Functions of S-layers.

Although S-layers are being increasingly identified on Bacteria and Archaea, it is enigmatic that in most cases S-layer function continues to elude us. In a few instances, S-layers have been shown to be virulence factors on pathogens (e.g. Campylobacter fetus ssp. fetus and Aeromonas salmonicida), protective against Bdellovibrio, a depository for surface-exposed enzymes (e.g. Bacillus stearothermophilus), shape-determining agents (e.g. Thermoproteus tenax) and nucleation factors for fine-grain mineral development (e.g. Synechococcus GL 24). Yet, for the vast majority of S-layered bacteria, the natural function of these crystalline arrays continues to be evasive. The following review up-dates the functional basis of S-layers and describes such diverse topics as the effect of S-layers on the Gram stain, bacteriophage adsorption in lactobacilli, phagocytosis by human polymorphonuclear leukocytes, the adhesion of a high-molecular-mass amylase, outer membrane porosity, and the secretion of extracellular enzymes of Thermoanaerobacterium. In addition, the functional aspect of calcium on the Caulobacter S-layer is explained.

[1]  J. Smit,et al.  An "all-purpose" cellulase reporter for gene fusion studies and application to the paracrystalline surface (S)-layer protein of Caulobacter crescentus. , 1993, Canadian journal of microbiology.

[2]  S. Sörlin,et al.  Phagocytosis and virulence of different strains of Porphyromonas gingivalis. , 1991, Scandinavian journal of dental research.

[3]  M. Stewart,et al.  Crystalline order to high resolution in the sheath of Methanospirillum hungatei: a cross-beta structure. , 1985, Journal of molecular biology.

[4]  J. Smit,et al.  Cell surface patterning and morphogenesis: biogenesis of a periodic surface array during Caulobacter development , 1982, The Journal of cell biology.

[5]  M. de Pedro,et al.  A conserved motif in S-layer proteins is involved in peptidoglycan binding in Thermus thermophilus , 1996, Journal of bacteriology.

[6]  An electron microscope survey of the surface structures and hydrophobicity of oral and non-oral species of the bacterial genus Bacteroides. , 1986, Archives of oral biology.

[7]  V. Braun,et al.  Chemical characterization, spatial distribution and function of a lipoprotein (murein-lipoprotein) of the E. coli cell wall. The specific effect of trypsin on the membrane structure. , 1969, European journal of biochemistry.

[8]  J. Smit,et al.  Identification of genes affecting production of the adhesion organelle of Caulobacter crescentus CB2 , 1990, Journal of bacteriology.

[9]  T. Beveridge,et al.  Ultrastructure, inferred porosity, and gram-staining character of Methanospirillum hungatei filament termini describe a unique cell permeability for this archaeobacterium , 1991, Journal of bacteriology.

[10]  Terry J. Beveridge,et al.  Bacterial S-layers , 1994 .

[11]  M. Blaser,et al.  Correlation between molecular size of the surface array protein and morphology and antigenicity of the Campylobacter fetus S layer , 1991, Infection and immunity.

[12]  J Frank,et al.  The structure of the stalk surface layer of a brine pond microorganism: correlation averaging applied to a double layered lattice structure , 1985, Journal of microscopy.

[13]  M. Salton The relationship between the nature of the cell wall and the Gram stain. , 1963, Journal of general microbiology.

[14]  S. Koval Predation on Bacteria Possessing S-Layers , 1993 .

[15]  W. Xu,et al.  Modeling and measuring the elastic properties of an archaeal surface, the sheath of Methanospirillum hungatei, and the implication of methane production , 1996, Journal of bacteriology.

[16]  F. Yoshimura,et al.  Purification and characterization of a novel type of fimbriae from the oral anaerobe Bacteroides gingivalis , 1984, Journal of bacteriology.

[17]  W. Baumeister,et al.  The S-layer of Caulobacter crescentus: three-dimensional image reconstruction and structure analysis by electron microscopy , 1992, Journal of bacteriology.

[18]  J. Aubert,et al.  Organization of a Clostridium thermocellum gene cluster encoding the cellulosomal scaffolding protein CipA and a protein possibly involved in attachment of the cellulosome to the cell surface , 1993, Journal of bacteriology.

[19]  A. Pugsley,et al.  Extracellular pullulanase of Klebsiella pneumoniae is a lipoprotein , 1986, Journal of bacteriology.

[20]  D. Briles,et al.  Structural properties and evolutionary relationships of PspA, a surface protein of Streptococcus pneumoniae, as revealed by sequence analysis , 1992, Journal of bacteriology.

[21]  R. Murray ON THE CELL WALL STRUCTURE OF SPIRILLUM SERPENS , 1963 .

[22]  G. Schulz,et al.  Structure of porin refined at 1.8 A resolution. , 1992, Journal of molecular biology.

[23]  A. Hoenger,et al.  The orientation of porin OmpF in the outer membrane of Escherichia coli. , 1993, Journal of molecular biology.

[24]  M. Stewart,et al.  Two patterns in the Aeromonas salmonicida A-layer may reflect a structural transformation that alters permeability , 1986, Journal of bacteriology.

[25]  P Béguin,et al.  A new type of cohesin domain that specifically binds the dockerin domain of the Clostridium thermocellum cellulosome-integrating protein CipA , 1996, Journal of bacteriology.

[26]  J. Aubert,et al.  Recognition specificity of the duplicated segments present in Clostridium thermocellum endoglucanase CelD and in the cellulosome-integrating protein CipA , 1994, Journal of bacteriology.

[27]  E Setter,et al.  Organization and distribution of the cellulosome in Clostridium thermocellum , 1985, Journal of bacteriology.

[28]  T J Beveridge,et al.  Participation of a cyanobacterial S layer in fine-grain mineral formation , 1992, Journal of bacteriology.

[29]  M. Blaser,et al.  A lipopolysaccharide-binding domain of the Campylobacter fetus S-layer protein resides within the conserved N terminus of a family of silent and divergent homologs , 1995, Journal of bacteriology.

[30]  U. Sleytr,et al.  Evidence for an S-layer protein pool in the peptidoglycan of Bacillus stearothermophilus , 1992, Journal of bacteriology.

[31]  J. Aubert,et al.  Cloning of a Clostridium thermocellum DNA fragment encoding polypeptides that bind the catalytic components of the cellulosome. , 1992, FEMS microbiology letters.

[32]  J. Šmarda S-Layer in Cyanobacteria , 1988 .

[33]  G. Antranikian,et al.  Immunocytochemical Identification and Localization of Active and Inactive α-Amylase and Pullulanase in Cells of Clostridium thermosulfurogenes EM1 , 1991, Applied and environmental microbiology.

[34]  U. Sleytr,et al.  Crystalline bacterial cell surface layers (S-layers): from cell structure to biomimetics. , 1996, Progress in biophysics and molecular biology.

[35]  M. R. Brown,et al.  Trojan horses of the microbial world: protozoa and the survival of bacterial pathogens in the environment. , 1994, Microbiology.

[36]  A C Steven,et al.  Ultrastructure of a periodic protein layer in the outer membrane of Escherichia coli , 1977, The Journal of cell biology.

[37]  J. Smit,et al.  The extreme N-terminus of the Caulobacter crescentus surface-layer protein directs export of passenger proteins from the cytoplasm but is not required for secretion of the native protein. , 1996, Canadian journal of microbiology.

[38]  T. Kawata,et al.  Distribution and chemical characterization of regular arrays in the cell walls of strains of the genus Lactobacillus , 1983 .

[39]  C. Breuil,et al.  Composition of Methanospirillum hungatii GP1 during growth on different media. , 1980, Canadian journal of microbiology.

[40]  L. Corbeil,et al.  Superficial antigens of Campylobacter (Vibrio) fetus: characterization of antiphagocytic component , 1975, Infection and immunity.

[41]  U. Sleytr,et al.  Evidence that an N-terminal S-layer protein fragment triggers the release of a cell-associated high-molecular-weight amylase in Bacillus stearothermophilus ATCC 12980 , 1996, Journal of bacteriology.

[42]  G. Harauz,et al.  The Organization of the Paracrystalline Multilayered Spacer-Plugs of Methanospirillum hungatei , 1994 .

[43]  O. Kandler,et al.  CHAPTER 9 – Cell Envelopes of Archaebacteria , 1985 .

[44]  P. Dhurjati,et al.  Properties conferred on Clostridium thermocellum endoglucanase CelC by grafting the duplicated segment of endoglucanase CelD. , 1993, Protein engineering.

[45]  J. Smit,et al.  Definition of form and Function for the S-Layer of Caulobacter crescentus , 1993 .

[46]  J. Smit,et al.  The Caulobacter crescentus holdfast: identification of holdfast attachment complex genes. , 1994, FEMS microbiology letters.

[47]  Mel Rosenberg,et al.  Hydrophobic interactions: role in bacterial adhesion , 1986 .

[48]  M. Blaser,et al.  Shift in S-layer protein expression responsible for antigenic variation in Campylobacter fetus , 1993, Journal of bacteriology.

[49]  S. Lortal Crystalline Surface-Layers of the Genus Lactobacillus , 1993 .

[50]  J. Smit,et al.  Alkaline phosphatase and a cellulase reporter protein are not exported from the cytoplasm when fused to large N-terminal portions of the Caulobacter crescentus surface (S)-layer protein. , 1994, Canadian journal of microbiology.

[51]  T. Beveridge,et al.  Comparative analyses of the sheath structures of Methanothrix concilii GP6 and Methanospirillum hungatei strains GP1 and JF1 , 1986 .

[52]  D. Stahl,et al.  The phylogeny of marine and freshwater caulobacters reflects their habitat , 1992, Journal of bacteriology.

[53]  D. S. Williams,et al.  Ultrastructure of Methanosarcina mazei , 1986 .

[54]  U. Sleytr,et al.  Molecular sieving through S layers of Bacillus stearothermophilus strains , 1987, Journal of bacteriology.

[55]  U. Sleytr,et al.  Comparative studies of S-layer proteins from Bacillus stearothermophilus strains expressed during growth in continuous culture under oxygen-limited and non-oxygen-limited conditions , 1994, Journal of bacteriology.

[56]  P. Gounon,et al.  Subcellular localization of Clostridium thermocellum ORF3p, a protein carrying a receptor for the docking sequence borne by the catalytic components of the cellulosome , 1994, Journal of bacteriology.

[57]  H. Bahl,et al.  Pullulanase of Thermoanaerobacterium thermosulfurigenes EM1 (Clostridium thermosulfurogenes): molecular analysis of the gene, composite structure of the enzyme, and a common model for its attachment to the cell surface , 1994, Journal of bacteriology.

[58]  G. Harauz,et al.  Characterization of the cell wall of the sheathed methanogen Methanospirillum hungatei GP1 as an S layer , 1993, Journal of bacteriology.

[59]  A. Demain,et al.  Sequencing of a Clostridium thermocellum gene (cipA) encoding the cellulosomal SL‐protein reveals an unusual degree of internal homology , 1993, Molecular microbiology.

[60]  J. Leong Molecular and biotechnological approaches to fish vaccines. , 1993, Current opinion in biotechnology.

[61]  J. Rosenbusch,et al.  Porin channel triplets merge into single outlets in Escherichia coli outer membranes , 1985, Nature.

[62]  N. Ravenscroft,et al.  Identification, isolation, and structural studies of the outer membrane lipopolysaccharide of Caulobacter crescentus , 1992, Journal of bacteriology.

[63]  J. Smit,et al.  Characterization of mutants of Caulobacter crescentus defective in surface attachment of the paracrystalline surface layer , 1994, Journal of bacteriology.

[64]  Eugene Rosenberg,et al.  Adherence of bacteria to hydrocarbons: A simple method for measuring cell‐surface hydrophobicity , 1980 .

[65]  W Baumeister,et al.  Bacterial surface proteins. Some structural, functional and evolutionary aspects. , 1988, Biophysical chemistry.

[66]  G. Sprott,et al.  Proportions of diether, macrocyclic diether, and tetraether lipids in Methanococcus jannaschii grown at different temperatures , 1991, Journal of bacteriology.

[67]  J. Carrascosa,et al.  S‐layer protein from Thermus thermophilus HB8 assembles into porin‐like structures , 1993, Molecular microbiology.

[68]  M. de Pedro,et al.  Purification, composition and Ca2+‐binding properties of the monomeric protein of the S‐layer of Thermus thermophilus , 1988 .

[69]  C. K. Hansen,et al.  Fibronectin type III‐like sequences and a new domain type in prokaryotic depolymerases with insoluble substrates , 1992, FEBS letters.

[70]  W. Baumeister,et al.  Structure of the porin from a bacterial stalk , 1987, FEBS letters.

[71]  J. Heijenoort,et al.  Cell wall and autolytic system of Lactobacillus helveticus ATCC 12046 , 1991 .

[72]  Vincent A. Fischetti,et al.  Sorting of protein a to the staphylococcal cell wall , 1992, Cell.

[73]  T. Beveridge Mechanism of gram variability in select bacteria , 1990, Journal of bacteriology.

[74]  E. Bayer,et al.  Ultrastructure of the cell surface cellulosome of Clostridium thermocellum and its interaction with cellulose , 1986, Journal of bacteriology.

[75]  P. Dhurjati,et al.  Interaction of the duplicated segment carried by Clostridium thermocellum cellulases with cellulosome components , 1991, FEBS letters.

[76]  J. Smit,et al.  Isolation and comparison of the paracrystalline surface layer proteins of freshwater caulobacters , 1992, Journal of bacteriology.

[77]  M. Landry,et al.  Discrimination between living and heat-killed prey by a marine zooflagellate, Paraphysomonas vestita (Stokes) , 1991 .

[78]  S. Koval,et al.  Effect of paracrystalline protein surface layers on predation by Bdellovibrio bacteriovorus , 1991, Journal of bacteriology.

[79]  T. Beveridge,et al.  The response of selected members of the archaea to the gram stain. , 1996, Microbiology.

[80]  U. Sleytr,et al.  Can S-Layers of Bacillaceae Control the Release of Their Own Exoproteins ? , 1993 .

[81]  J. H. Hannah,et al.  Orientation of porin channels in the outer membrane of Bordetella pertussis , 1993, Molecular microbiology.

[82]  T. Trust,et al.  Synthesis, export, and assembly of Aeromonas salmonicida A-layer analyzed by transposon mutagenesis , 1985, Journal of bacteriology.

[83]  P. Peterson,et al.  Influence of encapsulation on staphylococcal opsonization and phagocytosis by human polymorphonuclear leukocytes , 1978, Infection and immunity.

[84]  S. Lortal,et al.  X-ray Photoelectron-spectroscopy and Biochemical-analysis of the Surface of Lactobacillus-helveticus Atcc-12046 , 1995 .

[85]  T. Beveridge,et al.  Immunochemistry and localization of the enzyme disaggregatase in Methanosarcina mazei , 1993, Journal of bacteriology.

[86]  J. Smit,et al.  Transcriptional analysis of the major surface array gene of Caulobacter crescentus , 1988, Journal of bacteriology.

[87]  D. Absolom The role of bacterial hydrophobicity in infection: bacterial adhesion and phagocytic ingestion. , 1988, Canadian journal of microbiology.

[88]  L. Shapiro,et al.  The expression of asymmetry during Caulobacter cell differentiation. , 1994, Annual review of biochemistry.

[89]  Christopher H. King,et al.  Enhancement of Edwardsiella tarda and Aeromonas salmonicida through ingestion by the ciliated protozoan Tetrahymena pyriformis , 1988 .

[90]  D. Ellar,et al.  Orded substructure in the cell wall of Bacillus cereus , 1967, Journal of bacteriology.

[91]  A Bairoch,et al.  New families in the classification of glycosyl hydrolases based on amino acid sequence similarities. , 1993, The Biochemical journal.

[92]  P. Pouwels,et al.  Identification, cloning, and nucleotide sequence of a silent S-layer protein gene of Lactobacillus acidophilus ATCC 4356 which has extensive similarity with the S-layer protein gene of this species , 1995, Journal of bacteriology.

[93]  P. Gounon,et al.  OlpB, a new outer layer protein of Clostridium thermocellum, and binding of its S-layer-like domains to components of the cell envelope , 1995, Journal of bacteriology.

[94]  W. Baumeister,et al.  Isolation and cloning of Omp alpha, a coiled‐coil protein spanning the periplasmic space of the ancestral eubacterium Thermotoga maritima. , 1992, The EMBO journal.

[95]  J. Heijenoort,et al.  S-layer of Lactobacillus helveticus ATCC 12046: isolation, chemical characterization and re-formation after extraction with lithium chloride , 1992 .

[96]  U. Sleytr,et al.  The S-layer from Bacillus stearothermophilus DSM 2358 functions as an adhesion site for a high-molecular-weight amylase , 1995, Journal of bacteriology.

[97]  R. Murray,et al.  Components of the regular surface array of Aquaspirillum serpens MW5 and their assembly in vitro , 1984, Journal of bacteriology.

[98]  G. Sprott,et al.  Structures of polar lipids from the thermophilic, deep-sea archaeobacterium Methanococcus jannaschii. , 1990, Biochemistry and cell biology = Biochimie et biologie cellulaire.

[99]  T. Beveridge,et al.  Cell division and filament splitting in Methanothrix concilii , 1986 .

[100]  H. König Archaeobacterial cell envelopes , 1988 .

[101]  J. White,et al.  Novel surface attachment mechanism of the Streptococcus pneumoniae protein PspA , 1994, Journal of bacteriology.

[102]  W. Liebl,et al.  Identification of a novel cellulose‐binding domain the multidomain 120 kDa xylanase XynA of the hyperthermophilic bacterium Thermotoga maritima , 1995 .

[103]  M. Brennan,et al.  Type 2 fimbrial lectin-mediated phagocytosis of oral Actinomyces spp. by polymorphonuclear leukocytes , 1986, Infection and immunity.

[104]  K. Lounatmaa,et al.  Eubacterium yurii subspecies margaretiae is resistant to nonopsonic phagocytic ingestion. , 1993, Scandinavian journal of dental research.

[105]  P. Pouwels,et al.  S-layer protein of Lactobacillus acidophilus ATCC 4356: purification, expression in Escherichia coli, and nucleotide sequence of the corresponding gene , 1993, Journal of bacteriology.

[106]  T. Beveridge Ultrastructure, chemistry, and function of the bacterial wall. , 1981, International review of cytology.

[107]  R. Huber,et al.  A porin‐type protein is the main constituent of the cell envelope of the ancestral eubacterium Thermotoga maritima , 1990 .

[108]  M. Stewart,et al.  Unusual stability of the Methanospirillum hungatei sheath , 1985, Journal of bacteriology.

[109]  H. Jespersen,et al.  Comparison of the domain-level organization of starch hydrolases and related enzymes. , 1991, The Biochemical journal.

[110]  K. Lounatmaa,et al.  Ingestion of Bacteroides buccae, Bacteroides oris, Porphyromonas gingivalis, and Fusobacterium nucleatum by human polymorphonuclear leukocytes in vitro. , 1990, Oral microbiology and immunology.

[111]  O. Schneewind,et al.  Proteolytic cleavage and cell wall anchoring at the LPXTG motif of surface proteins in Gram‐positive bacteria , 1994, Molecular microbiology.

[112]  C. Choquet,et al.  Freeze-fracture planes of methanogen membranes correlate with the content of tetraether lipids , 1993, Journal of bacteriology.

[113]  R. Glaeser,et al.  Periodic surface array in Caulobacter crescentus: fine structure and chemical analysis , 1981, Journal of bacteriology.

[114]  J. Smit,et al.  Transformation of freshwater and marine caulobacters by electroporation , 1991, Journal of bacteriology.

[115]  E. Ishiguro,et al.  Loss of virulence during culture of Aeromonas salmonicida at high temperature , 1981, Journal of bacteriology.

[116]  T. Beveridge,et al.  Advances in Bacterial Paracrystalline Surface Layers , 1993, NATO ASI Series.

[117]  Henry C. Wu,et al.  Lipoproteins in bacteria , 1990, Journal of bioenergetics and biomembranes.

[118]  M. Kostrzynska,et al.  Antigenic differences among Campylobacter fetus S-layer proteins , 1990, Journal of bacteriology.

[119]  T. Beveridge,et al.  Septation and filament splitting in Methanospirillum hungatei , 1987 .

[120]  B. Trus,et al.  Naturally crystalline porin in the outer membrane of Bordetella pertussis. , 1988, Journal of molecular biology.

[121]  K. Lounatmaa,et al.  Hexagonal periodicity in the outer membrane of Bacteroides buccae. , 1987, Journal of general microbiology.

[122]  Linker mutagenesis of the Caulobacter crescentus S-layer protein: toward a definition of an N-terminal anchoring region and a C-terminal secretion signal and the potential for heterologous protein secretion , 1997, Journal of bacteriology.

[123]  P. Patriarca,et al.  Evidence for the involvement of human polymorphonuclear leucocyte mannose‐like receptors in the phagocytosis of Escherichia coli , 1979, FEBS letters.

[124]  T J Beveridge,et al.  Periplasmic space and the concept of the periplasm. , 1991, Trends in biochemical sciences.

[125]  A. Demain,et al.  Two components of an extracellular protein aggregate of Clostridium thermocellum together degrade crystalline cellulose , 1988 .

[126]  W Baumeister,et al.  Domain structure of the Acetogenium kivui surface layer revealed by electron crystallography and sequence analysis , 1994, Journal of bacteriology.

[127]  J. Ferry,et al.  Effect of molybdenum and tungsten on synthesis and composition of formate dehydrogenase in Methanobacterium formicicum , 1988, Journal of bacteriology.

[128]  F Mandl,et al.  Dynamics in oxygen-induced changes in S-layer protein synthesis from Bacillus stearothermophilus PV72 and the S-layer-deficient variant T5 in continuous culture and studies of the cell wall composition , 1996, Journal of bacteriology.

[129]  M. Blaser,et al.  Pathogenesis of Campylobacter fetus infections. Failure of encapsulated Campylobacter fetus to bind C3b explains serum and phagocytosis resistance. , 1988, The Journal of clinical investigation.

[130]  J. Smit,et al.  A transducing bacteriophage for Caulobacter crescentus uses the paracrystalline surface layer protein as a receptor , 1991, Journal of bacteriology.

[131]  J. Smit,et al.  Cloning of the major protein of the Caulobacter crescentus periodic surface layer: detection and characterization of the cloned peptide by protein expression assays , 1984, Journal of bacteriology.

[132]  T J Beveridge,et al.  Cellular responses of Bacillus subtilis and Escherichia coli to the Gram stain , 1983, Journal of bacteriology.

[133]  D. Cabral,et al.  Nonopsonic phagocytosis of nonmucoid Pseudomonas aeruginosa by human neutrophils and monocyte-derived macrophages is correlated with bacterial piliation and hydrophobicity , 1986, Infection and immunity.

[134]  M. Sela,et al.  Inhibition of superoxide production in human polymorphonuclear leukocytes by oral treponemal factors , 1988, Infection and immunity.

[135]  E. Bayer,et al.  Relationship of cellulosomal and noncellulosomal xylanases of Clostridium thermocellum to cellulose-degrading enzymes , 1990, Journal of bacteriology.

[136]  M. Blaser,et al.  Pathogenesis of Campylobacter fetus infections. Role of surface array proteins in virulence in a mouse model. , 1990, The Journal of clinical investigation.

[137]  H. Yamada,et al.  Morphological alterations of cell wall concomitant with protein release in a protein-producing bacterium, Bacillus brevis 47 , 1981, Journal of bacteriology.

[138]  R. Scherrer Cell structure and quantitative gram stain of Bacillus megaterium. , 1963, Journal of General Microbiology.

[139]  T. Beveridge,et al.  Chemical mechanism of the Gram stain and synthesis of a new electron-opaque marker for electron microscopy which replaces the iodine mordant of the stain , 1983, Journal of bacteriology.

[140]  T. Beveridge,et al.  Physicochemical characteristics of the mineral-forming S-layer from the cyanobacterium Synechococcus strain GL24 , 1994 .

[141]  A. Archibald The Bacillus Cell Envelope , 1989 .

[142]  A. Tärnvik,et al.  Degradation of human immunoglobulins G and M and complement factors C3 and C5 by black-pigmented Bacteroides. , 1985, Journal of medical microbiology.

[143]  J. Accolas,et al.  Comparative Study of 35 Bacteriophages of Lactobacillus helveticus: Morphology and Host Range , 1992, Applied and environmental microbiology.

[144]  T. Beveridge,et al.  Characterization of a dynamic S layer on Bacillus thuringiensis , 1989, Journal of bacteriology.

[145]  J. Smit,et al.  High-level expression vectors for Caulobacter crescentus incorporating the transcription/translation initiation regions of the paracrystalline surface-layer-protein gene. , 1990, Plasmid.

[146]  P. Model,et al.  Cell wall sorting signals in surface proteins of gram‐positive bacteria. , 1993, The EMBO journal.

[147]  J. Smit,et al.  Nucleotide sequence analysis of the gene encoding the Caulobacter crescentus paracrystalline surface layer protein. , 1992, Canadian journal of microbiology.