Structure and Function of Bacterial Super-Biosystem Responsible for Import and Depolymerization of Macromolecules

Generally, when microbes assimilate macromolecules, they incorporate low-molecular-weight products derived from macromolecules through the actions of extracellular degrading enzymes. However, a Gram-negative bacterium, Sphingomonas sp. A1, has a smart biosystem for the import and depolymerization of macromolecules. The bacterial cells directly incorporate a macromolecule, alginate, into the cytoplasm through a “superchannel”, as we named it. The superchannel consists of a pit on the cell surface, alginate-binding proteins in the periplasm, and an ATP-binding cassette transporter in the inner membrane. Cytoplasmic polysaccharide lyases depolymerize alginate into the constituent monosaccharides. Other than the proteins characterized so far, novel proteins (e.g., flagellin homologs) have been found to be crucial for the import and depolymerization of alginate through genomics- and proteomics-based identification, thus indicating that the biosystem is precisely constructed and regulated by diverse proteins. In this review, we focus on the structure and function of the bacterial biosystem together with the evolution of related proteins.

[1]  Wataru Hashimoto,et al.  Direct evidence for Sphingomonas sp. A1 periplasmic proteins as macromolecule-binding proteins associated with the ABC transporter: molecular insights into alginate transport in the periplasm. , 2005, Biochemistry.

[2]  B. Mikami,et al.  Crystallization and preliminary X-ray analysis of alginate lyases A1-II and A1-II' from Sphingomonas sp. A1. , 2005, Acta crystallographica. Section F, Structural biology and crystallization communications.

[3]  K. Murata,et al.  Molecular identification of Sphingomonas sp. A1 alginate lyase (A1-IV') as a member of novel polysaccharide lyase family 15 and implications in alginate lyase evolution. , 2005, Journal of bioscience and bioengineering.

[4]  Wataru Hashimoto,et al.  Molecular identification and characterization of an alginate-binding protein on the cell surface of Sphingomonas sp. A1. , 2004, Biochemical and biophysical research communications.

[5]  B. Mikami,et al.  Structure and Function of a Hypothetical Pseudomonas aeruginosa Protein PA1167 Classified into Family PL-7 , 2004, Journal of Biological Chemistry.

[6]  B. Mikami,et al.  Crystal Structure of Unsaturated Glucuronyl Hydrolase, Responsible for the Degradation of Glycosaminoglycan, from Bacillus sp. GL1 at 1.8 Å Resolution* , 2004, Journal of Biological Chemistry.

[7]  T. Basta,et al.  Detection and Characterization of Conjugative Degradative Plasmids in Xenobiotic-Degrading Sphingomonas Strains , 2004, Journal of bacteriology.

[8]  Jue Chen,et al.  ATP-binding cassette transporters in bacteria. , 2004, Annual review of biochemistry.

[9]  S. Larsen,et al.  Rhamnogalacturonan lyase reveals a unique three‐domain modular structure for polysaccharide lyase family 4 , 2004, FEBS letters.

[10]  K. Murata,et al.  Origin and Diversity of Alginate Lyases of Families PL-5 and -7 in Sphingomonas sp. Strain A1 , 2004, Journal of bacteriology.

[11]  S. Lory,et al.  Sequence Polymorphism in the Glycosylation Island and Flagellins of Pseudomonas aeruginosa , 2004, Journal of bacteriology.

[12]  C. Hughes,et al.  Docking of cytosolic chaperone-substrate complexes at the membrane ATPase during flagellar type III protein export. , 2004, Proceedings of the National Academy of Sciences of the United States of America.

[13]  R. Pickersgill,et al.  The Crystal Structure of Pectate Lyase Pel9A from Erwinia chrysanthemi* , 2004, Journal of Biological Chemistry.

[14]  B. Mikami,et al.  Posttranslational processing of polysaccharide lyase: maturation route for gellan lyase in Bacillus sp. GL1. , 2004, Archives of biochemistry and biophysics.

[15]  B. Mikami,et al.  Structure and Function of a Hypothetical Pseudomonas aeruginosa Protein PA1167 Classified into Family PL-7 A NOVEL ALGINATE LYASE WITH A -SANDWICH FOLD* , 2004 .

[16]  Jia Liu,et al.  The complete genome sequence of the Arabidopsis and tomato pathogen Pseudomonas syringae pv. tomato DC3000 , 2003, Proceedings of the National Academy of Sciences of the United States of America.

[17]  K. Namba,et al.  Complete atomic model of the bacterial flagellar filament by electron cryomicroscopy , 2003, Nature.

[18]  B. Mikami,et al.  Crystallization and preliminary X-ray analysis of alginate lyase, a member of family PL-7, from Pseudomonas aeruginosa. , 2003, Acta crystallographica. Section D, Biological crystallography.

[19]  K. Murata,et al.  Molecular identification of an alpha-L-rhamnosidase from Bacillus sp strain GL1 as an enzyme involved in complete metabolism of gellan. , 2003, Archives of biochemistry and biophysics.

[20]  Li-Chu Tsai,et al.  Crystal structure of a natural circularly permuted jellyroll protein: 1,3-1,4-beta-D-glucanase from Fibrobacter succinogenes. , 2003, Journal of molecular biology.

[21]  B. Mikami,et al.  A novel member of glycoside hydrolase family 88: overexpression, purification, and characterization of unsaturated beta-glucuronyl hydrolase of Bacillus sp. GL1. , 2003, Protein expression and purification.

[22]  K. Murata,et al.  An exotype alginate lyase in Sphingomonas sp. A1: overexpression in Escherichia coli, purification, and characterization of alginate lyase IV (A1-IV). , 2003, Protein expression and purification.

[23]  B. Mikami,et al.  Crystal Structure of Bacillus sp. GL1 Xanthan Lyase, Which Acts on the Side Chains of Xanthan* , 2003, The Journal of Biological Chemistry.

[24]  B. Mikami,et al.  Crystal Structure of AlgQ2, a Macromolecule (Alginate)-binding Protein of Sphingomonas sp. A1, Complexed with an Alginate Tetrasaccharide at 1.6-Å Resolution* , 2003, The Journal of Biological Chemistry.

[25]  R. Shimizu,et al.  The ΔfliD mutant of Pseudomonas syringae pv. tabaci, which secretes flagellin monomers, induces a strong hypersensitive reaction (HR) in non-host tomato cells , 2003, Molecular Genetics and Genomics.

[26]  B. Mikami,et al.  A Super-Channel in Bacteria: Macro-molecule Uptake and Depolymerization Systems of Sphingomonas sp. Al with a Special Cell Surface Structure , 2002, Biotechnology & genetic engineering reviews.

[27]  K. Murata,et al.  Biodegradation of Alginate, Xanthan, and Gellan , 2002 .

[28]  Satoshi Murakami,et al.  Crystal structure of bacterial multidrug efflux transporter AcrB , 2002, Nature.

[29]  J. Turkenburg,et al.  Convergent evolution sheds light on the anti-β-elimination mechanism common to family 1 and 10 polysaccharide lyases , 2002, Proceedings of the National Academy of Sciences of the United States of America.

[30]  B. Mikami,et al.  X-ray structural analysis of alginate lyase A1-III mutants/substrate complexes: activation of a catalytic tyrosine residue by a flexible lid loop , 2002 .

[31]  Bert L de Groot,et al.  Mechanism of hyaluronan degradation by Streptococcus pneumoniae hyaluronate lyase. Structures of complexes with the substrate. , 2002, The Journal of biological chemistry.

[32]  K. Murata,et al.  Molecular Identification of Family 38 α-Mannosidase of Bacillus sp. Strain GL1, Responsible for Complete Depolymerization of Xanthan , 2002, Applied and Environmental Microbiology.

[33]  T. Tamura,et al.  Preparation and properties of alginate lyase modified with poly(ethylene glycol). , 2002, Journal of pharmaceutical sciences.

[34]  M. Lascombe,et al.  Atomic (0.94 A) resolution structure of an inverting glycosidase in complex with substrate. , 2002, Journal of molecular biology.

[35]  B. Mikami,et al.  Crystal structure of AlgQ2, a macromolecule (alginate)-binding protein of Sphingomonas sp. A1 at 2.0A resolution. , 2002, Journal of molecular biology.

[36]  Lilly Y. W. Bourguignon,et al.  Signaling Properties of Hyaluronan Receptors* , 2002, The Journal of Biological Chemistry.

[37]  T. Yamane,et al.  The first structure of pectate lyase belonging to polysaccharide lyase family 3. , 2001, Acta crystallographica. Section D, Biological crystallography.

[38]  Songlin Li,et al.  Hyaluronan Binding and Degradation byStreptococcus agalactiae Hyaluronate Lyase* , 2001, The Journal of Biological Chemistry.

[39]  R. Macnab,et al.  The role in flagellar rod assembly of the N-terminal domain of Salmonella FlgJ, a flagellum-specific muramidase. , 2001, Journal of molecular biology.

[40]  C. B. Roth,et al.  Structure of MsbA from E. coli: a homolog of the multidrug resistance ATP binding cassette (ABC) transporters. , 2001, Science.

[41]  H. van Tilbeurgh,et al.  Crystal structure of maltose phosphorylase from Lactobacillus brevis: unexpected evolutionary relationship with glucoamylases. , 2001, Structure.

[42]  B. Mikami,et al.  Crystallization and preliminary X-ray analysis of AlgS, a bacterial ATP-binding cassette (ABC) protein specific to macromolecule import. , 2001, Acta crystallographica. Section D, Biological crystallography.

[43]  H. Ikushiro,et al.  A water-soluble homodimeric serine palmitoyltransferase from Sphingomonas paucimobilis EY2395T strain. Purification, characterization, cloning, and overproduction. , 2001, The Journal of biological chemistry.

[44]  S. Akira,et al.  The innate immune response to bacterial flagellin is mediated by Toll-like receptor 5 , 2001, Nature.

[45]  B. Mikami,et al.  Crystal structure of alginate lyase A1-III complexed with trisaccharide product at 2.0 A resolution. , 2001, Journal of molecular biology.

[46]  Takashi Kumasaka,et al.  Structure of the bacterial flagellar protofilament and implications for a switch for supercoiling , 2001, Nature.

[47]  K. Murata,et al.  Polysaccharide Lyase: Molecular Cloning, Sequencing, and Overexpression of the Xanthan Lyase Gene of Bacillus sp. Strain GL1 , 2001, Applied and Environmental Microbiology.

[48]  R. Linhardt,et al.  Active site of chondroitin AC lyase revealed by the structure of enzyme-oligosaccharide complexes and mutagenesis. , 2001, Biochemistry.

[49]  B. Mikami,et al.  Super-channel in Bacteria: Function and Structure of a Macromolecule Import System Mediated by a Pit-dependent ABC Transporter , 2001, FEMS microbiology letters.

[50]  B. Mikami,et al.  Crystal structure of N-acyl-D-glucosamine 2-epimerase from porcine kidney at 2.0 A resolution. , 2000, Journal of molecular biology.

[51]  S. Lory,et al.  Complete genome sequence of Pseudomonas aeruginosa PAO1, an opportunistic pathogen , 2000, Nature.

[52]  S. Kawai,et al.  Molecular Identification of Oligoalginate Lyase ofSphingomonas sp. Strain A1 as One of the Enzymes Required for Complete Depolymerization of Alginate , 2000, Journal of bacteriology.

[53]  J. Cruz,et al.  Macrophage Damage by Leishmania amazonensis Cytolysin: Evidence of Pore Formation on Cell Membrane , 2000, Infection and Immunity.

[54]  K. Murata,et al.  A Novel Bacterial ATP-Binding Cassette Transporter System That Allows Uptake of Macromolecules , 2000, Journal of bacteriology.

[55]  Colin Hughes,et al.  Crystal structure of the bacterial membrane protein TolC central to multidrug efflux and protein export , 2000, Nature.

[56]  M. J. Jedrzejas,et al.  Mechanism of hyaluronan binding and degradation: structure of Streptococcus pneumoniae hyaluronate lyase in complex with hyaluronic acid disaccharide at 1.7 A resolution. , 2000, Journal of molecular biology.

[57]  B. Mikami,et al.  Overexpression in Escherichia coli, purification, and characterization of Sphingomonas sp. A1 alginate lyases. , 2000, Protein expression and purification.

[58]  P. Howell,et al.  Crystal structure of a class I α1,2‐mannosidase involved in N‐glycan processing and endoplasmic reticulum quality control , 2000, The EMBO journal.

[59]  B. Mikami,et al.  Crystallization and preliminary X-ray crystallographic analysis of alginate lyase A1-II from Sphingomonas species A1. , 2000, Biochimica et biophysica acta.

[60]  L M Harvey,et al.  Gellan Gum , 2000, Critical reviews in biotechnology.

[61]  N. Schiller,et al.  ALGINATE LYASE: review of major sources and enzyme characteristics, structure-function analysis, biological roles, and applications. , 2000, Annual review of microbiology.

[62]  A. Matte,et al.  Crystal structure of chondroitinase B from Flavobacterium heparinum and its complex with a disaccharide product at 1.7 A resolution. , 1999, Journal of molecular biology.

[63]  D. White,et al.  Preface to special issue on Sphingomonas , 1999, Journal of Industrial Microbiology and Biotechnology.

[64]  S. Kawai,et al.  Unsaturated glucuronyl hydrolase of Bacillus sp. GL1: novel enzyme prerequisite for metabolism of unsaturated oligosaccharides produced by polysaccharide lyases. , 1999, Archives of biochemistry and biophysics.

[65]  S. Kawai,et al.  Characterization of alpha-L-rhamnosidase of Bacillus sp. GL1 responsible for the complete depolymerization of gellan. , 1999, Archives of biochemistry and biophysics.

[66]  B. Mikami,et al.  Crystal structure of alginate lyase A1-III from Sphingomonas species A1 at 1.78 A resolution. , 1999, Journal of molecular biology.

[67]  M. Shimizu Modulation of intestinal functions by food substances. , 1999, Die Nahrung.

[68]  S. Kawai,et al.  Microbial System for Polysaccharide Depolymerization: Enzymatic Route for Xanthan Depolymerization by Bacillus sp. Strain GL1 , 1999, Applied and Environmental Microbiology.

[69]  J. Costerton,et al.  Bacterial biofilms: a common cause of persistent infections. , 1999, Science.

[70]  Y. Kamio,et al.  Assembly of Staphylococcus aureus leukocidin into a pore-forming ring-shaped oligomer on human polymorphonuclear leukocytes and rabbit erythrocytes. , 1999, Bioscience, biotechnology, and biochemistry.

[71]  D. Pappin,et al.  Re‐evaluation of the primary structure of Ralstonia eutropha phasin and implications for polyhydroxyalkanoic acid granule binding , 1999, FEBS letters.

[72]  L. Wyns,et al.  Carbohydrate binding, quaternary structure and a novel hydrophobic binding site in two legume lectin oligomers from Dolichos biflorus. , 1999, Journal of molecular biology.

[73]  J. Deisenhofer,et al.  Crystal structure of the outer membrane active transporter FepA from Escherichia coli , 1999, Nature Structural Biology.

[74]  Luc Moulinier,et al.  Transmembrane Signaling across the Ligand-Gated FhuA Receptor Crystal Structures of Free and Ferrichrome-Bound States Reveal Allosteric Changes , 1998, Cell.

[75]  S. Kawai,et al.  Molecular cloning of two genes for beta-D-glucosidase in Bacillus sp. GL1 and identification of one as a gellan-degrading enzyme. , 1998, Archives of biochemistry and biophysics.

[76]  Christopher M Thomas,et al.  Complete sequence of the IncPbeta plasmid R751: implications for evolution and organisation of the IncP backbone. , 1998, Journal of molecular biology.

[77]  K. Murata,et al.  Xanthan Lyase of Bacillus sp. Strain GL1 Liberates Pyruvylated Mannose from Xanthan Side Chains , 1998, Applied and Environmental Microbiology.

[78]  Z. Dauter,et al.  Structure of glucoamylase from Saccharomycopsis fibuligera at 1.7 A resolution. , 1998, Acta crystallographica. Section D, Biological crystallography.

[79]  K. Murata,et al.  Polysaccharide lyase: molecular cloning of gellan lyase gene and formation of the lyase from a huge precursor protein in Bacillus sp. GL1. , 1998, Archives of biochemistry and biophysics.

[80]  B. Chait,et al.  The structure of the potassium channel: molecular basis of K+ conduction and selectivity. , 1998, Science.

[81]  K. Murata,et al.  Sphingomonas sp. A1 lyase active on both poly-β-d-mannuronate and heteropolymeric regions in alginate , 1998 .

[82]  K. Murata,et al.  alpha-L-rhamnosidase of Sphingomonas sp. R1 producing an unusual exopolysaccharide of sphingan. , 1998, Bioscience, biotechnology, and biochemistry.

[83]  P. Karplus,et al.  Structure and mechanism of endo/exocellulase E4 from Thermomonospora fusca , 1997, Nature Structural Biology.

[84]  K. Hara,et al.  Stimulation of human keratinocyte growth by alginate oligosaccharides, a possible co‐factor for epidermal growth factor in cell culture , 1997, FEBS letters.

[85]  H. Kumagai,et al.  Microbial system for polysaccharide depolymerization: enzymatic route for gellan depolymerization by Bacillus sp. GL1. , 1997, Archives of biochemistry and biophysics.

[86]  C. Baker,et al.  Group B streptococcal infections. , 1997, Clinics in perinatology.

[87]  S. Valla,et al.  Bacterial alginates: biosynthesis and applications , 1997, Applied Microbiology and Biotechnology.

[88]  C. Bompard-Gilles,et al.  Substrate mimicry in the active center of a mammalian alpha-amylase: structural analysis of an enzyme-inhibitor complex. , 1996, Structure.

[89]  D. White,et al.  The genus Sphingomonas: physiology and ecology. , 1996, Current opinion in biotechnology.

[90]  K. Murata,et al.  Purification and characterization of microbial gellan lyase , 1996, Applied and environmental microbiology.

[91]  K. Murata,et al.  Pit structure on bacterial cell surface. , 1996, Biochemical and biophysical research communications.

[92]  R. Dominguez,et al.  The crystal structure of endoglucanase CelA, a family 8 glycosyl hydrolase from Clostridium thermocellum. , 1996, Structure.

[93]  M C Peitsch,et al.  ProMod and Swiss-Model: Internet-based tools for automated comparative protein modelling. , 1996, Biochemical Society transactions.

[94]  S. Aizawa Flagellar assembly in Salmonella typhimurium , 1996, Molecular microbiology.

[95]  R. Macnab,et al.  Flagella and motility , 1996 .

[96]  D. Balkwill,et al.  Aromatic-degrading Sphingomonas isolates from the deep subsurface , 1995, Applied and environmental microbiology.

[97]  K. Murata,et al.  Direct uptake of alginate molecules through a pit on the bacterial cell surface: A novel mechanism for the uptake of macromolecules , 1995 .

[98]  A. Yokota,et al.  Phylogenetic evidence for Sphingomonas and Rhizomonas as nonphotosynthetic members of the alpha-4 subclass of the Proteobacteria. , 1994, International journal of systematic bacteriology.

[99]  S. Kawasaki,et al.  The cell envelope structure of the lipopolysaccharide-lacking gram-negative bacterium Sphingomonas paucimobilis , 1994, Journal of bacteriology.

[100]  T. Imanaka,et al.  A simple method for determination of substrate specificity of alginate lyases , 1994 .

[101]  K. Murata,et al.  On the self-processing of bacterial alginate lyase , 1994 .

[102]  T. J. Pollock Gellan-related polysaccharides and the genus Sphingomonas , 1993 .

[103]  M. Yoder,et al.  New domain motif: the structure of pectate lyase C, a secreted plant virulence factor. , 1993, Science.

[104]  Y. Ishida,et al.  Promotion of germination and shoot elongation of some plants by alginate oligomers prepared with bacterial alginate lyase , 1993 .

[105]  K. Murata,et al.  Bacterial alginate lyase gene : nucleotide sequence and molecular route for generation of alginate lyase species , 1993 .

[106]  K. Murata,et al.  Bacterial Alginate Lyase Inactive on Alginate Biosynthesized by Pseudomonas aeruginosa , 1993 .

[107]  T. Imanaka,et al.  Bacterial alginate lyase: Enzymology, genetics and application , 1993 .

[108]  A. Golubev,et al.  Crystal structure of glucoamylase from Aspergillus awamori var. X100 to 2.2-A resolution. , 1994, The Journal of biological chemistry.

[109]  F. Quiocho,et al.  Crystallographic evidence of a large ligand-induced hinge-twist motion between the two domains of the maltodextrin binding protein involved in active transport and chemotaxis. , 1992, Biochemistry.

[110]  P. Alzari,et al.  Three-dimensional structure of a thermostable bacterial cellulase , 1992, Nature.

[111]  H. Wilkes,et al.  Metabolism of dibenzo-p-dioxin by Sphingomonas sp. strain RW1 , 1992, Applied and environmental microbiology.

[112]  K. Murata,et al.  Effect of depolymerized alginates on the growth of bifidobacteria. , 1992, Bioscience, biotechnology, and biochemistry.

[113]  K. Murata,et al.  Cloning of a gene for intracellular alginate lyase in a bacterium isolated from a ditch , 1992 .

[114]  F. Quiocho,et al.  The 2.3-A resolution structure of the maltose- or maltodextrin-binding protein, a primary receptor of bacterial active transport and chemotaxis. , 1992, The Journal of biological chemistry.

[115]  G. Griffiths,et al.  A T. cruzi-secreted protein immunologically related to the complement component C9: Evidence for membrane pore-forming activity at low pH , 1990, Cell.

[116]  T. Ezaki,et al.  Proposals of Sphingomonas paucimobilis gen. nov. and comb. nov., Sphingomonas parapaucimobilis sp. nov., Sphingomonas yanoikuyae sp. nov., Sphingomonas adhaesiva sp. nov., Sphingomonas capsulata comb, nov., and Two Genospecies of the Genus Sphingomonas , 1990, Microbiology and immunology.

[117]  M. N. Vyas,et al.  Sugar and signal-transducer binding sites of the Escherichia coli galactose chemoreceptor protein. , 1988, Science.

[118]  C. Baker,et al.  Group B Streptococcal Infections , 1988 .

[119]  C. Cooney,et al.  Polysaccharide lyases , 1986, Applied biochemistry and biotechnology.

[120]  John F. Kennedy,et al.  Production, properties and applications of Xanthan , 1984 .

[121]  Per-Erik Jansson,et al.  Structural studies of gellan gum, an extracellular polysaccharide elaborated by Pseudomonas elodea , 1983 .

[122]  P. Jansson,et al.  Structure of extracellular polysaccharide from Xanthomonas campestris. , 1975, Carbohydrate research.

[123]  O. Smidsrod,et al.  Uronic acid sequence in alginate from different sources , 1974 .

[124]  M. Cadmus,et al.  Production of polysaccharide with Xanthomonas campestris , 1961 .