Periplasmic chitooligosaccharide-binding protein requires a three-domain organization for substrate translocation – Scientific Reports

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  • Gooday, G. W. Aggressive and defensive roles for chitinases. EXS 87, 157–169 (1999).

    CAS 
    PubMed 

    Google Scholar
     

  • Zhang, R., Zhou, J., Song, Z. & Huang, Z. Enzymatic properties of β-N-acetylglucosaminidases. Appl. Microbiol. Biotechnol. 102, 93–103 (2018).

    Article 
    CAS 
    PubMed 

    Google Scholar
     

  • Bonin, M., Sreekumar, S., Cord-Landwehr, S. & Moerschbacher, B. M. Preparation of defined chitosan oligosaccharides using chitin deacetylases. Int. J. Mol. Sci. 21, 7835 (2020).

    Article 
    CAS 
    PubMed 
    PubMed Central 

    Google Scholar
     

  • Loose, J. S., Forsberg, Z., Fraaije, M. W., Eijsink, V. G. & Vaaje-Kolstad, G. A rapid quantitative activity assay shows that the Vibrio cholerae colonization factor GbpA is an active lytic polysaccharide monooxygenase. FEBS Lett. 588, 3435–3440 (2014).

    Article 
    CAS 
    PubMed 

    Google Scholar
     

  • Muthukrishnan, S., Merzendorfer, H., Arakane, Y. & Yang, Q. Chitin organizing and modifying enzymes and proteins involved in remodeling of the insect cuticle. Adv. Exp. Med. Biol. 1142, 83–114 (2019).

    Article 
    CAS 
    PubMed 

    Google Scholar
     

  • Nazari, B. et al. Chitin-induced gene expression in secondary metabolic pathways of Streptomyces coelicolor A3(2) grown in soil. Appl. Environ. Microbiol. 79, 707–713 (2013).

    Article 
    ADS 
    CAS 
    PubMed 
    PubMed Central 

    Google Scholar
     

  • Zhang, X., Lin, H., Wang, X. & Austin, B. Significance of Vibrio species in the marine organic carbon cycle: A review. Sci. China Earth Sci. 61, 1357–1368 (2018).

    Article 
    ADS 
    CAS 

    Google Scholar
     

  • Bassler, B. L., Yu, C., Lee, Y. C. & Roseman, S. Chitin utilization by marine bacteria: Degradation and catabolism of chitin oligosaccharides by Vibrio furnissii. J. Biol. Chem. 266, 24276–24286 (1991).

    Article 
    CAS 
    PubMed 

    Google Scholar
     

  • Suginta, W., Robertson, P. A. W., Austin, B., Fry, S. C. & Fothergill-Gilmore, L. A. Chitinases from Vibrio: Activity screening and purification of chiA from Vibrio carchariae. J. Appl. Microbiol. 89, 76–84 (2000).

    Article 
    CAS 
    PubMed 

    Google Scholar
     

  • Suginta, W. et al. An endochitinase A from Vibrio carchariae: Cloning, expression, mass and sequence analyses, and chitin hydrolysis. Arch. Biochem. Biophys. 424, 171–180 (2004).

    Article 
    CAS 
    PubMed 

    Google Scholar
     

  • Keyhani, N. O., Li, X. B. & Roseman, S. Chitin catabolism in the marine bacterium Vibrio furnissii. Identification and molecular cloning of a chitoporin. J. Biol. Chem. 275, 33068–33076 (2000).

    Article 
    CAS 
    PubMed 

    Google Scholar
     

  • Suginta, W. et al. Molecular uptake of chitooligosaccharides through chitoporin from the marine bacterium Vibrio harveyi. PLoS ONE. 8, e55126 (2013).

    Article 
    ADS 
    CAS 
    PubMed 
    PubMed Central 

    Google Scholar
     

  • Suginta, W., Chumjan, W., Mahendran, K. R., Schulte, A. & Winterhalter, M. Chitoporin from Vibrio harveyi, a channel with exceptional sugar specificity. J. Biol. Chem. 288, 11038–11046 (2013).

    Article 
    CAS 
    PubMed 
    PubMed Central 

    Google Scholar
     

  • Aunkham, A. et al. Structural basis for chitin acquisition by marine Vibrio species. Nat. Commun. 9, 220 (2018).

    Article 
    ADS 
    PubMed 
    PubMed Central 

    Google Scholar
     

  • Keyhani, N. O. & Roseman, S. The chitin catabolic cascade in the marine bacterium Vibrio furnissii. Molecular cloning, isolation, and characterization of a periplasmic chitodextrinase. J. Biol. Chem. 271, 33414–33424 (1996).

    Article 
    CAS 
    PubMed 

    Google Scholar
     

  • Keyhani, N. O. & Roseman, S. The chitin catabolic cascade in the marine bacterium Vibrio furnissii. Molecular cloning, isolation, and characterization of a periplasmic b-N-acetylglucosaminidase. J. Biol. Chem. 27, 33425–33432 (1996).

    Article 

    Google Scholar
     

  • Suginta, W., Chuenark, D., Mizuhara, M. & Fukamizo, T. Novel β-N-acetylglucosaminidases from Vibrio harveyi 650: Cloning, expression, enzymatic properties, and subsite identification. BMC Biochem. 11, 40 (2010).

    Article 
    PubMed 
    PubMed Central 

    Google Scholar
     

  • Keyhani, N. O., Wang, L. X., Lee, Y. C. & Roseman, S. The chitin catabolic cascade in the marine bacterium Vibrio furnissii. Characterization of an N, N’-diacetyl chitobiose transport system. J. Biol. Chem. 271, 33409–33413 (1996).

    Article 
    CAS 
    PubMed 

    Google Scholar
     

  • Chandravanshi, M., Tripathi, S. K. & Kanaujia, S. P. An updated classification and mechanistic insights into ligand binding of the substrate-binding proteins. FEBS Lett. 595, 2395–2409 (2021).

    Article 
    CAS 
    PubMed 

    Google Scholar
     

  • Ortega, Á., Matilla, M. A. & Krell, T. The repertoire of solute-binding proteins of model bacteria reveals large differences in number, type, and ligand range. Microbiol. Spectr. 10, e0205422 (2022).

    Article 
    PubMed 

    Google Scholar
     

  • Li, X. & Roseman, S. The chitinolytic cascade in Vibrios is regulated by chitin oligosaccharides and a two-component chitin catabolic sensor/kinase. Proc. Natl. Acad. Sci. USA. 101, 627–631 (2004).

    Article 
    ADS 
    CAS 
    PubMed 

    Google Scholar
     

  • Klancher, C. A., Yamamoto, S., Dalia, T. N. & Dalia, A. B. ChiS is a noncanonical DNA-binding hybrid sensor kinase that directly regulates the chitin utilization program in Vibrio cholerae. Proc. Natl. Acad. Sci. USA. 117, 20180–20189 (2020).

    Article 
    ADS 
    CAS 
    PubMed 
    PubMed Central 

    Google Scholar
     

  • Scheepers, G. H., Lycklama, J. A. & Poolman, B. An updated structural classification of substrate-binding proteins. FEBS Lett. 590, 4393–4401 (2016).

    Article 
    CAS 
    PubMed 

    Google Scholar
     

  • Fukamizo, T., Kitaoku, Y. & Suginta, W. Periplasmic solute-binding proteins: Structure classification and chitooligosaccharide recognition. Int. J. Biol. Macromol. 128, 985–993 (2019).

    Article 
    CAS 
    PubMed 

    Google Scholar
     

  • Shears, P. Cholera. Ann. Trop. Med. Parasitol. 88, 109–122 (1994).

    Article 
    CAS 
    PubMed 

    Google Scholar
     

  • Austin, B. & Zhang, X. H. Vibrio harveyi: A significant pathogen of marine vertebrates and invertebrates. Lett. Appl. Microbiol. 43, 119–214 (2006).

    Article 
    CAS 
    PubMed 

    Google Scholar
     

  • Chekan, J. R. et al. Structural and biochemical basis for mannan utilization by Caldanaerobius polysaccharolyticus strain ATCC BAA-17. J. Biol. Chem. 289, 34965–34977 (2014).

    Article 
    PubMed 
    PubMed Central 

    Google Scholar
     

  • Cuneo, M. J., Beese, L. S. & Hellinga, H. W. Structural analysis of semi-specific oligosaccharide recognition by a cellulose-binding protein of Thermotoga maritima reveals adaptations for functional diversification of the oligopeptide periplasmic binding protein fold. J. Biol. Chem. 284, 33217–33223 (2009).

    Article 
    CAS 
    PubMed 
    PubMed Central 

    Google Scholar
     

  • Suginta, W. et al. Structure and function of a novel periplasmic chitooligosaccharide-binding protein from marine Vibrio bacteria. J. Biol. Chem. 293, 5150–5159 (2018).

    Article 
    CAS 
    PubMed 
    PubMed Central 

    Google Scholar
     

  • Kitaoku, Y. et al. A structural model for (GlcNAc)2 translocation via a periplasmic chitooligosaccharide-binding protein from marine Vibrio bacteria. J. Biol. Chem. 297, 101071 (2021).

    Article 
    CAS 
    PubMed 
    PubMed Central 

    Google Scholar
     

  • Chaudhuri, B. N., Ko, J., Park, C., Jones, T. A. & Mowbray, S. L. Structure of D-allose binding protein from Escherichia coli bound to D-allose at 1.8 A resolution. J. Mol. Biol. 286, 1519–1531 (1999).

    Article 
    CAS 
    PubMed 

    Google Scholar
     

  • Borrok, M. J., Kiessling, L. L. & Forest, K. T. Conformational changes of glucose/galactose-binding protein illuminated by open, unliganded, and ultra-high-resolution ligand-bound structures. Protein Sci. 16, 1032–1041 (2007).

    Article 
    CAS 
    PubMed 
    PubMed Central 

    Google Scholar
     

  • Anamizu, K. et al. Substrate size-dependent conformational changes of bacterial pectin-binding protein crucial for chemotaxis and assimilation. Sci. Rep. 12, 12653 (2022).

    Article 
    ADS 
    CAS 
    PubMed 
    PubMed Central 

    Google Scholar
     

  • Pace, C. N. & McGrath, T. Substrate stabilization of lysozyme to thermal and guanidine hydrochloride denaturation. J. Biol. Chem. 255, 3862–3865 (1980).

    Article 
    CAS 
    PubMed 

    Google Scholar
     

  • Zolotnitsky, G. et al. Mapping glycoside hydrolase substrate subsites by isothermal titration calorimetry. Proc. Natl. Acad. Sci. USA. 101, 11275–11280 (2004).

    Article 
    ADS 
    CAS 
    PubMed 
    PubMed Central 

    Google Scholar
     

  • Fraczkiewicz, R. & Braun, W. Exact and efficient analytical calculation of the accessible surface areas and their gradients for macromolecules. J. Comput. Chem. 19, 319–333 (1998).

    Article 
    CAS 

    Google Scholar
     

  • Rupley, J. A. The hydrolysis of chitin by concentrated hydrochloric acid, and the preparation of low-molecular weight substrates for lysozyme. Biochim. Biophys. Acta 83, 245–255 (1964).

    CAS 
    PubMed 

    Google Scholar
     

  • Laemmli, U. K. Cleavage of structural proteins during the assembly of the head of bacteriophage T4. Nature 227, 680–685 (1970).

    Article 
    ADS 
    CAS 
    PubMed 

    Google Scholar
     

  • Pace, C. N., Vajdos, F., Fee, L., Grimsley, G. & Gray, T. How to measure and predict the molar absorption coefficient of a protein. Protein Sci. 4, 2411–2423 (1995).

    Article 
    CAS 
    PubMed 
    PubMed Central 

    Google Scholar
     

  • Honda, Y., Fukamizo, T., Boucher, I. & Brzezinski, R. Substrate binding to the inactive mutants of Streptomyces sp. N174 chitosanase: indirect evaluation from the thermal unfolding experiments. FEBS Lett. 411, 346–350 (1997).

    Article 
    CAS 
    PubMed 

    Google Scholar
     

  • Turnbull, W. B. & Daranas, A. H. On the value of c: Can low affinity systems be studied by isothermal titration calorimetry?. J. Am. Chem. Soc. 125, 14859–14866 (2003).

    Article 
    CAS 
    PubMed 

    Google Scholar
     

  • Ohnuma, T. et al. Chitin oligosaccharide binding to a family GH19 chitinase from the moss Bryum coronatum. FEBS J. 278, 3991–4001 (2011).

    Article 
    CAS 
    PubMed 

    Google Scholar
     

  • Kabsch, W. XDS. Acta Crystallogr. D 66, 125–132 (2010).

    Article 
    ADS 
    CAS 
    PubMed 
    PubMed Central 

    Google Scholar
     

  • McCoy, A. J. et al. Phaser crystallographic software. J. Appl. Crystallogr. 40, 658–674 (2007).

    Article 
    ADS 
    CAS 
    PubMed 
    PubMed Central 

    Google Scholar
     

  • Afonine, P. V. et al. Towards automated crystallographic structure refinement with phenix.refine. Acta Crystallogr. D. 68, 352–367 (2012).

    Article 
    ADS 
    CAS 
    PubMed 
    PubMed Central 

    Google Scholar
     

  • Emsley, P. & Cowtan, K. Coot: Model-building tools for molecular graphics. Acta Crystallogr. D. 60, 2126–2132 (2004).

    Article 
    ADS 
    PubMed 

    Google Scholar
     

  • Williams, C. J. et al. MolProbity: More and better reference data for improved all-atom structure validation. Protein Sci. 27, 293–315 (2018).

    Article 
    CAS 
    PubMed 

    Google Scholar
     

  • van Der Spoel, D. et al. GROMACS: Fast, flexible, and free. J. Comput. Chem. 26, 1701–1718 (2005).

    Article 
    PubMed 

    Google Scholar
     

  • Lindorff-Larsen, K. et al. Improved side-chain torsion potentials for the Amber ff99SB protein force field. Proteins 78, 1950–1958 (2010).

    Article 
    CAS 
    PubMed 
    PubMed Central 

    Google Scholar
     

  • Sousa Da Silva, A. W. & Vrancen, W. F. ACPYPE: AnteChamber PYthon Parser interfacE. BMC Res. Not. 5, 367 (2012).

    Article 

    Google Scholar
     

  • Jakalian, A., Jack, D. B. & Bayly, C. I. Fast, efficient generation of high-quality atomic charges. AM1-BCC model: II Parameterization and validation. J. Comput. Chem. 23, 1623–1641 (2002).

    Article 
    CAS 
    PubMed 

    Google Scholar
     

  • Jorgensen, W. L., Chandrasekhar, J., Madura, J. D., Impey, R. W. & Klein, M. L. Comparison of simple potential functions for simulating liquid water. J. Chem. Phys. 79, 926–935 (1983).

    Article 
    ADS 
    CAS 

    Google Scholar
     

  • Berendsen, H. J. C., Postma, J. P. M., DiNola, A. & Haak, J. R. Molecular dynamics with coupling to an external bath. J. Chem. Phys. 81, 3684–3690 (1984).

    Article 
    ADS 
    CAS 

    Google Scholar
     

  • Bussi, G., Donadio, D. & Parrinello, M. Canonical sampling through velocity rescaling. J. Chem. Phys. 126, 014101 (2007).

    Article 
    ADS 
    PubMed 

    Google Scholar
     

  • Parrinello, M. & Rahman, A. Polymorphic transitions in single crystals: A new molecular dynamics method. J. Appl. Phys. 52, 7182–7190 (1981).

    Article 
    ADS 
    CAS 

    Google Scholar
     

  • Amadei, A., Linssen, A. B. M. & Berendsen, H. J. C. Essential dynamics of proteins. Proteins. 17, 412–425 (1993).

    Article 
    CAS 
    PubMed 

    Google Scholar
     

  • Bakan, A., Meireles, L. M. & Bahar, I. ProDy: Protein dynamics inferred from theory and experiments. Bioinformatics 27, 1575–1577 (2011).

    Article 
    CAS 
    PubMed 
    PubMed Central 

    Google Scholar
     

  • Humphrey, W., Dalke, A. & Schulten, K. VMD: Visual molecular dynamics. J. Mol. Graph. 14, 33–38 (1996).

    Article 
    CAS 
    PubMed 

    Google Scholar
     

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