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

The Pseudomonas aeruginosa genes pilB‐D and pilQ are necessary for the assembly of type 4 fimbriae. Homologues of these genes and of the subunit (pilin) gene have been described in various different bacterial species, but not always in association with type 4 fimbrial biosynthesis and function. Pil‐like proteins are also involved in protein secretion, DNA transfer by conjugation and transformation, and morphogenesis of filamentous bacteriophages. It seems likely that the Pil homologues function in the processing and export of proteins resembling type 4 fimbrial sub‐units, and in their organization into fimbrial‐like structures. These may either be true type 4 fimbriae, or components of protein complexes which act in the transport of macromolecules (DNA or protein) into or out of the cell. Some PilB‐like and PilQ‐like proteins are apparently also involved in the assembly of non‐type 4 polymeric structures (filamentous phage virions and conjugative pili). The diverse studies summarized in this review are providing insight into an extensive infrastructural system which appears to be utilized in the formation of a variety of cell surface‐associated complexes.

[1]  C. d’Enfert,et al.  Pullulanase secretion in Escherichia coli K‐12 requires a cytoplasmic protein and a putative polytopic cytoplasmic membrane protein , 1992, Molecular microbiology.

[2]  G. Condemine,et al.  Some of the out genes involved in the secretion of pectate lyases in Erwinia chrysanthemi are regulated by kdgR , 1992, Molecular microbiology.

[3]  M. Sandkvist,et al.  A protein required for secretion of cholera toxin through the outer membrane of Vibrio cholerae. , 1993, Gene.

[4]  J. Mattick,et al.  Morphogenetic expression of Bacteroides nodosus fimbriae in Pseudomonas aeruginosa , 1987, Journal of bacteriology.

[5]  S. Lory,et al.  A single bifunctional enzyme, PilD, catalyzes cleavage and N-methylation of proteins belonging to the type IV pilin family. , 1993, Proceedings of the National Academy of Sciences of the United States of America.

[6]  J. Nataro,et al.  A plasmid‐encoded type IV fimbrial gene of enteropathogenic Escherichia coli associated with localized adherence , 1992, Molecular microbiology.

[7]  D. K. Willis,et al.  Current ReviewhrpGenes of Phytopathogenic Bacteria , 1991 .

[8]  S. Lory,et al.  Amino acid substitutions in pilin of Pseudomonas aeruginosa. Effect on leader peptide cleavage, amino-terminal methylation, and pilus assembly. , 1991, The Journal of biological chemistry.

[9]  S. Lory,et al.  Multiple roles of the pilus biogenesis protein pilD: involvement of pilD in excretion of enzymes from Pseudomonas aeruginosa , 1991, Journal of bacteriology.

[10]  J. Guest,et al.  Nucleotide sequence of the gene encoding the GMP reductase of Escherichia coli K12. , 1988, The Biochemical journal.

[11]  U. Bonas,et al.  Determinants of pathogenicity in Xanthomonas campestris pv. vesicatoria are related to proteins involved in secretion in bacterial pathogens of animals. , 1992, Molecular plant-microbe interactions : MPMI.

[12]  J. Mattick,et al.  Morphogenetic expression of Moraxella bovis fimbriae (pili) in Pseudomonas aeruginosa , 1990, Journal of bacteriology.

[13]  S. He,et al.  The Pseudomonas syringae pv. syringae 61 hrpH product, an envelope protein required for elicitation of the hypersensitive response in plants , 1992, Journal of bacteriology.

[14]  A. Pugsley.  The complete general secretory pathway in gram-negative bacteria. , 1993, Microbiological reviews.

[15]  P. Sparling,et al.  Factors affecting genetic transformation of Neisseria gonorrhoeae , 1977, Journal of bacteriology.

[16]  J. Mattick,et al.  Characterization of pilQ, a new gene required for the biogenesis of type 4 fimbriae in Pseudomonas aeruginosa , 1993, Molecular microbiology.

[17]  B. Pasloske,et al.  Mutations in the fifth-position glutamate in Pseudomonas aeruginosa pilin affect the transmethylation of the N-terminal phenylalanine. , 1993, Canadian journal of microbiology.

[18]  P M van Wezenbeek,et al.  Nucleotide sequence of the filamentous bacteriophage M13 DNA genome: comparison with phage fd. , 1980, Gene.

[19]  R. Gupta,et al.  Cloning of HSP60 (GroEL) operon from Clostridium perfringens using a polymerase chain reaction based approach. , 1992, Biochimica et biophysica acta.

[20]  C. Squires,et al.  ClpB is the Escherichia coli heat shock protein F84.1 , 1991, Journal of bacteriology.

[21]  A. Pugsley,et al.  Two distinct steps in pullulanase secretion by Escherichia coli K12 , 1991, Molecular microbiology.

[22]  J. Tomb,et al.  Nucleotide sequence of a cluster of genes involved in the transformation of Haemophilus influenzae Rd. , 1991, Gene.

[23]  J. Tommassen,et al.  Protein secretion inPseudomonas aeruginosa , 1992 .

[24]  J. Ottow.  Ecology, physiology, and genetics of fimbriae and pili. , 1975, Annual review of microbiology.

[25]  M. Bally,et al.  Secretion of extracellular proteins by Pseudomonas aeruginosa. , 1990, Biochimie.

[26]  D. Emery,et al.  Isolation of the gene encoding pilin of Bacteroides nodosus (strain 198), the causal organism of ovine footrot , 1984, FEBS letters.

[27]  S. Gottesman,et al.  Clp P represents a unique family of serine proteases. , 1990, The Journal of biological chemistry.

[28]  A. Goldberg,et al.  The heat-shock protein ClpB in Escherichia coli is a protein-activated ATPase. , 1992, The Journal of biological chemistry.

[29]  H. Ackermann,et al.  Comparative biology and evolution of bacteriophages. , 1982, Advances in virus research.

[30]  G. Cornelis,et al.  Analysis of virC, an operon involved in the secretion of Yop proteins by Yersinia enterocolitica , 1991, Journal of bacteriology.

[31]  J. Mattick,et al.  Characterisation of a Pseudomonas aeruginosa twitching motility gene and evidence for a specialised protein export system widespread in eubacteria. , 1991, Gene.

[32]  C. Squires,et al.  The Clp proteins: proteolysis regulators or molecular chaperones? , 1992, Journal of bacteriology.

[33]  B. Dupuy,et al.  Neisseria gonorrhoeae prepilin export studied in Escherichia coli , 1991, Journal of bacteriology.

[34]  C. E. Wilde,et al.  Cloning and DNA sequence of the omc gene encoding the outer membrane protein-macromolecular complex from Neisseria gonorrhoeae , 1989, Infection and immunity.

[35]  D. Dubnau,et al.  A membrane protein with similarity to N-methylphenylalanine pilins is essential for DNA binding by competent Bacillus subtilis , 1990, Journal of bacteriology.

[36]  R. Schilperoort,et al.  Conjugative Transfer by the Virulence System of Agrobacterium tumefaciens , 1992, Science.

[37]  S. Straley,et al.  Structure and regulation of the Yersinia pestis yscBCDEF operon , 1992, Journal of bacteriology.

[38]  J. Tommassen,et al.  Protein secretion in Pseudomonas aeruginosa. , 1992, FEMS microbiology reviews.

[39]  M. Koomey,et al.  Conservation of genes encoding components of a type IV pilus assembly/two‐step protein export pathway in Neisseria gonorrhoeae , 1993, Molecular microbiology.

[40]  J. Mattick,et al.  Organization of the fimbrial gene region of Bacteroides nodosus: class I and class II strains , 1991, Molecular microbiology.

[41]  D. E. Bradley.  A function of Pseudomonas aeruginosa PAO polar pili: twitching motility. , 1980, Canadian journal of microbiology.

[42]  B. Pasloske,et al.  The expression of mutant pilins in Pseudomonas aeruginosa: fifth position glutamate affects pilin methylation , 1988, Molecular microbiology.

[43]  M. Ogierman,et al.  Nucleotide sequence of the structural gene, tcpA, for a major pilin subunit of Vibrio cholerae. , 1989, Gene.

[44]  C. Boucher,et al.  hrp genes of Pseudomonas solanacearum are homologous to pathogenicity determinants of animal pathogenic bacteria and are conserved among plant pathogenic bacteria. , 1992, Molecular plant-microbe interactions : MPMI.

[45]  M. Lessl,et al.  Sequence similarities between the RP4 Tra2 and the Ti VirB region strongly support the conjugation model for T-DNA transfer. , 1992, The Journal of biological chemistry.

[46]  Denise S Walker,et al.  Molecular cloning and characterization of 13 out genes from Erwinia carotovora subspecies carotovora: genes encoding members of a general secretion pathway (GSP) widespread in Gram‐negative bacteria , 1993, Molecular microbiology.

[47]  B. Dupuy,et al.  An enzyme with type IV prepilin peptidase activity is required to process components of the general extracellular protein secretion pathway of Klebsiella oxytoca , 1992, Molecular microbiology.

[48]  C. d’Enfert,et al.  Klebsiella pneumoniae pulS gene encodes an outer membrane lipoprotein required for pullulanase secretion , 1989, Journal of bacteriology.

[49]  S. Lory,et al.  Kinetics and sequence specificity of processing of prepilin by PilD, the type IV leader peptidase of Pseudomonas aeruginosa , 1992, Journal of bacteriology.

[50]  A. Datta,et al.  Characterization of the virB operon from an Agrobacterium tumefaciens Ti plasmid. , 1988, The Journal of biological chemistry.

[51]  P. Sansonetti,et al.  MxiD, an outer membrane protein necessary for the secretion of the Shigella flexneri Ipa invasins , 1993, Molecular microbiology.

[52]  B. Jiang,et al.  The Aeromonas hydrophila exeE gene, required both for protein secretion and normal outer membrane biogenesis, is a member of a general secretion pathway , 1992, Molecular microbiology.

[53]  J. Seyer,et al.  Processing of TCP pilin by TcpJ typifies a common step intrinsic to a newly recognized pathway of extracellular protein secretion by gram-negative bacteria. , 1991, Genes & development.

[54]  M. Ogierman,et al.  Genetic organization and sequence of the promoter-distal region of the tcp gene cluster of Vibrio cholerae. , 1993, Gene.

[55]  L. Frost.  Bacterial conjugation: everybody's doin' it. , 1992, Canadian journal of microbiology.

[56]  M. Russel,et al.  Filnmentous phage assembly , 1991, Molecular microbiology.

[57]  D. E. Bradley.  Evidence for the retraction of Pseudomonas aeruginosa RNA phage pili. , 1972, Biochemical and biophysical research communications.

[58]  A. Collmer,et al.  Analysis of eight out genes in a cluster required for pectic enzyme secretion by Erwinia chrysanthemi: sequence comparison with secretion genes from other gram-negative bacteria , 1992, Journal of bacteriology.

[59]  M. Gordon,et al.  A gene required for transfer of T-DNA to plants encodes an ATPase with autophosphorylating activity. , 1989, Proceedings of the National Academy of Sciences of the United States of America.

[60]  R. Taylor,et al.  Vibrio cholerae O395 tcpA pilin gene sequence and comparison of predicted protein structural features to those of type 4 pilins , 1990, Infection and immunity.

[61]  C. Kay,et al.  Spectral properties of three quaternary arrangements of Pseudomonas pilin. , 1983, Biochemistry.

[62]  M. Bally,et al.  Protein secretion in Pseudomonas aeruginosa: the xcpA gene encodes an integral inner membrane protein homologous to Klebsiella pneumoniae secretion function protein PulO , 1991, Journal of bacteriology.

[63]  S. Lory,et al.  Product of the Pseudomonas aeruginosa gene pilD is a prepilin leader peptidase. , 1991, Proceedings of the National Academy of Sciences of the United States of America.

[64]  D. E. Bradley.  The adsorption of the Pseudomonas aeruginosa filamentous bacteriophage Pf to its host. , 1973, Canadian journal of microbiology.

[65]  J. Tommassen,et al.  Xcp‐mediated protein secretion in Pseudomonas aeruginosa: identification of two additional genes and evidence for regulation of xcp gene expression , 1993, Molecular microbiology.

[66]  J. Mattick,et al.  PilS and PilR, a two‐component transcriptional regulatory system controlling expression of type 4 fimbriae in Pseudomonas aeruginosa , 1993, Molecular microbiology.

[67]  L. Frost,et al.  The physiology and biochemistry of pili. , 1988, Advances in microbial physiology.

[68]  A. Pugsley.  Processing and methylation of PulG, a pilin‐like component of the general secretory pathway of Klebsiella oxytoca , 1993, Molecular microbiology.

[69]  D. Dubnau,et al.  Molecular cloning and characterization of comC, a late competence gene of Bacillus subtilis , 1989, Journal of bacteriology.

[70]  J. Tommassen,et al.  Protein secretion in gram‐negative bacteria: transport across the outer membrane involves common mechanisms in different bacteria. , 1990, The EMBO journal.

[71]  J. Walker,et al.  Distantly related sequences in the alpha‐ and beta‐subunits of ATP synthase, myosin, kinases and other ATP‐requiring enzymes and a common nucleotide binding fold. , 1982, The EMBO journal.

[72]  G. Schoolnik,et al.  An inducible bundle-forming pilus of enteropathogenic Escherichia coli. , 1991, Science.

[73]  P. R. Sibbald,et al.  The P-loop--a common motif in ATP- and GTP-binding proteins. , 1990, Trends in biochemical sciences.

[74]  R. Konings,et al.  Nucleotide sequence of the genome of Pf3, an IncP-1 plasmid-specific filamentous bacteriophage of Pseudomonas aeruginosa , 1985, Journal of virology.

[75]  B. Dupuy,et al.  PuIO, a component of the pullulanase secretion pathway of Klebsiella oxytoca, correctly and efficiently processes gonococcal type IV prepilin in Escherichia coli , 1992, Molecular microbiology.

[76]  Christopher M Thomas,et al.  Conjugative transfer functions of broad‐host‐range plasmid RK2 are coregulated with vegetative replication , 1992, Molecular microbiology.

[77]  T. Meyer,et al.  Production of Neisseria gonorrhoeae pili (fimbriae) in Pseudomonas aeruginosa , 1992, Journal of bacteriology.

[78]  A. Tomkinson,et al.  Complete nucleotide sequence of the Escherichia coti recC gene and of the thyA-recC intergenk region , 1986 .

[79]  M. Koomey,et al.  Pilin expression and processing in pilus mutants of Neisseria gonorrhoeae: critical role of Gly‐1 in assembly , 1991, Molecular Microbiology.

[80]  D. Dubnau,et al.  Cloning and characterization of a cluster of linked Bacillus subtilis late competence mutations , 1989, Journal of bacteriology.

[81]  F. Tang,et al.  Cloning and characterization of a gene required for the secretion of extracellular enzymes across the outer membrane by Xanthomonas campestris pv. campestris , 1992, Journal of bacteriology.

[82]  M. Kitagawa,et al.  Expression of ClpB, an analog of the ATP-dependent protease regulatory subunit in Escherichia coli, is controlled by a heat shock sigma factor (sigma 32) , 1991, Journal of bacteriology.

[83]  Su-ryang Kim,et al.  Nucleotide sequence of the R721 shufflon , 1992, Journal of bacteriology.

[84]  P. Harrison,et al.  Cloning, sequencing, and mapping of the bacterioferritin gene (bfr) of Escherichia coli K-12 , 1989, Journal of bacteriology.

[85]  S. Lory,et al.  Genetic and functional characterization of the gene cluster specifying expression of Pseudomonas aeruginosa pili , 1993, Infection and immunity.

[86]  H. Seifert,et al.  DNA transformation leads to pilin antigenic variation in Neisseria gonorrhoeae , 1988, Nature.

[87]  J. Mattick,et al.  Conservation of the regulatory subunit for the Clp ATP-dependent protease in prokaryotes and eukaryotes. , 1990, Proceedings of the National Academy of Sciences of the United States of America.

[88]  K. Shirasu,et al.  Characterization of the virB operon of an Agrobacterium tumefaciens Ti plasmid: nucleotide sequence and protein analysis , 1990, Molecular microbiology.

[89]  S. Lory,et al.  Products of three accessory genes, pilB, pilC, and pilD, are required for biogenesis of Pseudomonas aeruginosa pili , 1990, Journal of bacteriology.

[90]  S. Goodgal,et al.  Sequence and transcriptional regulation of com101A, a locus required for genetic transformation in Haemophilus influenzae , 1991, Journal of bacteriology.

[91]  J. Tommassen,et al.  Protein secretion in Pseudomonas aeruginosa: characterization of seven xcp genes and processing of secretory apparatus components by prepilin peptidase , 1992, Molecular microbiology.

[92]  S. Lory,et al.  Identification of pilR, which encodes a transcriptional activator of the Pseudomonas aeruginosa pilin gene , 1992, Journal of bacteriology.

[93]  C. d’Enfert,et al.  Genetics of extracellular protein secretion by gram-negative bacteria. , 1990, Annual review of genetics.

[94]  R. Taylor,et al.  Biogenesis and regulation of the Vibrio cholerae toxin-coregulated pilus: analogies to other virulence factor secretory systems. , 1993, Gene.

[95]  S. Lory,et al.  Components of the protein-excretion apparatus of Pseudomonas aeruginosa are processed by the type IV prepilin peptidase. , 1992, Proceedings of the National Academy of Sciences of the United States of America.

[96]  T. Meyer,et al.  Pilus genes of Neisseria gonorrheae: chromosomal organization and DNA sequence. , 1984, Proceedings of the National Academy of Sciences of the United States of America.

[97]  H. Seifert,et al.  Pilin expression in Neisseria gonorrhoeae is under both positive and negative transcriptional control. , 1988, The EMBO journal.

[98]  A. Pugsley,et al.  Five genes at the 3′ end of the Klebsiella pneumoniae pulC operon are required for pullulanase secretion , 1990, Molecular microbiology.

[99]  M. Green,et al.  Sequence analysis of the inversion region containing the pilin genes of Moraxella bovis , 1990, Journal of bacteriology.

[100]  S. Goodgal.  DNA uptake in Haemophilus transformation. , 1982, Annual review of genetics.

[101]  B. Spratt,et al.  The nucleotide sequences of the ponA and ponB genes encoding penicillin-binding protein 1A and 1B of Escherichia coli K12. , 1985, European journal of biochemistry.

[102]  M. Marinus,et al.  Identification of the gene (aroK) encoding shikimic acid kinase I of Escherichia coli , 1992, Journal of bacteriology.

[103]  J M Ghuysen,et al.  Comparison of the sequences of class A beta-lactamases and of the secondary structure elements of penicillin-recognizing proteins , 1991, Antimicrobial Agents and Chemotherapy.

[104]  S. He,et al.  Cloned Erwinia chrysanthemi out genes enable Escherichia coli to selectively secrete a diverse family of heterologous proteins to its milieu. , 1991, Proceedings of the National Academy of Sciences of the United States of America.