Genomic analysis of secretion systems

Current Opinion in Microbiology

Volumn 6, Issue 5, 2003, Pages 519-527

  Pallen, Mark J ^a   Chaudhuri, Roy R ^a   Henderson, Ian R ^a  

^a UNIVERSITY OF BIRMINGHAM   (United Kingdom)

Author keywords

[No Author keywords available]

Indexed keywords

DOCKING PROTEIN; TRANSACTIVATOR PROTEIN;

BACTERIAL MEMBRANE; BIFIDOBACTERIUM LONGUM; CELL MEMBRANE; CHLAMYDOPHILA; CHLAMYDOPHILA CAVIAE; CLOSTRIDIUM TETANI; ESCHERICHIA COLI; EXTRACELLULAR MATRIX; FUSOBACTERIUM NUCLEATUM; GENE CLUSTER; GENE EXPRESSION REGULATION; GENE SEQUENCE; GENETIC CODE; GENOMICS; HOST PATHOGEN INTERACTION; NONHUMAN; PROTEIN DOMAIN; PROTEIN SECRETION; PROTEIN TARGETING; PSEUDOMONAS PUTIDA; RALSTONIA SOLANACEARUM; REGULATORY MECHANISM; REVIEW; SEQUENCE ANALYSIS; SEQUENCE HOMOLOGY; SHIGELLA FLEXNERI; STREPTOCOCCUS AGALACTIAE; TRANSPORT KINETICS;

BACTERIA (MICROORGANISMS); BIFIDOBACTERIUM; BIFIDOBACTERIUM LONGUM; CHLAMYDOPHILA; CHLAMYDOPHILA CAVIAE; CLOSTRIDIUM; CLOSTRIDIUM TETANI; ESCHERICHIA COLI; EUKARYOTA; FUSOBACTERIUM; FUSOBACTERIUM NUCLEATUM; NEGIBACTERIA; POSIBACTERIA; PSEUDOMONAS; PSEUDOMONAS PUTIDA; RALSTONIA; RALSTONIA SOLANACEARUM; SHIGELLA; SHIGELLA FLEXNERI; STREPTOCOCCUS; STREPTOCOCCUS AGALACTIAE;

EID: 0242291971     PISSN: 13695274     EISSN: None     Source Type: Journal    
DOI: 10.1016/j.mib.2003.09.005     Document Type: Review

References (74)

1. Cao TB, Saier MH Jr: The general protein secretory pathway: phylogenetic analyses leading to evolutionary conclusions. Biochim Biophys Acta 2003, 1609:115-125.
2. Lenz LL, Portnoy DA: Identification of a second Listeria secA gene associated with protein secretion and the rough phenotype. Mol Microbiol 2002, 45:1043-1056. The authors describe the identification and characterization of a second seca gene in Listeria monocytogenes, which has a function distinct from the orthodox seca gene. They show that the Listeria SecA2 is involved in smooth-rough phenotypic variation and contributes to bacterial virulence.
3. Braunstein M, Espinosa BJ, Chan J, Belisle JT: SecA2 functions in the secretion of superoxide dismutase A and in the virulence of Mycobacterium tuberculosis. Mol Microbiol 2003, 48:453-464. The authors describe the identification and characterization of a second seca gene in Mycobacterium tuberculosis. They show that second mycobacterial SecA contributes to the secretion of superoxide dismutase, even though this protein lacks a traditional signal sequence. They also show their SecA2 to be associated with bacterial virulence in mice.
4. Sijbrandi R, Urbanus ML, ten Hagen-Jongman CM, Bernstein HD, Oudega B, Otto BR, Luirink J: Signal recognition particle (SRP)-mediated targeting and Sec-dependent translocation of an extracellular Escherichia coli protein. J Biol Chem 2003, 278:4654-4659. This study provides evidence that haemoglobin protease, an autotransporter from E. coli with an unusually long signal peptide, requires a functional SRP pathway for optimal translocation across the inner membrane.
5. Yen MR, Tseng YH, Nguyen EH, Wu LF, Saier MH Jr: Sequence and phylogenetic analyses of the twin-arginine targeting (Tat) protein export system. Arch Microbiol 2002, 177:441-450.
6. van Dijl JM, Braun PG, Robinson C, Quax WJ, Antelmann H, Hecker M, Muller J, Tjalsma H, Bron S, Jongbloed JD: Functional genomic analysis of the Bacillus subtilis Tat pathway for protein secretion. J Biotechnol 2002, 98:243-254.
7. Dilks K, Rose RW, Hartmann E, Pohlschroder M: Prokaryotic utilization of the twin-arginine translocation pathway: a genomic survey. J Bacteriol 2003, 185:1478-1483.
8. Ball G, Durand E, Lazdunski A, Filloux A: A novel type II secretion system in Pseudomonas aeruginosa. Mol Microbiol 2002, 43:475-485. A description of a second type II secretion system (hxc) from Pseudomonas aeruginosa strain PAO1 that exports an alkaline phosphatase and is regulated In response to phosphate levels. This provides the first example of two functioning type II systems in the same cell.
9. Iwobi A, Heesemann J, Garcia E, Igwe E, Noelting C, Rakin A: Novel virulence-associated type II secretion system unique to high-pathogenicity Yersinia enterocolitica. Infect Immun 2003, 71:1872-1879.
10. Hensel M, Shea JE, Gleeson C, Jones MD, Dalton E, Holden DW: Simultaneous identification of bacterial virulence genes by negative selection. Science 1995, 269:400-403.
11. Makino K, Oshima K, Kurokawa K, Yokoyama K, Uda T, Tagomori K, Lijima Y, Najima M, Nakano M, Yamashita A et al.: Genome sequence of Vibrio parahaemolyticus: a pathogenic mechanism distinct from that of V. cholerae. Lancet 2003, 361;743-749. Genome sequencing reveals a new type-III secretion system in Vibrio parahaemolyticus that sets it apart from its relative Vibrio cholerae.
12. Stevens MP, Wood MW, Taylor LA, Monaghan P, Hawes P, Jones PW, Wallis TS, Galyov EE: An Inv/Mxi-Spa-like type III protein secretion system in Burkholderia pseudomallei modulates intracellular behaviour of the pathogen. Mol Microbiol 2002, 46:649-659. A demonstration that a novel Spi-1-like TTSS from Burkholderia is functional and likely to be involved in virulence. Mutants lacking a functional system showed reduced replication in macrophage-like cells were unable to escape from endocytic vacuoles and showed a complete absence of formation of membrane protrusions and actin tails.
13. Rainbow L, Hart CA, Winstanley C: Distribution of type III secretion gene clusters in Burkholderia pseudomallei, B. thailandensis and B. mallei. J Med Microbiol 2002, 51:374-384.
14. Foultier B, Troisfontaines P, Muller S, Opperdoes FR, Cornelis GR: Characterization of the Ysa pathogenicity locus in the chromosome of Yersinia enterocolitica and phylogeny analysis of type III secretion systems. J Mol Evol 2002, 55:37-51.
15. Young BM, Young GM: Evidence for targeting of Yop effectors by the chromosomally encoded Ysa type III secretion system of Yersinia enterocolitica. J Bacteriol 2002, 184:5563-5571.
16. Foultier B, Troisfontaines P, Vertommen D, Marenne MN, Rider M, Parsot C, Cornelis GR: Identification of substrates and chaperone from the Yersinia enterocolitica 1B Ysa type III secretion system. Infect Immun 2003, 71:242-253.
17. Burr SE, Stuber K, Wahli T, Frey J: Evidence for a type III secretion system in Aeromonas salmonicida subsp. salmonicida. J Bacteriol 2002, 184:5966-5970. These authors show that Aeromonas contains a TTSS that is required for virulence and secretes an ADP-ribosyltransferase.
18. Stuber K, Frey J, Burnens AP, Kuhnert P: Detection of type III secretion genes as a general indicator of bacterial virulence. Mol Cell Probes 2003, 17:25-32.
19. Freiberg C, Fellay R, Bairoch A, Broughton WJ, Rosenthal A, Perret X: Molecular basis of symbiosis between Rhizobium and legumes. Nature 1997, 387:394-401.
20. Marie C, Broughton WJ, Deakin WJ: Rhizobium type III secretion systems: legume charmers or alarmers? Curr Opin Plant Biol 2001, 4:336-342.
21. Ffrench-Constant RH, Waterfield N, Burland V, Perna NT, Daborn PJ, Bowen D, Blattner FR: A genomic sample sequence of the entomopathogenic bacterium Photorhabdus luminescens W14: potential implications for virulence. Appl Environ Microbiol 2000, 66:3310-3329.
22. Dale C, Young SA, Haydon DT, Welburn SC: The insect endosymbiont Sodalis glossinidius utilizes a type III secretion system for cell invasion. Proc Natl Acad Scow USA 2001, 98:1883-1888.
23. Dale C, Plague GR, Wang B, Ochman H, Moran NA: Type III secretion systems and the evolution of mutualistic endosymbiosis. Proc Natl Acad Scow USA 2002, 99:12397-12402. A second example of a TTSS in an insect endosymbiont. Genes encoding the system are up-regulated under conditions that coincide with host cell invasion.
24. Collmer A, Lindeberg M, Petnicki-Ocwieja T, Schneider DJ, Alfano JR: Genomic mining type III secretion system effectors in Pseudomonas syringae yields new picks for all TTSS prospectors. Trends Microbiol 2002, 10:462-469. Reviews the stunning progress in identifying TTSS effectors using a variety of genome-mining approaches.
25. Zwiesler-Vollick J, Plovanich-Jones AE, Nomura K, Bandyopadhyay S, Joardar V, Kunkel BN, He SY: Identification of novel hrp-regulated genes through functional genomic analysis of the Pseudomonas syringae pv. tomato DC3000 genome. Mol Microbiol 2002, 45:1207-1218. Using a search motif based on promoter sequences, 73 hrp-regulated genes were predicted in the genome sequence. Follow-up studies including gene expression and type III translocation assays provide evidence that some of the novel genes are HrpS-regulated and encode putative effector proteins.
26. Fouts DE, Abramovitch RB, Alfano JR, Baldo AM, Buell CR, Cartinhour S, Chatterjee AK, D'Ascenzo M, Gwinn ML, Lazarowitz SG et al.: Genome wide identification of Pseudomonas syringae pv. tomato DC3000 promoters controlled by the HrpL alternative sigma factor. Proc Natl Acad Scow USA 2002, 99:2275-2280. The authors used an iterative process involving computational and gene expression techniques to identify virulence-implicated genes downstream of HrpL-responsive promoters. They identified several novel putative effectors and some non-TTSS HrpL-regulated genes.
27. Pallen M, Chaudhuri R, Khan A: Bacterial FHA domains: neglected players in the phospho-threonine signalling game? Trends Microbiol 2002, 10:556-563. Evidence is provided of FHA domains in some type-III secreted proteins, hinting at a link between reversible phospho-threonine modifications and regulation of secretion. A serine-threonine protein kinase is encoded in a TTSS gene cluster in chlamydia.
28. Pallen MJ, Francis MS, Fütterer K: Tetratricopeptide-like repeats in type-III-secretion chaperones and regulators. FEMS Microbiol Lett 2003, in press. PSI-BLAST searches and multiple alignments provide compelling evidence of the presence of alk-α-helical arrays, encoded by 34 amino acid tetratricopeptide repeats in the 'chaperones-of-the-translocators' class of TTSS chaperones. This paper provides clear structural demarcation of this class from other TTSS chaperones of known structure. Homology modes lay the foundation for future structure-function studies of chaperone-substrate interaction.
29. Pallen MJ: Glucoamylase-like domains within the regulatory subunits of phosphorylase kinase. Protein Scow 2003, in press. A bioinformatics study of a putative effector from E. coli sheds light on the function of the mammalian enzyme phosphorylase kinase.
30. Ward DV, Draper O, Zupan JR, Zambryski PC: Peptide linkage mapping of the Agrobacterium tumefaciens vir-encoded type IV secretion system reveals protein subassemblies. Proc Natl Acad Scow USA 2002, 99:11493-11500.
31. Sanchez DO, Zandomeni RO, Cravero S, Verdun RE, Pierrou E, Faccio P, Diaz G, Lanzavecchia S, Aguero F, Frasch AC et al.: Gene discovery through genomic sequencing of Brucella abortus. Infect Immun 2001, 69:865-868.
32. Seubert A, Schulein R, Dehio C: Bacterial persistence within erythrocytes: a unique pathogenic strategy of Bartonella spp. Int J Med Microbiol 2002, 291:555-560.
33. Ohashi N, Zhi N, Lin Q, Rikihisa Y: Characterization and transcriptional analysis of gene clusters for a type IV secretion machinery in human granulocytic and monocytic ehrlichiosis agents. Infect Immun 2002, 70:2128-2138.
34. Sullivan JT, Trzebiatowski JR, Cruickshank RW, Gouzy J, Brown SD, Elliot RM, Fleetwood DJ, McCallum NG, Rossbach U, Stuart GS et al.: Comparative sequence analysis of the symbiosis island of Mesorhizobium loti strain R7A. J Bacteriol 2002, 184:3086-3095.
35. Cao TB, Saier MH Jr: Conjugal type IV macromolecular transfer systems of Gram-negative bacteria: organismal distribution, structural constraints and evolutionary conclusions. Microbiology 2001, 147:3201-3214.
36. Van Sluys MA, Monteiro-Vitorello CB, Camargo LE, Menck CF, Da Silva AC, Ferro JA, Oliveira MC, Setubal JC, Kitajima JP, Simpson AJ: Comparative genomic analysis of plant-associated bacteria. Annu Rev Phytopathol 2002, 40:169-189.
37. Ma Q, Zhai Y, Schneider JC, Ramseier TM, Saier MH: Protein secretion systems of Pseudomonas aeruginosa and P. fluorescens. Biochim Biophys Acta 2003, 1611:223-233.
38. Yen MR, Peabody CR, Partovi SM, Zhai Y, Tseng YH, Saier MH: Protein-translocating outer membrane porins of Gram-negative bacteria. Biochim Biophys Acta 2002, 1562:6-31.
39. Henderson IR, Lam AC: Polymorphic proteins of Chlamydia spp.-autotransporters beyond the Proteobacteria. Trends Microbiol 2001, 9:573-578.
40. Vandahl BB, Pedersen AS, Gevaert K, Holm A, Vandekerckhove J, Christiansen G, Birkelund S: The expression, processing and localization of polymorphic membrane proteins in Chlamydia pneumoniae strain CWL02. BMC Microbiol 2002, 2:36.
41. Stothard DR, Toth GA, Batteiger BE: Polymorphic membrane protein H has evolved in parallel with the three disease-causing groups of Chlamydia trachomatis. Infect Immun 2003, 71:1200-1208.
42. Welch RA, Burland V, Plunkett G III, Redford P, Roesch P, Rasko D, Buckles EL, Liou SR, Boutin A, Hackett J et al.: Extensive mosaic structure revealed by the complete genome sequence of uropathogenic Escherichia coli. Proc Natl Acad Scow USA 2002, 99:17020-17024.
43. van Ulsen P, van Alphen L, Hopman CT, van der Ende A, Tommassen J: In vivo expression of Neisseria meningitidis proteins homologous to the Haemophilus influenzae Hap and Hia autotransporters. FEMS Immunol Med Microbiol 2001, 32:53-64.
44. Turner DP, Wooldridge KG, Ala'Aldeen DA: Autotransported serine protease A of Neisseria meningitidis: an immunogenic, surface-exposed outer membrane, and secreted protein. Infect Immun 2002, 70:4447-4461.
45. Pizza M, Scarlato V, Masignani V, Giuliani MM, Arico B, Comanducci M, Jennings GT, Baldi L, Bartolini E, Capecchi B et al.: Identification of vaccine candidates against serogroup B meningococcus by whole-genome sequencing. Science 2000, 287:1816-1820.
46. Rojas CM, Ham JH, Deng WL, 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 Scow USA 2002, 99:13142-13147.
47. 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:RESEARCH0044.
48. Pallen MJ: The ESAT-6/WXG100 superfamily-and a new Gram-positive secretion system? Trends Microbiol 2002, 10:209-212. Extends a previous study [47] by showing that genes encoding large membrane-bound ATPases and ESAT-6-like proteins cluster within many diverse Gram-positive genomes, including Bacillus subtilis, Staphylococcus aureus, Clostridium acetobutylicum and Listeria. Adds great weight to the idea that the YukA-like ATPase forms the core of a dedicated secretion system in Gram-positive bacteria.
49. Pallen MJ, Lam AC, Antonio M, Dunbar K: An embarrassment of sortases - a richness of substrates? Trends Microbiol 2001, 9:97-102.
50. Roche FM, Massey R, Peacock SJ, Day NP, Visai L, Speziale P, Lam A, Pallen M, Foster TJ: Characterization of novel LPXTG-containing proteins of Staphylococcus aureus identified from genome sequences. Microbiology 2003, 149:643-654.
51. Lee SG, Pancholi V, Fischetti VA: Characterization of a unique glycosylated anchor endopeptidase that cleaves the LPXTG sequence motif of cell surface proteins of Gram-positive bacteria. J Biol Chem 2002, 277:46912-46922. The discovery of a second enzyme with sortase-like activity with apparently non-ribosomal origin casts doubt on the idea that all enzymes can be identified from scrutiny of genome sequences.
52. Schell MA, Karmirantzou M, Snel B, Vilanova D, Berger B, Pessi G, Zwahlen MC, Desiere F, Bork P, Delley M et al.: The genome sequence of Bifidobacterium longum reflects its adaptation to the human gastrointestinal tract. Proc Natl Acad Scow USA 2002, 99:14422-14427.
53. Read TD, Myers GS, Brunham RC, Nelson WC, Paulsen IT, Heidelberg J, Holtzapple E, Khouri H, Federova NB, Carty HA et al.: Genome sequence of Chlamydophila caviae (Chlamydia psittaci GPIC): examining the role of niche-specific genes in the evolution of the Chlamydiaceae. Nucleic Acids Res 2003, 31:2134-2147.
54. Bruggemann H, Baumer S, Fricke WF, Wiezer A, Liesegang H, Decker I, Herzberg C, Martinez-Arias R, Merkl R, Henne A et al.: The genome sequence of Clostridium tetani, the causative agent of tetanus disease. Proc Natl Acad Scow USA 2003, 100:1316-1321.
55. Kapatral V, Anderson I, Ivanova N, Reznik G, Los T, Lykidis A, Bhattacharyya A, Bartman A, Gardner W, Grechkin G et al.: Genome sequence and analysis of the oral bacterium Fusobacterium nucleatum strain ATCC 2558. J Bacteriol 2002, 184:2005-2018.
56. Nelson KE, Weinel C, Paulsen IT, Dodson RJ, Hilbert H, Martins dos Santos VA, Fouts DE, Gill SR, Pop M, Holmes M et al.: Complete genome sequence and comparative analysis of the metabolically versatile Pseudomonas putida KT244. Environ Microbiol 2002, 4:799-808.
57. Salanoubat M, Genin S, Artiguenave F, Gouzy J, Mangenot S, Arlat M, Billault A, Brottier P, Camus JC, Cattolico L et al.: Genome sequence of the plant pathogen Ralstonia solanacearum. Nature 2002, 415:497-502.
58. Wei J, Goldberg MB, Burland V, Venkatesan MM, Deng W, Fournier G, Mayhew GF, Plunkett G III, Rose DJ, Darling A et al.: Complete genome sequence and comparative genomics of Shigella flexneri serotype 2a strain 2457T. Infect Immun 2003, 71:2775-2786.
59. Tettelin H, Masignani V, Cieslewicz MJ, Eisen JA, Peterson S, Wessels MR, Paulsen IT, Nelson KE, Margarit I, Read TD et al.: Complete genome sequence and comparative genomic analysis of an emerging human pathogen, serotype V Streptococcus agalactiae. Proc Natl Acad Scow USA 2002, 99:12391-12396.
60. Hueck CJ: Type III protein secretion systems in bacterial pathogens of animals and plants. Microbiol Mol Biol Rev 1998, 62:379-433.
61. Yuk MH, Harvill ET, Miller JF: The BvgAS virulence control system regulates type III secretion in Bordetella bronchiseptica. Mol Microbiol 1998, 28:945-959.
62. Gottfert M, Rothlisberger S, Kundig C, Beck C, Marty R, Hennecke H: Potential symbiosis-specific genes uncovered by sequencing a 410-kilobase DNA region of the Bradyrhizobium japonicum chromosome. J Bacteriol 2001, 183:1405-1412.
63. Parsons YN, Glendinning KJ, Thornton V, Hales BA, Hart CA, Winstanley C: A putative type III secretion gene cluster is widely distributed in the Burkholderia cepacia complex but absent from genomovar I. FEMS Microbiol Lett 2001, 203:103-108.
64. Winstanley C, Hales BA, Hart CA: Evidence for the presence in Burkholderia pseudomallei of a type III secretion system-associated gene cluster. J Med Microbiol 1999, 48:649-656.
65. Deng W, Li Y, Vallance BA, Finlay BB: Locus of enterocyte effacement from Citrobacter rodentium: sequence analysis and evidence for horizontal transfer among attaching and effacing pathogens. Infect Immun 2001, 69:6323-6335.
66. Rantakari A, Virtaharju O, Vahamiko S, Taira S, Palva ET, Saarilahti HT, Romantschuk M: Type III secretion contributes to the pathogenesis of the soft-rot pathogen Erwinia carotovora: partial characterization of the hrp gene cluster. Mol Plant-Microbe Interact 2001, 14:962-968.
67. Ham JH, Bauer DW, Fouts DE, Collmer A: A cloned Erwinia chrysanthemi Hrp (type III protein secretion) system functions in Escherichia coli to deliver Pseudomonas syringae Avr signals to plant cells and to secrete Avr proteins in culture. Proc Natl Acad Scow USA 1998, 95:10206-10211.
68. Perna NT, Plunkett G III, Burland V, Mau B, Glasner JD, Rose DJ, Mayhew GF, Evans PS, Gregor J, Kirkpatrick HA et al.: Genome sequence of enterohaemorrhagic Escherichia coli 0157:H. Nature 2001, 409:529-533.
69. Kaneko T, Nakamura Y, Sato S, Asamizu E, Kato T, Sasamoto S, Watanabe A, Idesawa K, Ishikawa A, Kawashima K et al: Complete genome structure of the nitrogen-fixing symbiotic bacterium Mesorhizobium loti. DNA Res 2000, 7:331-338.
70. Frederick RD, Ahmad M, Majerczak DR, Arroyo-Rodriguez AS, Manulis S, Coplin DL: Genetic organization of the Pantoea stewartii subsp. stewartii hrp gene cluster and sequence analysis of the hrpA, hrpC, hrpN, and wtsE operons. Mol Plant-Microbe Interact 2001, 14:1213-1222.
71. Preston GM, Bertrand N, Rainey PB: Type III secretion in plant growth-promoting Pseudomonas fluorescens SBW2. Mol Microbiol 2001, 41:999-1014.
72. Parkhill J, Dougan G, James KD, Thomson NR, Pickard D, Wain J, Churcher C, Mungall KL, Bentley SD, Holden MT et al.: Complete genome sequence of a multiple drug resistant Salmonella enterica serovar Typhi CT1. Nature 2001, 413:848-852.
73. da Silva AC, Ferro JA, Reinach FC, Farah CS, Furlan LR, Quaggio RB, Monteiro-Vitorello CB, Van Sluys MA, Almeida NF, Alves LM et al.: Comparison of the genomes of two Xanthomonas pathogens with differing host specificities. Nature 2002, 417:459-463.
74. Zhu W, MaGbanua MM, White FF: Identification of two novel hrp-associated genes in the hrp gene cluster of Xanthomonas oryzae pv. oryzae. J Bacteriol 2000, 182:1844-1853.