mol Plant-Microbe Interact 1994; 7/3: 370–77.
37. [39] Ray SK, Rajeshwari R, Sonti RV. Mutants of Xanthomonas oryzae pv. oryzae deficient in general secretory pathway are virulence deficient and unable to secrete xylanase. Mol Plant-Microbe Interact 2000; 13/4: 394–401.
38. [40] Toth IK, Bell KS, Holeva MC, Birch PRJ. Soft rot erwiniae: from genes to genomes. Mol Plant Pathol 2003; 4/1: 17–30.
39. [41] Filloux A. The underlying mechanisms of type II protein secretion. Biochim Biophys Acta 2004; 1694(1–3):163-179.
40. [42] Cianciotto NP. Type II secretion: a protein secretion system for all seasons. Trends Microbiol 2005; 13/12:581-588.
41. [43] Szczesny R, Jordan M, Schramm C, Schulz S, Cogez V, et al. Functional characterization of the Xcs and Xps type II secretion systems from the plant pathogenic bacterium Xanthomonas campestris pv vesicatoria. New Phytol 2010; 187/4: 983–1002.
42. [44] Chang JH, Desveaux D, Creason AL. ABCs and 123s Bacterial Secretion Systems of Plant Pathogenesis. Annu Rev Phytopathol 2014; 52:317–45. DOI:10.1146/annurev-phyto-011014-015624.
43. [45] Kazemi-Pour N, Condemine G, Hugouvieux-Cotte-Pattat N. The secretome of the plant pathogenic bacterium Erwinia chrysanthemi. Proteomics 2004; 4/10: 3177–86.
44. [46] Charkowski A, Blanco C, Condemine G, Expert D, Franza T, et al. The role of secretion systems and small molecules in soft-rot Enterobacteriaceae pathogenicity. Annu Rev Phytopathol 2012; 50:425–49.
45. [47] Hassan S, Shevchik VE, Robert X, Hugouvieux-Cotte-Pattat N. PelN is a new pectate lyase of Dickeya dadantii with unusual characteristics. J Bacteriol 2013; 195/10: 2197–206.
46. [48] Büttner D. Protein export according to schedule: architecture, assembly, and regulation of type III secretion systems from plant- and animal-pathogenic bacteria. Microbiol Mol Biol Rev 2012; 76/2:262–310.
47. [49] Simpson AJ, Reinach FC, Arruda P, Abreu FA, Acencio M, et al. The genome sequence of the plant pathogen Xylella fastidiosa. The Xylella fastidiosa Consortium of the Organization for Nucleotide Sequencing and Analysis. Nature 2000; 406/6792: 151–159.
48. [50] Goodner B, Hinkle G, Gattung S, Miller N, Blanchard M, et al. Genome sequence of the plant pathogen and biotechnology agent Agrobacterium tumefaciens C58. Science 2001; 294/5550:2323–28.
49. [51] Wood DW, Setubal JC, Kaul R, Monks DE, Kitajima JP, et al. The genome of the natural genetic engineer Agrobacterium tumefaciens C58. Science 2001; 294/5550: 2317–2323.
50. [52] Nykyri J, Niemi O, Koskinen P, Nokso-Koivisto J, Pasanen M, et al. Revised phylogeny and novel horizontally acquired virulence determinants of the model soft rot phytopathogen Pectobacterium wasabiae SCC3193. PLoS Pathog 2012; 8/11:e1003013.
51. [53] Loper JE, Hassan KA, Mavrodi DV, Davis EW, Lim CK, et al. Comparative genomics of plantassociated Pseudomonas spp.: insights into diversity and inheritance of traits involved in multitrophic interactions. PLoS Genet 2012; 8/7:e1002784.
52. [54] Kimbrel JA, Thomas WJ, Jiang Y, Creason AL, Thireault CA, et al. Mutualistic co-evolution of type III effector genes in Sinorhizobium fredii and Bradyrhizobium japonicum. PLoS Pathog 2013; 9/2:e1003204.
53. [55] Cornelis GR. The type III secretion injectisome. Nat Rev Microbiol 2006; 4:811-825. Doi:10.1038/nrmicro1526.
54. [56] Gerlach RG, Hensel M. Protein secretion systems and adhesins: The molecular armory of Gram-negative pathogens. Int J Med Microbiol 2007; 297:401–415.
55. [57] Alfano JR, Collmer A. Type III secretion system effector proteins: double agents in bacterial disease and plant defense. Annu Rev Phytopathol 2004; 42:385-414. DOI: 10.1146/annurev.phyto.42.040103.110731.
56. [58] Zhao Y, Qi M. Comparative genomics of Erwinia amylovora and related Erwinia species: What do we learn? Genes 2011; 2/3: 627–639.
57. [59] Genin S, Denny TP. Pathogenomics of the Ralstonia solanacearum species complex. Annu Rev Phytopathol 2012; 50:67–89.
58. [60] Bhowmick S, Tripathy SA. Tale of Effectors; Their Secretory Mechanisms and Computational Discovery in Pathogenic, Non-Pathogenic and Commensal Microbes. Mol Biol 2014; 3/118: 1-14 doi:10.4172/2168-9547.1000118.
59. [61] Backert S, Meyer TF. Type IV secretion systems and their effectors in bacterial pathogenesis. Curr Opin Microbiol 2006; 9/2: 207–217.
60. [62] Cascales E, Christie PJ. The versatile bacterial type IV secretion systems. Nat Rev Microbiol 2003; 1/2:137-49.
61. [63] Henderson IR, Navarro-Garcia F, Desvaux M, Fernandez RC, Ala'Aldeen D. Type V protein secretion pathway: the autotransporter story. Microbiol Mol Biol Rev 2004; 68/4: 692-744. DOI:10.1128/MMBR.68.4.692-744.2004.
62. [64] Christie PJ, Atmakuri K, Krishnamoorthy V, Jakubowski S, Cascales E. Biogenesis, architecture, and function of bacterial type IV secretion systems. Annu Rev Microbiol 2005; 59/1: 451–485.
63. [65] Lessl M, Lanka E. Common mechanisms in bacterial conjugation and Ti-mediated T-DNA transfer to plant cells. Cell 1994; 6: 77/3: 321-324.
64. [66] Christie P J, Cascales E. Structural and dynamic properties of bacterial type IV secretion systems. Mol Membr Biol 2005; 22(1–2): 51–61.
65. [67] Fronzes R, Christie PJ, Waksman G. The structural biology of type IV secretion systems. Nat Rev Microbiol 2009; 7/10:703-14.
66. [68] Hubber AM, Sullivan JT, Ronson CW. Symbiosis-induced cascade regulation of the Mesorhizobium loti R7A VirB/D4 type IV secretion system. Mol Plant Microbe Interact 2007; 20/3: 255-261. Doi:10.1094/MPMI-20-3-0255.
67. [69] Xu L, Luo Z Q. Cell biology of infection by Legionella pneumophila. Microbes Infect 2013; 15/2: 157–167.
68. [70] Hubber A, Roy CR. Modulation of host cell function by Legionella pneumophila type IV effectors. Annu Rev Cell Dev Biol 2010; 26: 261-283.
69. [71] Nagai H, Kubori T. Type IVB secretion systems of legionella and other Gram-negative bacteria. Front Microbiol 2011; 2: 136.
70. [72] Kubori T, Nagai H. The Type IVB secretion system: an enigmatic chimera. Curr Opin Microbiol 2016; 29: 22-29.
71. [73] Vincent CD, Friedman, JR, Jeong KC, Buford EC, Miller JL, Vogel JP. Identification of the core transmembrane complex of the Legionella Dot/Icm type IV secretion system. Mol Microbiol 2006; 62/5: 1278-1291.
72. [74] Sexton JA, Pinkner JS, Roth R, Heuser JE, Hultgren SJ, Vogel JP. The Legionella pneumophila PilT homologue DotB exhibits ATPase activity that is critical for intracellular growth. J Bacteriol 2004; 186/6: 1658–1666.
73. [75] Buscher BA, Conover GM, Miller JL, Vogel SA, Meyers S N, Isberg RR, Vogel JP. The DotL protein, a member of the TraGcoupling protein family, is essential for viability of Legionella pneumophila strain Lp02. J Bacteriol 2005; 187/9: 2927–2938.
74. [76] Duménil G, Isberg RR. The Legionella pneumophila IcmR protein exhibits chaperone activity for IcmQ by preventing its participation in high-molecular-weight complexes. Mol Microbiol 2001; 40/5: 1113–1127.
75. [77] Leyton DL, Rossiter AE, Henderson IR. From self sufficiency to dependence: mechanisms and factors important for autotransporter biogenesis. Nat Rev Microbiol 2012; 10/3: 213–225.
76. [78] Pohlner J, Halter R, Beyreuther K, Meyer TF. Gene structure and extracellular secretion of Neisseria gonorrhoeae IgA protease. Nature 1987; 325/6103: 458-62.
77. [79] Grijpstra J, Arenas J, Rutten L, Tommassen J. Autotransporter secretion: varying on a theme. Res Microbiol 2013; 164/6:562–82.
78. [80] Ruhe ZC, Low DA, Hayes CS. Bacterial contact-dependent growth inhibition. Trends Microbiol 2013; 21/5: 230–237.
79. [81] Preston GM, Studholme DJ, Caldelari I. Profiling the secretomes of plant pathogenic Proteobacteria. FEMS Microbiol Rev 2005; 29/2: 331–360.
80. [82] Rojas CM, Ham JH, Deng W-L, Doyle JJ, Collmer A. HecA, a member of a class of adhesins produced by diverse pathogenic bacteria, contributes to the attachment, aggregation, epidermal cell killing, and virulence phenotypes of Erwinia chrysanthemi EC16 on Nicotiana clevelandii seedlings. Proc Natl Acad Sci USA 2002; 99/20: 13142–13147.
81. [83] Gottig N, Garavaglia BS, Garofalo CG, Orellano EG, Ottado J. A filamentous hemagglutinin-like protein of Xanthomonas axonopodis pv. citri, the phytopathogen responsible for citrus canker, is involved in bacterial virulence. PLoS ONE 2009; 4/2:e4358.
82. [84] Voegel TM, Warren JG, Matsumoto A, Igo MM, Kirkpatrick BC. Localization and characterization of Xylella fastidiosa haemagglutinin adhesins. Microbiology 2010; 156: 2172–2179.
83. [85] Hodak H, Clantin B,Willery E, Villeret V, Locht C, Jacob-Dubuisson F. Secretion signal of the filamentous haemagglutinin, a model two-partner secretion substrate. Mol Microbiol 2006; 61/2: 368–82.
84. [86] Lambert-Buisine C, Willery E, Locht C, Jacob-Dubuisson F. N-terminal characterization of the Bordetella pertussis filamentous haemagglutinin. Mol Microbiol 1998; 28/6: 1283-93.
85. [87] McCann JR, St Geme JW 3rd. The HMW1C-like glycosyltransferases--an enzyme family with a sweet tooth for simple sugars. PLoS Pathog 2014; 10/4:e1003977.
86. [88] Waksman G, Hultgren SJ. Structural biology of the chaperone-usher pathway of pilus biogenesis. Nat Rev Microbiol 2009; 7/11: 765-774.
87. [89] Mougous JD, Cuff ME, Raunser S, Shen A, Zhou M, Gifford CA, Goodman AL, Joachimiak G, Ordoñez CL, Lory S, Walz T, Joachimiak A, Mekalanos JJ. A virulence locus of Pseudomonas aeruginosa encodes a protein secretion apparatus. Science 2006; 312/5779: 1526-30.
88. [90] Bernal P, Llamas MA, Filloux A. Type VI secretion systems in plant-associated bacteria. Environ Microbiol 2018; 20/1:1-15. doi: 10.1111/1462-2920.13956.
89. [91] Kapitein N, Mogk A. Deadly syringes: type VI secretion system activities in pathogenicity and interbacterial competition. Curr Opin Microbiol 2013; 16: 52-58.
90. [92] Pukatzki S, Ma AT, Revel AT, Sturtevant D, Mekalanos JJ. Type VI secretion system translocates a phage tail spike-like protein into target cells where it cross-links actin. Proc Natl Acad Sci U S A 2007; 104/39: 15508-15513.
91. [93] De Maayer P, Venter SN, Kamber T, Duffy B, Coutinho TA, Smits THM. Comparative genomics of the type VI secretion systems of Pantoea and Erwinia species reveals the presence of putative effector islands that may be translocated by the VgrG and Hcp proteins. BMC Genomics 2011; 12:576 doi: 10.1186/1471-2164-12-576.
92. [94] Haapalainen M, Mosorin H, Dorati F, Wu R-F, Roine E, et al. Hcp2, a secreted protein of the phytopathogen Pseudomonas syringae pv. tomato DC3000, is required for fitness for competition against bacteria and yeasts. J Bacteriol 2012; 194/18:4810–22.
93. [95] Koskiniemi S, Lamoureux JG, Nikolakakis KC, t’Kint de Roodenbeke C, Kaplan MD, et al. 2013. Rhs proteins from diverse bacteria mediate intercellular competition. Proc Natl Acad Sci USA 2013; 110/17:7032–7037.
94. [96] Hood RD, Singh P, Hsu F, Güvener T, Carl MA, Trinidad RR, Silverman JM, Ohlson BB, Hicks KG, Plemel RL, Li M, Schwarz S, Wang WY, Merz AJ, Goodlett DR, Mougous JD. A type VI secretion system of Pseudomonas aeruginosa targets a toxin to bacteria. Cell Host Microbe 2010; 7/1: 25-37. doi: 10.1016/j.chom.2009.12.007.
95. [97] Schwarz S, West TE, Boyer F, Chiang W-C, Carl MA, Hood RD, Rohmer L, Tolker-Nielsen T, Skerrett SJ, Mougous JD. Burkholderia type VI secretion systems have distinct roles in eukaryotic and bacterial cell interactions. PLoS Pathog 2010; 6, e1001068.
96. [98] Silverman JM., Brunet, YR., Cascales, E, Mougous JD. Structure and regulation of the type VI secretion system. Annu Rev Microbiol 2012; 66: 453-472.
97. [99] Basler M, Ho BT, Mekalanos JJ. Tit-for-tat: type VI secretion system counterattack during bacterial cell-cell interactions. Cell 2013; 152/4: 884-894.
98. [100] Brunet YR, Espinosa L, Harchouni S., Mignot T, Cascales E. Imaging type VI secretion-mediated bacterial killing. Cell Rep 2013; 3: 36-41.
99. [101] Hachani A, Allsopp LP, Oduko Y, Filloux A. The VgrG proteins are “A la carte” delivery systems for bacterial type VI effectors. J Biol Chem 2014; 289: 17872 17884.
100. [102] Russell AB, Wexler AG, Harding BN, Whitney JC, Bohn AJ, Goo YA, Tran BQ, Barry NA, Zheng H, Peterson SB, Chou S, Gonen T, Goodlett DR, Goodman AL, Mougous JD. A type VI secretion-related pathway in Bacteroidetes mediates interbacterial antagonism. Cell Host Microbe 2014; 16/2: 227-236. 10.1016/j.chom.2014.07.007.
101. [103] Cascales E, Cambillau C. Structural biology of type VI secretion systems. Philos Trans R Soc Lond B Biol Sci 2012; 367; 1102-1111.
102. [104] Abby SS, Cury J, Guglielmini J, Néron B, Touchon M, Rocha EPC. Identification of protein secretion systems in bacterial genomes. Sci Rep 2016; 6: 23080 doi: 10.1038/srep23080.
103. [105] Records AR. The type VI secretion system: a multipurpose delivery system with a phage-like machinery. Mol Plant-Microbe Interact 2011; 24/7: 751–57.
104. [106] WuH-Y, Chung P-C, Shih H-W,Wen S-R, Lai E-M, 2008. Secretome analysis uncovers anHcp-family protein secreted via a type VI secretion system in Agrobacterium tumefaciens. J Bacteriol 2008; 190/8: 2841–2850.
105. [107] Records AR, Gross DC. Sensor kinases RetS and LadS regulate Pseudomonas syringae type VI secretion and virulence factors. J Bacteriol 2010; 192/14: 3584–96.
106. [108] Gonz´alez A, Plener L, Restrepo S, Boucher C, Genin S. Detection and functional characterization of a large genomic deletion resulting in decreased pathogenicity in Ralstonia solanacearum race 3 biovar 2 strains. Environ Microbiol 2011; 13/12:3172–85.
107. [109] Goodfellow M, Jones AL. Bergey's Manual of Systematic Bacteriology. Actinobacteria New York, NY, USA; Springer Verlag 2012; 5: 235–243.
108. [110] Pallen MJ. The ESAT-6/WXG100 superfamily—and a new Gram-positive secretion system? Trends Microbiol 2002; 10/5: 209–212.
109. [111] Gey Van Pittius NC, Gamieldien J, Hide W, Brown GD, Siezen RJ, Beyers AD. The ESAT-6 gene cluster of Mycobacterium tuberculosis and other high G + C gram-positive bacteria. Genome Biol 2001; 2/10: research0044.1-research0044.18. [Online.]
110. [112] de Jonge MI, Pehau-Arnaudet G, Fretz MM, Romain F, Bottai D, et al. ESAT-6 from Mycobacterium tuberculosis dissociates from its putative chaperone CFP-10 under acidic conditions and exhibits membrane-lysing activity. J Bacteriol 2007 189/16:6028–34.
111. [113] van der Wel N, Hava D, Houben D, Fluitsma D, van Zon M, et al. M. tuberculosis and M. leprae translocate from the phagolysosome to the cytosol in myeloid cells. Cell 2007; 129/7: 1287–1298.
112. [114] Smith J, Manoranjan J, Pan M, Bohsali A, Xu J, et al. Evidence for pore formation in host cell membranes by ESX-1-secreted ESAT-6 and its role in Mycobacterium marinum escape from the vacuole. Infect Immun 2008; 76/12: 5478–87.
113. [115] Simeone R, Bottai D, Brosch R. ESX/type VII secretion systems and their role in host-pathogen interaction. Curr Opin Microbiol 2009; 12/1: 4–10.
114. [116] Houben D, Demangel C, van Ingen J, Perez J, Balde ´on L, et al. ESX-1-mediated translocation to the cytosol controls virulence of mycobacteria. Cell Microbiol 2012; 14/8: 1287–98.
115. [117] Simeone R, Bobard A, Lippmann J, Bitter W, Majlessi L, et al. Phagosomal rupture by Mycobacterium tuberculosis results in toxicity and host cell death. PLoS Pathog 2012; 8/2:e1002507.
116. [118] Stoop EJM, BitterW, van der Sar AM. Tubercle bacilli rely on a type VII army for pathogenicity. Trends Microbiol 2012; 20/10: 477–484.
117. [119] Fyans JK, Bignell D, Loria R, Toth I, Palmer T. The ESX/type VII secretion system modulates development, but not virulence, of the plant pathogen Streptomyces scabies. Mol Plant Pathol 2013; 14/2:119–130.
118. [120] Loferer H, Hammar M, Normark S. Availability of the fibre subunit CsgA and the nucleator protein CsgB during assembly of fibronectin-binding curli is limited by the intracellular concentration of the novel lipoprotein CsgG. Mol Microbiol 1997; 26: 11-23.
119. [121] Stathopoulos C, Hendrixson DR, Thanassi DG, Hultgren SJ, St Geme JW 3rd, Curtiss R 3rd. Secretion of virulence determinants by the general secretory pathway in gram-negative pathogens: an evolving story. Microbes Infect 2000; 2/9: 1061-1072.
120. [122] Sato K, Naito M, Yukitake H, Hirakawa H, Shoji M, McBride MJ, et al., A protein secretion system linked to bacteroidete gliding motility and pathogenesis. Proc Natl Acad Sci USA. 2010; 107: 276–281. 10.1073/pnas.0912010107.
121. [123] McBride MJ, Zhu Y. Gliding motility and Por secretion system genes are widespread among members of the phylum bacteroidetes. J Bacteriol 2013; 195: 270–278.
122. [124] Nguyen KA, Travis J, Potempa J. Does the importance of the C-terminal residues in the maturation of RgpB from Porphyromonas gingivalis reveal a novel mechanism for protein export in a subgroup of Gram Negative bacteria? J Bacteriol 2007; 189: 833–843.
123. [125] Lasica AM, Ksiazek M, Madej M, Potempa J. The Type IX Secretion System (T9SS): Highlight and Recent Insights into Its Structure and Function. Front Cell Infect Microbiol 2017; 7: 215. doi: 10.3389/fcimb.2017.00215.
124. [126] Veith PD, Glew MD, Dhana G. Gorasia DG, Reynolds EC. Type IX secretion: the generation of bacterial cell surface coatings involved in virulence, gliding motility and the degradation of complex biopolymers. Mol Microbiol 2017; 106/1: 35–53. doi:10.1111/mmi.13752.
125. [127] Sato K, Yukitake H, Narita Y, Shoji M, Naito M, Nakayama K. Identification of Porphyromonas gingivalis proteins secreted by the Por secretion system. FEMS Microbiol Lett 2013; 338: 68–76.
126. [128] Vincent MS, Canestrari MJ, Leone P, Stathopulos J, Ize B, Zoued A, Cambillau C, Kellenberger C, Roussel A, Cascales E. Characterization of the Porphyromonas gingivalis Type IX Secretion Trans-envelope PorKLMNP Core Complex. J Biol Chem 2017; 292/8: 3252-3261. doi: 10.1074/jbc.M116.765081.
127. [129] Veith PD, Nor Muhammad NA, Dashper SG, Likić VA, Gorasia DG, Chen D, Byrne SJ, Catmul DV, Reynolds EC. Protein substrates of a novel secretion system are numerous in the Bacteroidetes phylum and have in common a cleavable C-terminal secretion signal, extensive post-translational modification and cell-surface attachment. J Proteome Res 2013; 12: 4449–4461.
128. [130] Guo Y, Nguyen KA, Potempa J. Dichotomy of gingipains action as virulence factors: from cleaving substrates with the precision of a surgeon's knife to a meat chopper-like brutal degradation of proteins. Periodontol 2000 2010; 54: 15–44. 10.1111/j.1600-0757.2010.00377.x.
129. [131] McBride MJ, Nakane D. Flavobacterium gliding motility and the type IX secretion system. Curr Opin Microbiol 2015; 28: 72-77.
130. [132] Kolton M, Frenkel O, Elad Y, Cytryn E. Potential role of flavobacterial gliding-motility and type IX secretion system complex in root colonization and plant defense. Mol Plant Microbe Interact 2014; 27: 1005–1013.
131. [133] Hebbar P, Berge O, Heulin T, Singh SP. Bacterial antagonists of sunflower (Helianthus-Annuus L) fungal pathogens. Plant Soil 1991; 133: 131–140.
132. [134] Alexander BJR, Stewart A. Glasshouse screening for biological control agents of Phytophthora cactorum on apple (Malus domestica). New Zeal J Crop Hort 2001; 29:159–169.
133. [135] Sang MK, Chun SC, Kim KD. Biological control of Phytophthora blight of pepper by antagonistic rhizobacteria selected from a sequential screening procedure. Biol Control 2008; 46: 424–433.
134. [136] Gunasinghe WKRN, Karunaratne AM. Interactions of Colletotrichum musae and Lasiodiplodia theobromae and their biocontrol by Pantoea agglomerans and Flavobacterium sp in expression of crown rot of "Embul" banana. Biocontrol 2009; 54:587–596.
135. [137] Chagnot C, Zorgani MA, Astruc T, Desvaux M. Proteinaceous determinants of surface colonization in bacteria: bacterial adhesion and biofilm formation from a protein secretion perspective. Front Microbiol 2013; 4:303. doi: 10.3389/fmicb.2013.00303.
136. [138] Khokhani D, Zhang C, Li Y, Wang Q, Zeng Q, Yamazaki A, Hutchins W, Zhou SS, Chen X, Yang CH. Discovery of Plant Phenolic Compounds That Act as Type III Secretion System Inhibitors or Inducers of the Fire Blight Pathogen, Erwinia amylovora. Appl Environ Microbiol 2013; 79/18: 5424-5436. doi:10.1128/AEM.00845-13.