Chapter 11 : Function, Evolution, and Classification of Macromolecular Transport Systems

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Function, Evolution, and Classification of Macromolecular Transport Systems, Page 1 of 2

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This chapter proposes a universal classification scheme for macromolecular transport systems based on the phylogeny of genes involved in transport and the sequence of events that led to the construction of each system. It focuses on the systems of gram-negative proteobacteria and their relatives in other prokaryotes and eukaryotes. The chapter concentrates on the terminal branches of the system along with the -independent transporters. It lays out current functional models and discusses evolutionary evidence and hypotheses for eight overarching types, making note of classification disagreements where appropriate. The chapter talks about on the type I secretion: the ATP-binding cassette transporters, type II secretion: the main terminal branch, type III secretion: contact-dependent systems, type IV secretion: conjugation- related systems, and type V secretion: the autotransporters, the chaperone/usher pathway, the alternate chaperone/ usher pathway, and the extracellular nucleation- precipitation pathway. In this chapter, the term "homology" is used to mean "similarity because of common ancestry". Thus, homology is always based on a hypothesis of common ancestry. Many studies presented in this chapter use tree-building techniques such as neighbor joining, which base the branching pattern of tree topology on measurements of aggregate sequence similarities. Confusion surrounding the classification of macromolecular transport systems is based on the lack of a standardized, logical, and systematic basis for nomenclature. Phylogenetic models can be put to work for investigation as good predictors of function that allow reasonable hypotheses to be generated and tested. In addition, many classification disagreements could be clarified by using an explicit and systematic phylogenetic system.

Citation: Planet P, Figurski D, DeSalle R. 2006. Function, Evolution, and Classification of Macromolecular Transport Systems, p 189-219. In Seifert H, DiRita V (ed), Evolution of Microbial Pathogens. ASM Press, Washington, DC. doi: 10.1128/9781555815622.ch11
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Image of FIGURE 1

Schematic representations of secretion systems. Symbols indicate established homologous relationships between genes for the proteins pictured. Putative NTPases from the superfamily are given single and double daggers. Single daggers indicate putative NTPases from the type II secretion family, and type IV secretion family NTPases are indicated by double daggers. Flagellar apparatuses and type IV pilus systems are grouped with their close relatives. See text for details.

Citation: Planet P, Figurski D, DeSalle R. 2006. Function, Evolution, and Classification of Macromolecular Transport Systems, p 189-219. In Seifert H, DiRita V (ed), Evolution of Microbial Pathogens. ASM Press, Washington, DC. doi: 10.1128/9781555815622.ch11
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Image of FIGURE 2

Functional reconstruction of type II and IV secretion using simple Fitch optimization and the superfamily phylogeny. (A) Reconstruction of substrate evolution. Shades and patterns indicate conjugation (gray);DNA uptake (hatched);and protein secretion, including pilin and flagellar subunits (black). In cases in which two functions have been observed, DNA transport (either conjugation or uptake) is shown. (B) Evolutionary reconstruction of surface organelles: cyclized/thick conjugative pili (black), type IV pili (gray), archaeal flagella (hatched), or no surface structure observed (checked). Trees are derived from the NTPase phylogeny done in this study and are pruned to include better studied taxa. They are rooted with the uncharacterized archaeal NTPases as in reference .

Citation: Planet P, Figurski D, DeSalle R. 2006. Function, Evolution, and Classification of Macromolecular Transport Systems, p 189-219. In Seifert H, DiRita V (ed), Evolution of Microbial Pathogens. ASM Press, Washington, DC. doi: 10.1128/9781555815622.ch11
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Image of FIGURE 3

Hypothetical reticulogram for secretion systems. Each line represents a different gene phylogeny. Primary (1°) and secondary (2°) gene associations that could form the basis of a classification system are shown. Type B is defined by a new association between a light gray gene and a black gene after the loss of the dashed gene. Thus, this is defined as a new type independent of type C. Type D can be divided into two subgroups based on the presence or absence of a light gray gene.

Citation: Planet P, Figurski D, DeSalle R. 2006. Function, Evolution, and Classification of Macromolecular Transport Systems, p 189-219. In Seifert H, DiRita V (ed), Evolution of Microbial Pathogens. ASM Press, Washington, DC. doi: 10.1128/9781555815622.ch11
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1. Aizawa, S. I. 2001. Bacterial flagella and type III secretion systems. FEMS Microbiol. Lett. 202:157164.
2. Aizawa, S. I. 1996. Flagellar assembly in Salmonella typhimurium. Mol. Microbiol. 19:15.
3. Austin, J. W.,, G. Sanders,, W. W. Kay, and, S. K. Collinson. 1998. Thin aggregative fimbriae enhance Salmonella enteritidis biofilm formation. FEMS Microbiol. Lett. 162:295301.
4. Baumler, A. J.,, A. J. Gilde,, R. M. Tsolis,, A. W. van der Velden,, B. M. Ahmer, and, F. Heffron. 1997. Contribution of horizontal gene transfer and deletion events to development of distinctive patterns of fimbrial operons during evolution of Salmonella serotypes. J. Bacteriol. 179:317322.
5. Ben Nasr, A.,, A. Olsen,, U. Sjobring,, W. Muller-Esterl, and, L. Bjorck. 1996. Assembly of human contact phase proteins and release of bradykinin at the surface of curli-expressing Escherichia coli. Mol. Microbiol. 20:927935.
6. Bhattacharjee, M. K.,, S. C. Kachlany,, D. H. Fine, and, D. H. Figurski. 2001. Nonspecific adherence and fibril biogenesis by Actinobacillus actinomycetemcomitans: TadA protein is an ATPase. J. Bacteriol. 183:59275936.
7. Bian, Z., and, S. Normark. 1997. Nucleator function of CsgB for the assembly of adhesive surface organelles in Escherichia coli. EMBO J. 16:58275836.
8. Bieber, D.,, S. W. Ramer,, C. Y. Wu,, W. J. Murray,, T. Tobe,, R. Fernandez, and, G. K. Schoolnik. 1998. Type IV pili, transient bacterial aggregates, and virulence of enteropathogenic Escherichia coli. Science 280:21142118.
9. Bitter, W.,, M. Koster,, M. Latijnhouwers,, H. de Cock, and, J. Tommassen. 1998. Formation of oligomeric rings by XcpQ and PilQ, which are involved in protein transport across the outer membrane of Pseudomonas aeruginosa. Mol. Microbiol. 27:209219.
10. Blocker, A.,, N. Jouihri,, E. Larquet,, P. Gounon,, F. Ebel,, C. Parsot,, P. Sansonetti, and, A. Allaoui. 2001. Structure and composition of the Shigella flexneri “needle complex”, a part of its type III secretion. Mol. Microbiol. 39:652663.
11. Bonci, A.,, A. Chiesurin,, P. Muscas, and, G. M. Rossolini. 1997. Relatedness and phylogeny within the family of periplasmic chaperones involved in the assembly of pili or capsule-like structures of gram-negative bacteria. J. Mol. Evol. 44:299309.
12. Boyd, E. F., and, D. L. Hartl. 1999. Analysis of the type 1 pilin gene cluster fim in Salmonella: its distinct evolutionary histories in the 5’ and 3’ regions. J. Bacteriol. 181:13011308.
13. Boyd, E. F., and, D. L. Hartl. 1998. Chromosomal regions specific to pathogenic isolates of Escherichia coli have a phylogenetically clustered distribution. J. Bacteriol. 180:11591165.
14. Boyd, E. F., and, D. L. Hartl. 1998. Diversifying selection governs sequence polymorphism in the major adhesin proteins fimA, papA, and sfaA of Escherichia coli. J. Mol. Evol. 47:258267.
15. Boyd, E. F., and, D. L. Hartl. 1997. Recent horizontal transmission of plasmids between natural populations of Escherichia coli and Salmonella enterica. J. Bacteriol. 179:16221627.
16. Bremer, K. 1995. Branch support and tree stability. Cladistics 10:295304.
17. Brochier, C.,, E. Bapteste,, D. Moreira, and, H. Philippe. 2002. Eubacterial phylogeny based on translational apparatus proteins. Trends Genet. 18:15.
18. Brown, E. W.,, M. L. Kotewicz, and, T. A. Cebula. 2002. Detection of recombination among Salmonella enterica strains using the incongruence length difference test. Mol. Phylogenet. Evol. 24:102120.
19. Bullitt, E.,, C. H. Jones,, R. Striker,, G. Soto,, F. Jacob-Dubuisson,, J. Pinkner,, M. J. Wick,, L. Makowski, and, S. J. Hultgren. 1996. Development of pilus organelle subassemblies in vitro depends on chaperone uncapping of a beta zipper. Proc. Natl. Acad. Sci. USA 93:1289012895.
20. Burns, D. L. 1999. Biochemistry of type IV secretion. Curr. Opin. Microbiol. 2:2529.
21. Cao, T. B., and, M. H. Saier, Jr. 2001. Conjugal type IV macromolecular transfer systems of gram-negative bacteria: organismal distribution, structural constraints and evolutionary conclusions. Microbiology 147:32013214.
22. Chapman, M. R.,, L. S. Robinson,, J. S. Pinkner,, R. Roth,, J. Heuser,, M. Hammar,, S. Normark, and, S. J. Hultgren. 2002. Role of Escherichia coli curli operons in directing amyloid fiber formation. Science 295:851855.
23. Charleston, M. A. 1998. Jungles: a new solution to the host/parasite phylogeny reconciliation problem. Math. Biosci. 149:191223.
24. Christie, P. J. 2001. Type IV secretion: intercellular transfer of macromolecules by systems ancestrally related to conjugation machines. Mol. Microbiol. 40:294305.
25. Christie, P. J., and, J. P. Vogel. 2000. Bacterial type IV secretion: conjugation systems adapted to deliver effector molecules to host cells. Trends Microbiol. 8:354360.
26. Cohen-Bazire, G., and, J. London. 1967. Basal organelles of bacterial flagella. J. Bacteriol. 94:458465.
27. Cohen-Krausz, S., and, S. Trachtenberg. 2002. The structure of the archeabacterial flagellar filament of the extreme halophile Halobacterium salinarum R1M1 and its relation to eubacterial flagellar filaments and type IV pili. J. Mol. Biol. 321:383395.
28. Collinson, S. K.,, S. C. Clouthier,, J. L. Doran,, P. A. Banser, and, W. W. Kay. 1996. Salmonella enteritidis agfBAC operon encoding thin, aggregative fimbriae. J. Bacteriol. 178:662667.
29. Collinson, S. K.,, L. Emody,, K. H. Muller,, T. J. Trust, and, W. W. Kay. 1991. Purification and characterization of thin, aggregative fimbriae from Salmonella enteritidis. J. Bacteriol. 173:47734781.
30. Collinson, S. K.,, S. L. Liu,, S. C. Clouthier,, P. A. Banser,, J. L. Doran,, K. E. Sanderson, and, W. W. Kay. 1996. The location of four fimbrin-encoding genes, agfA, fimA, sefA and sefD, on the Salmonella enteritidis and/or S. typhimurium XbaI-BlnI genomic restriction maps. Gene 169:7580.
31. Cunningham, C. W. 1997. Can three incongruence tests predict when data should be combined? Mol. Biol. Evol. 14:733740.
32. Dale, C.,, G. R. Plague,, B. Wang,, H. Ochman, and, N. A. Moran. 2002. Type III secretion systems and the evolution of mutualistic endosymbiosis. Proc. Natl. Acad. Sci. USA 99:1239712402.
33. Dale, C.,, S. A. Young,, D. T. Haydon, and, S. C. Welburn. 2001. The insect endosymbiont Sodalis glossinidius utilizes a type III secretion system for cell invasion. Proc. Natl. Acad. Sci. USA 98:18831888.
34. Davis, B. M.,, E. H. Lawson,, M. Sandkvist,, A. Ali,, S. Sozhamannan, and, M. K. Waldor. 2000. Convergence of the secretory pathways for cholera toxin and the filamentous phage, CTXphi. Science 288:333335.
35. Dinh, T.,, I. T. Paulsen, and, M. H. Saier, Jr. 1994. A family of extracytoplasmic proteins that allow transport of large molecules across the outer membranes of gram-negative bacteria. J. Bacteriol. 176:38253831.
36. Dobzhansky, T. 1948. Nothing in biology makes sense except in the light of evolution. Am. Biol. Teacher 35:125129.
37. Dodson, K. W.,, F. Jacob-Dubuisson,, R. T. Striker, and, S. J. Hultgren. 1993. Outer-membrane PapC molecular usher discriminately recognizes periplasmic chaperone-pilus subunit complexes. Proc. Natl. Acad. Sci. USA 90:36703674.
38. Doolittle, W. F. 1999. Phylogenetic classification and the universal tree [see comments]. Science 284:21242129.
39. Doran, J. L.,, S. K. Collinson,, J. Burian,, G. Sarlos,, E. C. Todd,, C. K. Munro,, C. M. Kay,, P. A. Banser,, P. I. Peterkin, and, W. W. Kay. 1993. DNA-based diagnostic tests for Salmonella species targeting agfA, the structural gene for thin, aggregative fimbriae. J. Clin. Microbiol. 31:22632273.
40. Driessen, A. J.,, P. Fekkes, and, J. P. van der Wolk. 1998. The Sec system. Curr. Opin. Microbiol. 1:216222.
41. Dubnau, D. 1999. DNA uptake in bacteria. Annu. Rev. Microbiol. 53:217244.
42. Economou, A. 2000. Bacterial protein translo-case: a unique molecular machine with an army of substrates. FEBS Lett. 476:1821.
43. Economou, A. 1999. Following the leader: bacterial protein export through the Sec pathway. Trends Microbiol. 7:315320.
44. Eisenbrandt, R.,, M. Kalkum,, E. M. Lai,, R. Lurz,, C. I. Kado, and, E. Lanka. 1999. Conjugative pili of IncP plasmids, and the Ti plasmid T pilus are composed of cyclic subunits. J. Biol. Chem. 274:2254822555.
45. Faguy, D. M.,, K. F. Jarrell,, J. Kuzio, and, M. L. Kalmokoff. 1994. Molecular analysis of archael flagellins: similarity to the type IV pilin-transport superfamily widespread in bacteria. Can. J. Micro-biol. 40:6771.
46. Farizo, K. M.,, T. Huang, and, D. L. Burns. 2000. Importance of holotoxin assembly in Ptl-mediated secretion of pertussis toxin from Bordetella pertussis. Infect. Immun. 68:40494054.
47. Farris, J. S. 1982. Distance data in phylogenetic analysis. Adv. Cladistics 1:323.
48. Farris, J. S. 1970. A method for computing Wagner trees. Syst. Zool. 19:8392.
49. Farris, J. S.,, V. A. Albert,, M. Kallersjo,, D. Lipscomb, and, A. G. Kluge. 1996. Parsimony jackknifing outperforms neighbor-joining. Cladistics 12:99124.
50. Farris, J. S.,, M. Kallersjo,, A. G. Kluge, and, C. Bult. 1995. Constructing a significance test for incongruence. Syst. Biol. 44:570572.
51. Felsenstein, J. 1985. Confidence limits on phylogenies: an approach using the bootstrap. Evolution 39:783791.
52. Felsenstein, J. 1996. Inferring phylogenies from protein sequences by parsimony, distance, and likelihood methods. Methods Enzymol. 266:418427.
53. Finkel, S. E., and, R. Kolter. 2001. DNA as a nutrient: novel role for bacterial competence gene homologs. J. Bacteriol. 183:62886293.
54. Fitch, W. M. 1971. Toward defining the course of evolution: minimum change for a specific tree topology. Syst. Zool. 20:406416.
55. Folkesson, A.,, A. Advani,, S. Sukupolvi,, J. D. Pfeifer,, S. Normark, and, S. Lofdahl. 1999. Multiple insertions of fimbrial operons correlate with the evolution of Salmonella serovars responsible for human disease. Mol. Microbiol. 33:612622.
56. Foultier, B.,, P. Troisfontaines,, S. Muller,, F. R. Opperdoes, and, G. R. Cornelis. 2002. Characterization of the ysa pathogenicity locus in the chromosome of Yersinia enterocolitica and phylogeny analysis of type III secretion systems. J. Mol. Evol. 55:3751.
57. Freiberg, C.,, R. Fellay,, A. Bairoch,, W. J. Broughton,, A. Rosenthal, and, X. Perret. 1997. Molecular basis of symbiosis between Rhizobium and legumes. Nature 387:394401.
58. Froehlich, B. J.,, A. Karakashian,, H. Sakellaris, and, J. R. Scott. 1995. Genes for CS2 pili of enterotoxigenic Escherichia coli and their interchangeability with those for CS1 pili. Infect. Immun. 63:48494856.
59. Fuller, T. E.,, M. J. Kennedy, and, D. E. Lowery. 2000. Identification of Pasteurella multocida virulence genes in a septicemic mouse model using signature-tagged mutagenesis. Microb. Pathog. 29:2538.
60. Geluk, F.,, P. P. Eijk,, S. M. van Ham,, H. M. Jansen, and, L. van Alphen. 1998. The fimbria gene cluster of nonencapsulated Haemophilus influenzae. Infect. Immun. 66:406417.
61. Gentschev, I.,, G. Dietrich, and, W. Goebel. 2002. The E. coli alpha-hemolysin secretion system and its use in vaccine development. Trends Microbiol. 10:3945.
62. Girardeau, J. P.,, Y. Bertin, and, I. Callebaut. 2000. Conserved structural features in class I major fimbrial subunits (Pilin) in gram-negative bacteria. Molecular basis of classification in seven subfamilies and identification of intrasubfamily sequence signature motifs which might be implicated in quaternary structure. J. Mol. Evol. 50:424442.
63. Gogarten, J. P.,, H. Kibak,, P. Dittrich,, L. Taiz,, E. J. Bowman,, B. J. Bowman,, M. F. Manolson,, R. J. Poole,, T. Date,, T. Oshima, et al. 1989. Evolution of the vacuolar H+-ATPase: implications for the origin of eukaryotes. Proc. Natl. Acad. Sci. USA 86:66616665.
64. Gophna, U.,, E. Z. Ron, and, D. Graur. 2003. Bacterial type III secretion systems are ancient and evolved by multiple horizontal-transfer events. Gene 312:151163.
65. Grass, S., and, J. W. St. Geme III. 2000. Maturation and secretion of the non-typable Haemophilus influenzae HMW1 adhesin: roles of the N-terminal and C-terminal domains. Mol. Microbiol. 36:5567.
66. Groisman, E. A., and, H. Ochman. 1996. Pathogenicity islands: bacterial evolution in quantum leaps. Cell 87:791794.
67. Haase, E. M.,, J. L. Zmuda, and, F. A. Scannapieco. 1999. Identification and molecular analysis of rough-colony-specific outer membrane proteins of Actinobacillus actinomycetemcomitans. Infect. Immun. 67:29012908.
68. Hacker, J., and, J. B. Kaper. 2000. Pathogenicity islands and the evolution of microbes. Annu. Rev. Microbiol. 54:641679.
69. Hale, T. L. 1991. Genetic basis of virulence in Shigella species. Microbiol. Rev. 55:206224.
70. Hammar, M.,, A. Arnqvist,, Z. Bian,, A. Olsen, and, S. Normark. 1995. Expression of two csg operons is required for production of fibronectin-and congo red-binding curli polymers in Escherichia coli K-12. Mol. Microbiol. 18:661670.
71. Hammar, M.,, Z. Bian, and, S. Normark. 1996. Nucleator-dependent intercellular assembly of adhesive curli organelles in Escherichia coli. Proc. Natl. Acad. Sci. USA 93:65626566.
72. Henderson, I. R.,, R. Cappello, and, J. P. Nataro. 2000. Autotransporter proteins, evolution and redefining protein secretion: response. Trends Microbiol. 8:534535.
73. Henderson, I. R.,, J. P. Nataro,, J. B. Kaper,, T. F. Meyer,, S. K. Farrand,, D. L. Burns,, B. B. Finlay, and, J. W. St. Geme III. 2000. Renaming protein secretion in the gram-negative bacteria. Trends Microbiol. 8:352.
74. Henderson, I. R.,, F. Navarro-Garcia, and, J. P. Nataro. 1998. The great escape: structure and function of the autotransporter proteins. Trends Microbiol. 6:370378.
75. Hennig, W. 1966. Phylogenetic Systematics. University of Illinois Press, Urbana.
76. Hobbs, M., and, J. S. Mattick. 1993. Common components in the assembly of type 4 fimbriae, DNA transfer systems, filamentous phage and protein-secretion apparatus: a general system for the formation of surface-associated protein complexes [see comments]. Mol. Microbiol. 10:233243.
77. Hofreuter, D.,, S. Odenbreit, and, R. Haas. 2001. Natural transformation competence in Helicobacter pylori is mediated by the basic components of a type IV secretion system. Mol. Microbiol. 41:379391.
78. Holland, I. B., and, M. A. Blight. 1999. ABC-ATPases, adaptable energy generators fuelling transmembrane movement of a variety of molecules in organisms from bacteria to humans. J. Mol. Biol. 293:381399.
79. Hueck, C. J. 1998. Type III protein secretion systems in bacterial pathogens of animals and plants. Microbiol. Mol. Biol. Rev. 62:379433.
80. Huelsenbeck, J. P., and, J. J. Bull. 1996. A likli-hood ratio test to detect conflicting phylogenetic signal. Syst. Biol. 45:9298.
81. Huelsenbeck, J. P.,, F. Ronquist,, R. Nielsen, and, J. P. Bollback. 2001. Bayesian inference of phylogeny and its impact on evolutionary biology. Science 294:23102314.
82. Inoue, T.,, I. Tanimoto,, H. Ohta,, K. Kato,, Y. Murayama, and, K. Fukui. 1998. Molecular characterization of low-molecular-weight component protein, Flp, in Actinobacillus actinomycetemcomitans fimbriae. Microbiol. Immunol. 42:253258.
83. Iwabe, N.,, K. Kuma,, M. Hasegawa,, S. Osawa, and, T. Miyata. 1989. Evolutionary relationship of archaebacteria, eubacteria, and eukaryotes inferred from phylogenetic trees of duplicated genes. Proc. Natl. Acad. Sci. USA 86:93559359.
84. Jacob-Dubuisson, F.,, R. Antoine, and, C. Locht. 2000. Autotransporter proteins, evolution and redefining protein secretion: response. Trends Microbiol. 8:533534.
85. Jacob-Dubuisson, F.,, C. Locht, and, R. Antoine. 2001. Two-partner secretion in gram-negative bacteria: a thrifty, specific pathway for large virulence proteins. Mol. Microbiol. 40:306313.
86. Jacob-Dubuisson, F.,, R. Striker, and, S. J. Hultgren. 1994. Chaperone-assisted self-assembly of pili independent of cellular energy. J. Biol. Chem. 269:1244712455.
87. Johnson, J. M., and, G. M. Church. 1999. Alignment and structure prediction of divergent protein families: periplasmic and outer membrane proteins of bacterial efflux pumps. J. Mol. Biol. 287:695715.
88. Johnson, J. R.,, T. T. O’Bryan,, M. Kuskowski, and, J. N. Maslow. 2001. Ongoing horizontal and vertical transmission of virulence genes and papA alleles among Escherichia coli blood isolates from patients with diverse-source bacteremia. Infect. Immun. 69:53635374.
89. Jones, C. H.,, P. N. Danese,, J. S. Pinkner,, T. J. Silhavy, and, S. J. Hultgren. 1997. The chaperone-assisted membrane release and folding pathway is sensed by two signal transduction systems. EMBO J. 16:63946406.
90. Jones, C. H.,, J. S. Pinkner,, R. Roth,, J. Heuser,, A. V. Nicholes,, S. N. Abraham, and, S. J. Hultgren. 1995. FimH adhesin of type 1 pili is assembled into a fibrillar tip structure in the Enterobacteriaceae. Proc. Natl. Acad. Sci. USA 92:20812085.
91. Kachlany, S. C.,, P. J. Planet,, M. K. Bhattacharjee,, E. Kollia,, R. DeSalle,, D. H. Fine, and, D. H. Figurski. 2000. Nonspecific adherence by Actinobacillus actinomycetemcomitans requires genes widespread in Bacteria and Archaea. J. Bacteriol. 182:61696176.
92. Kachlany, S. C.,, P. J. Planet,, R. DeSalle,, D. H. Fine, and, D. H. Figurski. 2001. Genes for tight adherence of Actinobacillus actinomycetemcomitans: from plaque to plague to pond scum. Trends Microbiol. 9:429437.
93. Kachlany, S. C.,, P. J. Planet,, R. Desalle,, D. H. Fine,, D. H. Figurski, and, J. B. Kaplan. 2001. flp-1, the first representative of a new pilin gene subfamily, is required for non-specific adherence of Actinobacillus actinomycetemcomitans. Mol. Microbiol. 40:542554.
94. Kennan, R. M.,, O. P. Dhungyel,, R. J. Whittington,, J. R. Egerton, and, J. I. Rood. 2001. The type IV fimbrial subunit gene (fimA) of Dichelobacter nodosus is essential for virulence, protease secretion, and natural competence. J. Bacteriol. 183:44514458.
95. Kim, J. F. 2001. Revisiting the chlamydial type III protein secretion system: clues to the origin of type III protein secretion. Trends Genet. 17:6569.
96. Kirn, T. J.,, M. J. Lafferty,, C. M. Sandoe, and, R. K. Taylor. 2000. Delineation of pilin domains required for bacterial association into microcolonies and intestinal colonization by Vibrio cholerae. Mol. Microbiol. 35:896910.
97. Kolaczkowski, B., and, J. W. Thornton. 2004. Performance of maximum parsimony and likelihood phylogenetics when evolution is heterogeneous. Nature 431:980984.
98. Koronakis, V.,, A. Sharff,, E. Koronakis,, B. Luisi, and, C. Hughes. 2000. Crystal structure of the bacterial membrane protein TolC central to multidrug efflux and protein export. Nature 405:914919.
99. Koski, L. B., and, G. B. Golding. 2001. The closest BLAST hit is often not the nearest neighbor. J. Mol. Evol. 52:540542.
100. Krall, L.,, U. Wiedemann,, G. Unsin,, S. Weiss,, N. Domke, and, C. Baron. 2002. Detergent extraction identifies different VirB protein sub-assemblies of the type IV secretion machinery in the membranes of Agrobacterium tumefaciens. Proc. Natl. Acad. Sci. USA 99:1140511410.
101. Kubori, T.,, A. Sukhan,, S. I. Aizawa, and, J. E. Galan. 2000. Molecular characterization and assembly of the needle complex of the Salmonella typhimurium type III protein secretion system. Proc. Natl. Acad. Sci. USA 97:1022510230.
102. Lai, E. M., and, C. I. Kado. 2000. The T-pilus of Agrobacterium tumefaciens. Trends Microbiol. 8:361369.
103. Lawley, T. D.,, M. W. Gilmour,, J. E. Gunton,, D. M. Tracz, and, D. E. Taylor. 2003. Functional and mutational analysis of conjugative transfer region 2 (Tra2) from the IncHI1 plasmid R27. J. Bacteriol. 185:581591.
104. Lawley, T. D.,, W. A. Klimke,, M. J. Gubbins, and, L. S. Frost. 2003. F factor conjugation is a true type IV secretion system. FEMS Microbiol. Lett. 224:115.
105. Lawrence, J. G. 1997. Selfish operons and speciation by gene transfer. Trends Microbiol. 5:355359.
106. Lawrence, J. G., and, J. R. Roth. 1996. Selfish operons: horizontal transfer may drive the evolution of gene clusters. Genetics 143:18431860.
107. Letellier, L.,, S. P. Howard, and, J. T. Buckley. 1997. Studies on the energetics of proaerolysin secretion across the outer membrane of Aeromonas species. Evidence for a requirement for both the protonmotive force and ATP. J. Biol. Chem. 272:1110911113.
108. Lewis, P. O. 2001. Phylogenetic systematics turns over a new leaf. Trends Ecol. Evol. 16:3037.
109. Li, X. Z., and, K. Poole. 2001. Mutational analysis of the OprM outer membrane component of the MexA-MexB-OprM multidrug efflux system of Pseudomonas aeruginosa. J. Bacteriol. 183:1227.
110. Llosa, M.,, F. X. Gomis-Ruth,, M. Coll, and, F. F. de la Cruz. 2002. Bacterial conjugation: a two-step mechanism for DNA transport. Mol. Microbiol. 45:18.
111. Loferer, H.,, M. Hammar, and, S. Normark. 1997. Availability of the fibre subunit CsgA and the nucleator protein CsgB during assembly of fibronectin-binding curli is limited by the intra-cellular concentration of the novel lipoprotein CsgG. Mol. Microbiol. 26:1123.
112. Macnab, R. M. 1999. The bacterial flagellum: reversible rotary propellor and type III export apparatus. J. Bacteriol. 181:71497153.
113. Marklund, B. I.,, J. M. Tennent,, E. Garcia,, A. Hamers,, M. Baga,, F. Lindberg,, W. Gaastra, and, S. Normark. 1992. Horizontal gene transfer of the Escherichia coli pap and prs pili operons as a mechanism for the development of tissue-specific adhesive properties. Mol. Micro-biol. 6:22252242.
114. Marron, M. B., and, C. J. Smyth. 1995. Molecular analysis of the cso operon of enterotoxigenic Escherichia coli reveals that CsoA is the adhesin of CS1 fimbriae and that the accessory genes are interchangeable with those of the cfa operon. Microbiology 141 (Pt. 11):28492859.
115. Martin, P. R.,, M. Hobbs,, P. D. Free,, Y. Jeske, and, J. S. Mattick. 1993. Characterization of pilQ, a new gene required for the biogenesis of type 4 fimbriae in Pseudomonas aeruginosa. Mol. Microbiol. 9:857868.
116. Masui, S.,, T. Sasaki, and, H. Ishikawa. 2000. Genes for the type IV secretion system in an intracellular symbiont, Wolbachia, a causative agent of various sexual alterations in arthropods. J. Bacteriol. 182:65296531.
117. Mattick, J. S. 2002. Type IV pili and twitching motility. Annu. Rev. Microbiol. 56:289314.
118. Mhlanga-Mutangadura, T.,, G. Morlin,, A. L. Smith,, A. Eisenstark, and, M. Golomb. 1998. Evolution of the major pilus gene cluster of Haemophilus influenzae. J. Bacteriol. 180:46934703.
119. Neil Sarkar, I.,, J. Thornton,, P. Planet,, D. Figurski,, B. Schierwater, and, R. DeSalle. 2002. An automated phylogenetic key for classifying homeoboxes. Mol. Phylogenet. Evol. 24:388.
120. Nelson, G. 1994. Homology and systematics, p. xvi, 483. In B. K. Hall (ed.), Homology: The Hierarchical Basis of Comparative Biology. Academic Press, San Diego, Calif.
121. Nguyen, L.,, I. T. Paulsen,, J. Tchieu,, C. J. Hueck, and, M. H. Saier, Jr. 2000. Phylogenetic analyses of the constituents of type III protein secretion systems. J. Mol. Microbiol. Biotechnol. 2:125144.
122. Nika, J. R.,, J. L. Latimer,, C. K. Ward,, R. J. Blick,, N. J. Wagner,, L. D. Cope,, G. G. Mahairas,, R. S. Munson, Jr., and, E. J. Hansen. 2002. Haemophilus ducreyi requires the flp gene cluster for microcolony formation in vitro. Infect. Immun. 70:29652975.
123. Nunn, D. 1999. Bacterial type II protein export and pilus biogenesis: more than just homologies? Trends Cell Biol. 9:402408.
124. Nunn, D. N., and, S. Lory. 1991. Product of the Pseudomonas aeruginosa gene pilD is a prepilin leader peptidase. Proc. Natl. Acad. Sci. USA 88:32813285.
125. O’Callaghan, D.,, C. Cazevieille,, A. Allardet Servent,, M. L. Boschiroli,, G. Bourg,, V. Foulongne,, P. Frutos,, Y. Kulakov, and, M. Ramuz. 1999. A homologue of the Agrobacterium tumefaciens VirB and Bordetella pertussis Ptl type IV secretion systems is essential for intracellular survival of Brucella suis. Mol. Microbiol. 33:12101220.
126. Ochman, H., and, E. A. Groisman. 1995. The evolution of invasion by enteric bacteria. Can. J. Microbiol. 41:555561.
127. Ochman, H.,, J. G. Lawrence, and, E. A. Groisman. 2000. Lateral gene transfer and the nature of bacterial innovation. Nature 405:299304.
128. Olsen, A.,, A. Arnqvist,, M. Hammar, and, S. Normark. 1993. Environmental regulation of curli production in Escherichia coli. Infect. Agents Dis. 2:272274.
129. Olsen, A.,, H. Herwald,, M. Wikstrom,, K. Persson,, E. Mattsson, and, L. Bjorck. 2002. Identification of two protein-binding and functional regions of curli, a surface organelle and virulence determinant of Escherichia coli. J. Biol. Chem. 277:3456834572.
130. Olsen, A.,, M. J. Wick,, M. Morgelin, and, L. Bjorck. 1998. Curli, fibrous surface proteins of Escherichia coli, interact with major histocompatibility complex class I molecules. Infect. Immun. 66:944949.
131. Page, R. D., and, M. A. Charleston. 1997. From gene to organismal phylogeny: reconciled trees and the gene tree/species tree problem. Mol. Phylogenet. Evol. 7:231240.
132. Pantoja, M.,, L. Chen,, Y. Chen, and, E. W. Nester. 2002. Agrobacterium type IV secretion is a two-step process in which export substrates associate with the virulence protein VirJ in the periplasm. Mol. Microbiol. 45:13251335.
133. Peabody, C. R.,, Y. J. Chung,, M. R. Yen,, D. Vidal-Ingigliardi,, A. P. Pugsley, and, M. H. Saier, Jr. 2003. Type II protein secretion and its relationship to bacterial type IV pili and archaeal flagella. Microbiology 149:30513072.
134. Phillips, A.,, D. Janies, and, W. Wheeler. 2000. Multiple sequence alignment in phylogenetic analysis. Mol. Phylogenet. Evol. 16:317330.
135. Planet, P. J. 2002. Reexamining microbial evolution through the lens of horizontal transfer. EXS (92):247303.
136. Planet, P. J.,, S. C. Kachlany,, R. DeSalle, and, D. H. Figurski. 2001. 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 98:25032508.
137. Planet, P. J.,, S. C. Kachlany,, D. H. Fine,, R. DeSalle, and, D. H. Figurski. 2003. The Widespread Colonization Island of Actino-bacillus actinomycetemcomitans. Nat. Genet. 34:193198.
138. Plano, G. V.,, J. B. Day, and, F. Ferracci. 2001. Type III export: new uses for an old pathway. Mol. Microbiol. 40:284293.
139. Plaut, A. G. 1983. The IgA1 proteases of pathogenic bacteria. Annu. Rev. Microbiol. 37:603622.
140. Pohlner, J.,, R. Halter,, K. Beyreuther, and, T. F. Meyer. 1987. Gene structure and extracellular secretion of Neisseria gonorrhoeae IgA protease. Nature 325:458462.
141. Pohlschroder, M.,, W. A. Prinz,, E. Hartmann, and, J. Beckwith. 1997. Protein translocation in the three domains of life: variations on a theme. Cell 91:563566.
142. Pugsley, A. P., and, B. Dupuy. 1992. An enzyme with type IV prepilin peptidase activity is required to process components of the general extracellular protein secretion pathway of Klebsiella oxytoca. Mol. Microbiol. 6:751760.
143. Pupo, G. M.,, D. K. Karaolis,, R. Lan, and, P. R. Reeves. 1997. Evolutionary relationships among pathogenic and nonpathogenic Escherichia coli strains inferred from multilocus enzyme electrophoresis and mdh sequence studies. Infect. Immun. 65:26852692.
144. Redfield, R. J. 1993. Genes for breakfast: the have-your-cake-and-eat-it-too of bacterial transformation. J. Hered. 84:400404.
145. Reid, S. D.,, C. J. Herbelin,, A. C. Bumbaugh,, R. K. Selander, and, T. S. Whittam. 2000. Parallel evolution of virulence in pathogenic Escherichia coli. Nature 406:6467.
146. Reumann, S.,, J. Davila-Aponte, and, K. Keegstra. 1999. The evolutionary origin of the protein-translocating channel of chloroplastic envelope membranes: identification of a cyanobacterial homolog. Proc. Natl. Acad. Sci. USA 96:784789.
147. Rivas, S.,, S. Bolland,, E. Cabezon,, F. M. Goni, and, F. de la Cruz. 1997. TrwD, a protein encoded by the IncW plasmid R388, displays an ATP hydrolase activity essential for bacterial conjugation. J. Biol. Chem. 272:2558325590.
148. Romling, U.,, Z. Bian,, M. Hammar,, W. D. Sierralta, and, S. Normark. 1998. Curli fibers are highly conserved between Salmonella typhimurium and Escherichia coli with respect to operon structure and regulation. J. Bacteriol. 180:722731.
149. Rudin, A.,, L. Olbe, and, A. M. Svennerholm. 1996. Monoclonal antibodies against fimbrial subunits of colonization factor antigen I (CFA/I) inhibit binding to human enterocytes and protect against enterotoxigenic Escherichia coli expressing heterologous colonization factors. Microb. Pathog. 21:3545.
150. Russel, M. 1998. Macromolecular assembly and secretion across the bacterial cell envelope: type II protein secretion systems. J. Mol. Biol. 279:485499.
151. Sagulenko, E.,, V. Sagulenko,, J. Chen, and, P. J. Christie. 2001. Role of Agrobacterium VirB11 ATPase in T-pilus assembly and substrate selection. J. Bacteriol. 183:58135825.
152. Saier, M. H., Jr. 2004. Evolution of bacterial type III protein secretion systems. Trends Microbiol. 12:113115.
153. Saier, M. H., Jr. 2000. A functional-phylogenetic classification system for transmembrane solute transporters. Microbiol. Mol. Biol. Rev. 64:354411.
154. Sajjan, U. S.,, L. Sun,, R. Goldstein, and, J. F. Forstner. 1995. Cable (cbl) type II pili of cystic fibrosis-associated Burkholderia (Pseudomonas) cepacia: nucleotide sequence of the cblA major subunit pilin gene and novel morphology of the assembled appendage fibers. J. Bacteriol. 177:10301038.
155. Sakellaris, H.,, N. K. Hannink,, K. Rajakumar,, D. Bulach,, M. Hunt,, C. Sasakawa, and, B. Adler. 2000. Curli loci of Shigella spp. Infect. Immun. 68:37803783.
156. Sakellaris, H.,, G. P. Munson, and, J. R. Scott. 1999. A conserved residue in the tip proteins of CS1 and CFA/I pili of enterotoxigenic Escherichia coli that is essential for adherence. Proc. Natl. Acad. Sci. USA 96:1282812832.
157. Sakellaris, H., and, J. R. Scott. 1998. New tools in an old trade: CS1 pilus morphogenesis. Mol. Microbiol. 30:681687.
158. Salmond, G. P. C. 1994. Secretion of extracellular virulence factors by plant pathogenic bacteria. Annu. Rev. Phytopathol. 32:181200.
159. Sandkvist, M. 2001. Biology of type II secretion. Mol. Microbiol. 40:271283.
160. Sandkvist, M. 2001. Type II secretion and pathogenesis. Infect. Immun. 69:35233535.
161. Sandkvist, M.,, M. Bagdasarian,, S. P. Howard, and, V. J. DiRita. 1995. Interaction between the autokinase EpsE and EpsL in the cytoplasmic membrane is required for extracellular secretion in Vibrio cholerae. EMBO J. 14:16641673.
162. Saurin, W.,, M. Hofnung, and, E. Dassa. 1999. Getting in or out: early segregation between importers and exporters in the evolution of ATP-binding cassette (ABC) transporters. J. Mol. Evol. 48:2241.
163. Sauvonnet, N.,, G. Vignon,, A. P. Pugsley, and, P. Gounon. 2000. Pilus formation and protein secretion by the same machinery in Escherichia coli. EMBO J. 19:22212228.
164. Schreiner, H. C.,, K. Sinatra,, J. B. Kaplan,, D. Furgang,, S. C. Kachlany,, P. J. Planet,, B. A. Perez,, D. H. Figurski, and, D. H. Fine. 2003. Tight-adherence genes of Actinobacillus actinomycetemcomitans are required for virulence in a rat model. Proc. Natl. Acad. Sci. USA 100:72957300.
165. Segal, G.,, M. Purcell, and, H. A. Shuman. 1998. Host cell killing and bacterial conjugation require overlapping sets of genes within a 22-kb region of the Legionella pneumophila genome. Proc. Natl. Acad. Sci. USA 95:16691674.
166. Segal, G.,, J. J. Russo, and, H. A. Shuman. 1999. Relationships between a new type IV secretion system and the icm/dot virulence system of Legionella pneumophila. Mol. Microbiol. 34:799809.
167. Shannon, J. L., and, R. C. Fernandez. 1999. The C-terminal domain of the Bordetella pertussis autotransporter BrkA forms a pore in lipid bilayer membranes. J. Bacteriol. 181:58385842.
168. Sigrist, C. J.,, L. Cerutti,, N. Hulo,, A. Gattiker,, L. Falquet,, M. Pagni,, A. Bairoch, and, P. Bucher. 2002. PROSITE: a documented database using patterns and profiles as motif descriptors. Brief Bioinform. 3:265274.
169. Skerker, J. M., and, H. C. Berg. 2001. Direct observation of extension and retraction of type IV pili. Proc. Natl. Acad. Sci. USA 98:69016904.
170. Skerker, J. M., and, L. Shapiro. 2000. Identification and cell cycle control of a novel pilus system in Caulobacter crescentus. EMBO J. 19:32233234.
171. Smeets, L. C., and, J. G. Kusters. 2002. Natural transformation in Helicobacter pylori: DNA transport in an unexpected way. Trends Microbiol. 10:159162; discussion, 162.
172. Sommer, J. M., and, A. Newton. 1989. Turning off flagellum rotation requires the pleiotropic gene pleD: pleA, pleC, and pleD define two morphogenic pathways in Caulobacter crescentus. J. Bacteriol. 171:392401.
173. Soto, G. E., and, S. J. Hultgren. 1999. Bacterial adhesins: common themes and variations in architecture and assembly. J. Bacteriol. 181:10591071.
174. Spinola, S. M.,, K. R. Fortney,, B. P. Katz,, J. L. Latimer,, J. R. Mock,, M. Vakevainen, and, E. J. Hansen. 2003. Haemophilus ducreyi requires an intact flp gene cluster for virulence in humans. Infect. Immun. 71:71787182.
175. St. Geme, J. W., III. 2000. The pathogenesis of nontypable Haemophilus influenzae otitis media. Vaccine 19(Suppl. 1): S41S50.
176. St. Geme, J. W., III, and, D. Cutter. 2000. The Haemophilus influenzae Hia adhesin is an auto-transporter protein that remains uncleaved at the C terminus and fully cell associated. J. Bacteriol. 182:60056013.
177. Swofford, D. L., and, W. P. Maddison. 1987. Reconstructing ancestral character states under Wagner parsimony. Math. Biosci. 87:199229.
178. Tatusov, R. L.,, E. V. Koonin, and, D. J. Lipman. 1997. A genomic perspective on protein families. Science 278:631637.
179. Thanassi, D. G., and, S. J. Hultgren. 2000. Multiple pathways allow protein secretion across the bacterial outer membrane. Curr. Opin. Cell Biol. 12:420430.
180. Thanassi, D. G.,, E. T. Saulino, and, S. J. Hultgren. 1998. The chaperone/usher pathway: a major terminal branch of the general secretory pathway. Curr. Opin. Microbiol. 1:223231.
181. Thanassi, D. G.,, E. T. Saulino,, M. J. Lombardo,, R. Roth,, J. Heuser, and, S. J. Hultgren. 1998. The PapC usher forms an oligomeric channel: implications for pilus biogenesis across the outer membrane. Proc. Natl. Acad. Sci. USA 95:31463151.
182. Thomas, N. A.,, S. L. Bardy, and, K. F. Jarrell. 2001. The archaeal flagellum: a different kind of prokaryotic motility structure. FEMS Microbiol. Rev. 25:147174.
183. Thornton, J. W., and, R. DeSalle. 2000. Gene family evolution and homology: genomics meets phylogenetics. Annu. Rev. Genomics Hum. Genet. 1:4173.
184. Thornton, J. W., and, R. DeSalle. 2000. A new method to localize and test the significance of incongruence: detecting domain shuffling in the nuclear receptor superfamily. Syst. Biol. 49:183201.
185. van Wely, K. H.,, J. Swaving,, R. Freudl, and, A. J. Driessen. 2001. Translocation of proteins across the cell envelope of Gram-positive bacteria. FEMS Microbiol. Rev. 25:437454.
186. Vidal, O.,, R. Longin,, C. Prigent-Combaret,, C. Dorel,, M. Hooreman, and, P. Lejeune. 1998. Isolation of an Escherichia coli K-12 mutant strain able to form biofilms on inert surfaces: involvement of a new ompR allele that increases curli expression. J. Bacteriol. 180:24422449.
187. Wall, D.,, P. E. Kolenbrander, and, D. Kaiser. 1999. The Myxococcus xanthus pilQ (sglA) gene encodes a secretin homolog required for type IV pilus biogenesis, social motility, and development. J. Bacteriol. 181:2433.
188. Ward, D. V.,, O. Draper,, J. R. Zupan, and, P. C. Zambryski. 2002. Peptide linkage mapping of the Agrobacterium tumefaciens vir-encoded type IV secretion system reveals protein subassemblies. Proc. Natl. Acad. Sci. USA 99:1149311500.
189. Welch, R. A. 2001. RTX toxin structure and function: a story of numerous anomalies and few analogies in toxin biology. Curr. Top. Microbiol. Immunol. 257:85111.
190. Wheeler, W. C. 1990. Nucleic acid sequence phylogeny and random outgroups. Cladistics 6:363368.
191. Whittam, T. S.,, M. L. Wolfe,, I. K. Wachsmuth,, F. Orskov,, I. Orskov, and, R. A. Wilson. 1993. Clonal relationships among Escherichia coli strains that cause hemorrhagic colitis and infantile diarrhea. Infect. Immun. 61:16191629.
192. Winans, S. C.,, D. L. Burns, and, P. J. Christie. 1996. Adaptation of a conjugal transfer system for the export of pathogenic macromolecules. Trends Microbiol. 4:6468.
193. Woese, C. 1998. The universal ancestor. Proc. Natl. Acad. Sci. USA 95:68546859.
194. Woese, C. R. 2000. Interpreting the universal phylogenetic tree. Proc. Natl. Acad. Sci. USA 97:83928396.
195. Wong, K. K.,, F. S. Brinkman,, R. S. Benz, and, R. E. Hancock. 2001. Evaluation of a structural model of Pseudomonas aeruginosa outer membrane protein OprM, an efflux component involved in intrinsic antibiotic resistance. J. Bacteriol. 183:367374.
196. Yen, M. R.,, C. R. Peabody,, S. M. Partovi,, Y. Zhai,, Y. H. Tseng, and, M. H. Saier. 2002. Protein-translocating outer membrane porins of gram-negative bacteria. Biochim. Biophys. Acta 1562:631.
197. Young, G. M.,, D. H. Schmiel, and, V. L. Miller. 1999. 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 96:64566461.
198. Zogaj, X.,, W. Bokranz,, M. Nimtz, and, U. Romling. 2003. Production of cellulose and curli fimbriae by members of the family Enterobacteriaceae isolated from the human gastrointestinal tract. Infect. Immun. 71:41514158.


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Properties of macromolecular transport systems

Citation: Planet P, Figurski D, DeSalle R. 2006. Function, Evolution, and Classification of Macromolecular Transport Systems, p 189-219. In Seifert H, DiRita V (ed), Evolution of Microbial Pathogens. ASM Press, Washington, DC. doi: 10.1128/9781555815622.ch11

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