Identification of protein secretion systems in bacterial genomes

Scientific Reports

Volumn 6, Issue , 2016, Pages

  Abby, Sophie S ^a,b,c   Cury, Jean ^a,b   Guglielmini, Julien ^a,b   Néron, Bertrand ^a   Touchon, Marie ^a,b   Rocha, Eduardo P C ^a,b  

^a INSTITUT PASTEUR   (France)

^b CNRS   (France)

^c UNIVERSITY OF VIENNA   (Austria)

Author keywords

[No Author keywords available]

Indexed keywords

BACTERIAL PROTEIN; LIPOPOLYSACCHARIDE; PROTEIN TRANSLOCASE;

BACTERIAL GENOME; BACTERIUM; BIOLOGICAL MODEL; CELL MEMBRANE; CLASSIFICATION; GENETICS; METABOLISM; PHYLOGENY;

BACTERIA; BACTERIAL PROTEINS; CELL MEMBRANE; GENOME, BACTERIAL; LIPOPOLYSACCHARIDES; MODELS, GENETIC; PHYLOGENY; PROTEIN TRANSLOCATION SYSTEMS;

EID: 84961176515     PISSN: None     EISSN: 20452322     Source Type: Journal    
DOI: 10.1038/srep23080     Document Type: Article

References (123)

1. Wandersman, C. & Delepelaire, P. Bacterial iron sources: from siderophores to hemophores. Annu. Rev. Microbiol. 58, 611 (2004).
2. Ruhe, Z. C., Low, D. A. & Hayes, C. S. Bacterial contact-dependent growth inhibition. Trends Microbiol. 21, 230 (2013).
3. Viprey, V., Del Greco, A., Golinowski, W., Broughton, W. J. & Perret, X. Symbiotic implications of type III protein secretion machinery in Rhizobium. Mol. Microbiol. 28, 1381 (1998).
4. Ma, W. & Guttman, D. S. Evolution of prokaryotic and eukaryotic virulence effectors. Curr. Opin. Plant Biol. 11, 412 (2008).
5. Raymond, B. et al. Subversion of trafficking, apoptosis, and innate immunity by type III secretion system effectors. Trends Microbiol. 21, 430 (2013).
6. Bleves, S. et al. Protein secretion systems in Pseudomonas aeruginosa: A wealth of pathogenic weapons. Int. J. Med. Microbiol. 300, 534 (2010).
7. Dalbey, R. E. & Kuhn, A. Protein traffic in Gram-negative bacteria-how exported and secreted proteins find their way. FEMS Microbiol. Rev. 36, 1023 (2012).
8. Chang, J. H., Desveaux, D. & Creason, A. L. The ABCs and 123s of bacterial secretion systems in plant pathogenesis. Annu Rev Phytopathol 52, 317 (2014).
9. Sato, K. et al. A protein secretion system linked to bacteroidete gliding motility and pathogenesis. Proc. Natl. Acad. Sci. USA 107, 276 (2010).
10. McBride, M. J. & Zhu, Y. Gliding motility and Por secretion system genes are widespread among members of the phylum bacteroidetes. J. Bacteriol. 195, 270 (2013).
11. Desvaux, M., Hebraud, M., Talon, R. & Henderson, I. R. Secretion and subcellular localizations of bacterial proteins: a semantic awareness issue. Trends Microbiol. 17, 139 (2009).
12. Abdallah, A. M. et al. Type VII secretion-mycobacteria show the way. Nat. Rev. Microbiol. 5, 883 (2007).
13. Tseng, T. T., Tyler, B. M. & Setubal, J. C. Protein secretion systems in bacterial-host associations, and their description in the Gene Ontology. BMC Microbiol. 9 Suppl 1, S2 (2009).
14. Planet, P. J., Kachlany, S. C., DeSalle, R. & Figurski, D. H. Phylogeny of genes for secretion NTPases: identification of the widespread tadA subfamily and development of a diagnostic key for gene classification. Proc. Natl. Acad. Sci. USA 98, 2503 (2001).
15. Minamino, T. & Namba, K. Self-assembly and type III protein export of the bacterial flagellum. J. Mol. Microbiol. Biotechnol. 7, 5 (2004).
16. Pelicic, V. Type IV pili: e pluribus unum? Mol. Microbiol. 68, 827 (2008).
17. Peabody, C. R. et al. Type II protein secretion and its relationship to bacterial type IV pili and archaeal flagella. Microbiology 149, 3051 (2003).
18. Nogueira, T., Touchon, M. & Rocha, E. P. Rapid evolution of the sequences and gene repertoires of secreted proteins in bacteria. PLoS ONE 7, e49403 (2012).
19. Gophna, U., Ron, E. Z. & Graur, D. Bacterial type III secretion systems are ancient and evolved by multiple horizontal-transfer events. Gene 312, 151 (2003).
20. Boyer, F., Fichant, G., Berthod, J., Vandenbrouck, Y. & Attree, I. Dissecting the bacterial type VI secretion system by a genome wide in silico analysis: what can be learned from available microbial genomic resources? BMC Genomics 10, 104 (2009).
21. Ren, C. P. et al. The ETT2 gene cluster, encoding a second type III secretion system from Escherichia coli, is present in the majority of strains but has undergone widespread mutational attrition. J. Bacteriol. 186, 3547 (2004).
22. Huynen, M., Snel, B., Lathe, W., 3rd & Bork, P. Predicting protein function by genomic context: quantitative evaluation and qualitative inferences. Genome Res. 10, 1204 (2000).
23. Wolf, Y. I., Rogozin, I. B., Kondrashov, A. S. & Koonin, E. V. Genome alignment, evolution of prokaryotic genome organization, and prediction of gene function using genomic context. Genome Res. 11, 356 (2001).
24. Abby, S. S. & Rocha, E. P. The non-flagellar type III secretion system evolved from the bacterial flagellum and diversified into hostcell adapted systems. PLoS Genet. 8, e1002983 (2012).
25. Abby, S. S., Neron, B., Menager, H., Touchon, M. & Rocha, E. P. MacSyFinder: A Program to Mine Genomes for Molecular Systems with an Application to CRISPR-Cas Systems. PLoS ONE 9, e110726 (2014).
26. Yen, M. R. et al. Protein-translocating outer membrane porins of Gram-negative bacteria. Biochim. Biophys. Acta 1562, 6 (2002).
27. Pallen, M. J., Beatson, S. A. & Bailey, C. M. Bioinformatics, genomics and evolution of non-flagellar type-III secretion systems: a Darwinian perspective. FEMS Microbiol. Rev. 29, 201 (2005).
28. Cianciotto, N. P. Type II secretion: a protein secretion system for all seasons. Trends Microbiol. 13, 581 (2005).
29. Saier, M. H., Ma, C. H., Rodgers, L., Tamang, D. G. & Yen, M. R. Protein secretion and membrane insertion systems in bacteria and eukaryotic organelles. Adv. Appl. Microbiol. 65, 141 (2008).
30. Guglielmini, J., de la Cruz, F. & Rocha, E. P. Evolution of conjugation and type IV secretion systems. Mol. Biol. Evol. 30, 315 (2013).
31. Barret, M., Egan, F. & O'Gara, F. Distribution and diversity of bacterial secretion systems across metagenomic datasets. Environmental microbiology reports 5, 117 (2013).
32. Delepelaire, P. Type I secretion in gram-negative bacteria. Biochim. Biophys. Acta 1694, 149 (2004).
33. Bouige, P., Laurent, D., Piloyan, L. & Dassa, E. Phylogenetic and functional classification of ATP-binding cassette (ABC) systems. Curr. Protein Pept. Sci. 3, 541 (2002).
34. Dassa, E. & Bouige, P. The ABC of ABCS: a phylogenetic and functional classification of ABC systems in living organisms. Res. Microbiol. 152, 211 (2001).
35. Jacob-Dubuisson, F., Fernandez, R. & Coutte, L. Protein secretion through autotransporter and two-partner pathways. Biochim. Biophys. Acta 1694, 235 (2004).
36. Henderson, I. R., Navarro-Garcia, F., Desvaux, M., Fernandez, R. C. & Ala'Aldeen, D. Type V protein secretion pathway: the autotransporter story. Microbiol. Mol. Biol. Rev. 68, 692 (2004).
37. Linke, D., Riess, T., Autenrieth, I. B., Lupas, A. & Kempf, V. A. Trimeric autotransporter adhesins: variable structure, common function. Trends Microbiol. 14, 264 (2006).
38. Tomich, M., Planet, P. J. & Figurski, D. H. The tad locus: postcards from the widespread colonization island. Nat. Rev. Microbiol. 5, 363 (2007).
39. Broms, J. E., Sjostedt, A. & Lavander, M. The Role of the Francisella Tularensis Pathogenicity Island in Type VI Secretion, Intracellular Survival, and Modulation of Host Cell Signaling. Front. Microbiol. 1, 136 (2010).
40. Russell, A. B. et al. A Type VI Secretion-Related Pathway in Bacteroidetes Mediates Interbacterial Antagonism. Cell Host Microbe 16, 227 (2014).
41. Eddy, S. R. Accelerated Profile HMM Searches. PLoS Comput. Biol. 7, e1002195 (2011).
42. Johnson, L. S., Eddy, S. R. & Portugaly, E. Hidden Markov model speed heuristic and iterative HMM search procedure. BMC Bioinformatics 11, 431 (2010).
43. Martinez-Garcia, P. M., Ramos, C. & Rodriguez-Palenzuela, P. T346Hunter: a novel web-based tool for the prediction of type III, type IV and type VI secretion systems in bacterial genomes. PLoS ONE 10, e0119317 (2015).
44. Holland, I. B., Schmitt, L. & Young, J. Type 1 protein secretion in bacteria, the ABC-transporter dependent pathway. Mol. Membr. Biol. 22, 29 (2005).
45. Kanonenberg, K., Schwarz, C. K. & Schmitt, L. Type I secretion systems-a story of appendices. Res. Microbiol. 164, 596 (2013).
46. Paulsen, I. T., Park, J. H., Choi, P. S. & Saier, M. H. Jr. A family of gram-negative bacterial outer membrane factors that function in the export of proteins, carbohydrates, drugs and heavy metals from gram-negative bacteria. FEMS Microbiol. Lett. 156, 1 (1997).
47. Dinh, T., Paulsen, I. T. & Saier, M. H. Jr. A family of extracytoplasmic proteins that allow transport of large molecules across the outer membranes of gram-negative bacteria. J. Bacteriol. 176, 3825 (1994).
48. Dassa, E. Natural history of ABC systems: not only transporters. Essays Biochem. 50, 19 (2011).
49. Davidson, A. L., Dassa, E., Orelle, C. & Chen, J. Structure, function, and evolution of bacterial ATP-binding cassette systems. Microbiol. Mol. Biol. Rev. 72, 317 (2008).
50. Koronakis, V., Eswaran, J. & Hughes, C. Structure and function of TolC: the bacterial exit duct for proteins and drugs. Annu. Rev. Biochem. 73, 467 (2004).
51. Burland, V. et al. The complete DNA sequence and analysis of the large virulence plasmid of Escherichia coli O157:H7. Nucleic Acids Res. 26, 4196 (1998).
52. Korotkov, K. V., Sandkvist, M. & Hol, W. G. The type II secretion system: biogenesis, molecular architecture and mechanism. Nat. Rev. Microbiol. 10, 336 (2012).
53. Nivaskumar, M. & Francetic, O. Type II secretion system: a magic beanstalk or a protein escalator. Biochim. Biophys. Acta 1843, 1568 (2014).
54. Cianciotto, N. P. Many substrates and functions of type II secretion: lessons learned from Legionella pneumophila. Future Microbiol. 4, 797 (2009).
55. Karaba, S. M., White, R. C. & Cianciotto, N. P. Stenotrophomonas maltophilia Encodes a Type II Protein Secretion System That Promotes Detrimental Effects on Lung Epithelial Cells. Infect. Immun. 81, 3210 (2013).
56. Zhilina, T. N. & Zavarzin, G. A. Extremely halophilic, methylotrophic, anaerobic bacteria. FEMS Microbiol. Lett. 87, 315 (1990).
57. Rondelet, A. & Condemine, G. Type II secretion: the substrates that won't go away. Res. Microbiol. 164, 556 (2013).
58. Galan, J. E. & Wolf-Watz, H. Protein delivery into eukaryotic cells by type III secretion machines. Nature 444, 567 (2006).
59. Cornelis, G. R. The type III secretion injectisome. Nat. Rev. Microbiol. 4, 811 (2006).
60. Ginocchio, C. C., Olmsted, S. B., Wells, C. L. & Galan, J. E. Contact with epithelial cells induces the formation of surface appendages on Salmonella typhimurium. Cell 76, 717 (1994).
61. Van Gijsegem, F. et al. The hrp gene locus of Pseudomonas solanacearum, which controls the production of a type III secretion system, encodes eight proteins related to components of the bacterial flagellar biogenesis complex. Mol. Microbiol. 15, 1095 (1995).
62. Young, G. M., Schmiel, D. H. & Miller, V. L. A new pathway for the secretion of virulence factors by bacteria: the flagellar export apparatus functions as a protein-secretion system. Proc. Natl. Acad. Sci. USA 96, 6456 (1999).
63. Sun, G. W. & Gan, Y. H. Unraveling type III secretion systems in the highly versatile Burkholderia pseudomallei. Trends Microbiol. 18, 561 (2010).
64. Hansen-Wester, I. & Hensel, M. Salmonella pathogenicity islands encoding type III secretion systems. Microbes Infect. 3, 549 (2001).
65. Alvarez-Martinez, C. E. & Christie, P. J. Biological diversity of prokaryotic type IV secretion systems. Microbiol. Mol. Biol. Rev. 73, 775 (2009).
66. de la Cruz, F., Frost, L. S., Meyer, R. J. & Zechner, E. Conjugative DNA Metabolism in Gram-negative Bacteria. FEMS Microbiol. Rev. 34, 18 (2010).
67. Guglielmini, J. et al. Key components of the eight classes of type IV secretion systems involved in bacterial conjugation or protein secretion. Nucleic Acids Res (2014).
68. Dautin, N. & Bernstein, H. D. Protein Secretion in Gram-Negative Bacteria via the Autotransporter Pathway. Annu. Rev. Microbiol. 61, 89 (2007).
69. Mazar, J. & Cotter, P. A. New insight into the molecular mechanisms of two-partner secretion. Trends Microbiol. 15, 508 (2007).
70. Leyton, D. L., Rossiter, A. E. & Henderson, I. R. From self sufficiency to dependence: mechanisms and factors important for autotransporter biogenesis. Nat. Rev. Microbiol. 10, 213 (2012).
71. Leo, J. C., Grin, I. & Linke, D. Type V secretion: mechanism(s) of autotransport through the bacterial outer membrane. Philos. Trans. R. Soc. Lond. B. Biol. Sci. 367, 1088 (2012).
72. Salacha, R. et al. The Pseudomonas aeruginosa patatin-like protein PlpD is the archetype of a novel Type V secretion system. Environ. Microbiol. 12, 1498 (2010).
73. Oberhettinger, P. et al. Intimin and invasin export their C-terminus to the bacterial cell surface using an inverse mechanism compared to classical autotransport. PLoS ONE 7, e47069 (2012).
74. Ruer, S., Ball, G., Filloux, A. & de Bentzmann, S. The 'P-usher', a novel protein transporter involved in fimbrial assembly and TpsA secretion. EMBO J. 27, 2669 (2008).
75. Mougous, J. D. et al. A virulence locus of Pseudomonas aeruginosa encodes a protein secretion apparatus. Science 312, 1526 (2006).
76. Hood, R. D. et al. A type VI secretion system of Pseudomonas aeruginosa targets a toxin to bacteria. Cell Host Microbe 7, 25 (2010).
77. Schwarz, S. et al. Burkholderia type VI secretion systems have distinct roles in eukaryotic and bacterial cell interactions. PLoS Pathog. 6, e1001068 (2010).
78. Silverman, J. M., Brunet, Y. R., Cascales, E. & Mougous, J. D. Structure and regulation of the type VI secretion system. Annu. Rev. Microbiol. 66, 453 (2012).
79. Basler, M., Ho, B. T. & Mekalanos, J. J. Tit-for-tat: type VI secretion system counterattack during bacterial cell-cell interactions. Cell 152, 884 (2013).
80. Brunet, Y. R., Espinosa, L., Harchouni, S., Mignot, T. & Cascales, E. Imaging type VI secretion-mediated bacterial killing. Cell reports 3, 36 (2013).
81. Hachani, A., Allsopp, L. P., Oduko, Y. & Filloux, A. The VgrG proteins are "A la carte" delivery systems for bacterial type VI effectors. J. Biol. Chem. 289, 17872 (2014).
82. Cascales, E. & Cambillau, C. Structural biology of type VI secretion systems. Philos. Trans. R. Soc. Lond. B. Biol. Sci. 367, 1102 (2012).
83. Shneider, M. M. et al. PAAR-repeat proteins sharpen and diversify the type VI secretion system spike. Nature 500, 350 (2013).
84. Pukatzki, S., Ma, A. T., Revel, A. T., Sturtevant, D. & Mekalanos, J. J. Type VI secretion system translocates a phage tail spike-like protein into target cells where it cross-links actin. Proc. Natl. Acad. Sci. USA 104, 15508 (2007).
85. Whitney, J. C. et al. Genetically distinct pathways guide effector export through the type VI secretion system. Mol. Microbiol. 92, 529 (2014).
86. Nano, F. E. et al. A Francisella tularensis pathogenicity island required for intramacrophage growth. J. Bacteriol. 186, 6430 (2004).
87. Ludu, J. S. et al. The Francisella pathogenicity island protein PdpD is required for full virulence and associates with homologues of the type VI secretion system. J. Bacteriol. 190, 4584 (2008).
88. Barker, J. R. et al. The Francisella tularensis pathogenicity island encodes a secretion system that is required for phagosome escape and virulence. Mol. Microbiol. 74, 1459 (2009).
89. Camacho, C. et al. BLAST +: architecture and applications. BMC Bioinformatics 10, 421 (2009).
90. Soding, J. Protein homology detection by HMM-HMM comparison. Bioinformatics 21, 951 (2005).
91. Finn, R. D. et al. The Pfam protein families database. Nucleic Acids Res. 36, D281 (2008).
92. Quevillon, E. et al. InterProScan: protein domains identifier. Nucleic Acids Res. 33, W116 (2005).
93. Kharade, S. S. & McBride, M. J. Flavobacterium johnsoniae PorV is required for secretion of a subset of proteins targeted to the type IX secretion system. J. Bacteriol. 197, 147 (2015).
94. Moslavac, S. et al. A TolC-like protein is required for heterocyst development in Anabaena sp. strain PCC 7120. J. Bacteriol. 189, 7887 (2007).
95. Staron, P., Forchhammer, K. & Maldener, I. Structure-function analysis of the ATP-driven glycolipid efflux pump DevBCA reveals complex organization with TolC/HgdD. FEBS Lett. 588, 395 (2014).
96. Rauschenbach, I., Yee, N., Haggblom, M. M. & Bini, E. Energy metabolism and multiple respiratory pathways revealed by genome sequencing of Desulfurispirillum indicum strain S5. Environ. Microbiol. 13, 1611 (2011).
97. Zeng, L. et al. Extracellular proteome analysis of Leptospira interrogans serovar Lai. Omics: a journal of integrative biology 17, 527 (2013).
98. Nguyen, B. D. & Valdivia, R. H. Virulence determinants in the obligate intracellular pathogen Chlamydia trachomatis revealed by forward genetic approaches. Proc. Natl. Acad. Sci. USA 109, 1263 (2012).
99. Schatz, D. et al. Self-suppression of biofilm formation in the cyanobacterium Synechococcus elongatus. Environ. Microbiol. 15, 1786 (2013).
100. Hager, A. J. et al. Type IV pili-mediated secretion modulates Francisella virulence. Mol. Microbiol. 62, 227 (2006).
101. Huber, R. et al. Thermotoga maritima sp. nov. represents a new genus of unique extremely thermophilic eubacteria growing up to 90 C. Arch. Microbiol. 144, 324 (1986).
102. Petrus, A. K. et al. Genes for the major structural components of Thermotogales species' togas revealed by proteomic and evolutionary analyses of OmpA and OmpB homologs. PLoS ONE 7, e40236 (2012).
103. Sutcliffe, I. C. A phylum level perspective on bacterial cell envelope architecture. Trends Microbiol. 18, 464 (2010).
104. Francke, C. et al. Comparative analyses imply that the enigmatic Sigma factor 54 is a central controller of the bacterial exterior. BMC Genomics 12, 385 (2011).
105. Vesth, T. et al. Veillonella, Firmicutes: Microbes disguised as Gram negatives. Stand Genomic Sci 9, 431 (2013).
106. Haft, D. H. et al. TIGRFAMs and Genome Properties in 2013. Nucleic Acids Res. 41, D387 (2013).
107. Guglielmini, J., Quintais, L., Garcillan-Barcia, M. P., de la Cruz, F. & Rocha, E. P. The Repertoire of ICE in Prokaryotes Underscores the Unity, Diversity, and Ubiquity of Conjugation. PLoS Genet. 7, e1002222 (2011).
108. Neron, B. et al. Mobyle: a new full web bioinformatics framework. Bioinformatics 25, 3005 (2009).
109. Nunn, D. N. & Lory, S. Product of the Pseudomonas aeruginosa gene pilD is a prepilin leader peptidase. Proc. Natl. Acad. Sci. USA 88, 3281 (1991).
110. Pepe, C. M., Eklund, M. W. & Strom, M. S. Cloning of an Aeromonas hydrophila type IV pilus biogenesis gene cluster: complementation of pilus assembly functions and characterization of a type IV leader peptidase/N-methyltransferase required for extracellular protein secretion. Mol. Microbiol. 19, 857 (1996).
111. Marsh, J. W. & Taylor, R. K. Identification of the Vibrio cholerae type 4 prepilin peptidase required for cholera toxin secretion and pilus formation. Mol. Microbiol. 29, 1481 (1998).
112. Christie, P. J. Type IV secretion: the Agrobacterium VirB/D4 and related conjugation systems. Biochim. Biophys. Acta 1694, 219 (2004).
113. Nagai, H. & Kubori, T. Type IVB Secretion Systems of Legionella and Other Gram-Negative Bacteria. Front. Microbiol. 2, 136 (2011).
114. Schroder, G., Schuelein, R., Quebatte, M. & Dehio, C. Conjugative DNA transfer into human cells by the VirB/VirD4 type IV secretion system of the bacterial pathogen Bartonella henselae. Proc. Natl. Acad. Sci. USA 108, 14643 (2011).
115. Abby, S. S., Tannier, E., Gouy, M. & Daubin, V. Lateral gene transfer as a support for the tree of life. Proc. Natl. Acad. Sci. USA 109, 4962 (2012).
116. Yutin, N., Puigbo, P., Koonin, E. V. & Wolf, Y. I. Phylogenomics of prokaryotic ribosomal proteins. PLoS ONE 7, e36972 (2012).
117. Wu, D. et al. A phylogeny-driven genomic encyclopaedia of Bacteria and Archaea. Nature 462, 1056 (2009).
118. Boussau, B., Gueguen, L. & Gouy, M. Accounting for horizontal gene transfers explains conflicting hypotheses regarding the position of aquificales in the phylogeny of Bacteria. BMC Evol. Biol. 8, 272 (2008).
119. Souza, R. C. et al. AtlasT4SS: a curated database for type IV secretion systems. BMC Microbiol. 12, 172 (2012).
120. Bi, D. et al. SecReT4: a web-based bacterial type IV secretion system resource. Nucleic Acids Res. 41, D660 (2013).
121. Li, J. et al. SecReT6: a web-based resource for type VI secretion systems found in bacteria. Environ. Microbiol. 17, 2196 (2015).
122. Pundhir, S. & Kumar, A. SSPred: A prediction server based on SVM for the identification and classification of proteins involved in bacterial secretion systems. Bioinformation 6, 380 (2011).
123. Wang, Y., Huang, H., Sun, M., Zhang, Q. & Guo, D. T3DB: an integrated database for bacterial type III secretion system. BMC Bioinformatics 13, 66 (2012).