Polysaccharide degradation systems of the saprophytic bacterium Cellvibrio japonicus

REVIEW

Abstract

Study of recalcitrant polysaccharide degradation by bacterial systems is critical for understanding biological processes such as global carbon cycling, nutritional contributions of the human gut microbiome, and the production of renewable fuels and chemicals. One bacterium that has a robust ability to degrade polysaccharides is the Gram-negative saprophyte Cellvibrio japonicus. A bacterium with a circuitous history, C. japonicus underwent several taxonomy changes from an initially described Pseudomonas sp. Most of the enzymes described in the pre-genomics era have also been renamed. This review aims to consolidate the biochemical, structural, and genetic data published on C. japonicus and its remarkable ability to degrade cellulose, xylan, and pectin substrates. Initially, C. japonicus carbohydrate-active enzymes were studied biochemically and structurally for their novel polysaccharide binding and degradation characteristics, while more recent systems biology approaches have begun to unravel the complex regulation required for lignocellulose degradation in an environmental context. Also included is a discussion for the future of C. japonicus as a model system, with emphasis on current areas unexplored in terms of polysaccharide degradation and emerging directions for C. japonicus in both environmental and biotechnological applications.

Keywords

Carbohydrate active enzyme Cellvibrio japonicus Lignocellulose Polysaccharide degradation Saprophyte 

References

  1. Adams EL, Kroon PA, Williamson G, Gilbert HJ, Morris VJ (2004) Inactivated enzymes as probes of the structure of arabinoxylans as observed by atomic force microscopy. Carbohydr Res 339:579–590. doi:10.1016/j.carres.2003.11.023 CrossRefGoogle Scholar
  2. Andrews SR et al (2004) The use of forced protein evolution to investigate and improve stability of family 10 xylanases. The production of Ca2+-independent stable xylanases. J Biol Chem 279:54369–54379. doi:10.1074/jbc.M409044200 CrossRefGoogle Scholar
  3. Attia M, Stepper J, Davies GJ, Brumer H (2016) Functional and structural characterization of a potent GH74 endo-xyloglucanase from the soil saprophyte Cellvibrio japonicus unravels the first step of xyloglucan degradation. FEBS J. doi:10.1111/febs.13696 Google Scholar
  4. Bartolome B, Faulds CB, Kroon PA, Waldron K, Gilbert HJ, Hazlewood G, Williamson G (1997) An Aspergillus niger esterase (ferulic acid esterase III) and a recombinant Pseudomonas fluorescens subsp. cellulosa esterase (Xy1D) release a 5-5′ferulic dehydrodimer (diferulic acid) from barley and wheat cell walls. Appl Environ Microbiol 63:208–212Google Scholar
  5. Beylot MH, Emami K, McKie VA, Gilbert HJ, Pell G (2001a) Pseudomonas cellulosa expresses a single membrane-bound glycoside hydrolase family 51 arabinofuranosidase. Biochem J 358:599–605CrossRefGoogle Scholar
  6. Beylot MH, McKie VA, Voragen AG, Doeswijk-Voragen CH, Gilbert HJ (2001b) The Pseudomonas cellulosa glycoside hydrolase family 51 arabinofuranosidase exhibits wide substrate specificity. Biochem J 358:607–614CrossRefGoogle Scholar
  7. Bokinsky G et al (2011) Synthesis of three advanced biofuels from ionic liquid-pretreated switchgrass using engineered Escherichia coli. Proc Natl Acad Sci USA 108:19949–19954CrossRefGoogle Scholar
  8. Bolam DN et al (1996) Mannanase A from Pseudomonas fluorescens ssp. cellulosa is a retaining glycosyl hydrolase in which E212 and E320 are the putative catalytic residues. Biochemistry 35:16195–16204. doi:10.1021/bi961866d CrossRefGoogle Scholar
  9. Boraston AB, Bolam DN, Gilbert HJ, Davies GJ (2004) Carbohydrate-binding modules: fine-tuning polysaccharide recognition. Biochem J 382:769–781CrossRefGoogle Scholar
  10. Braithwaite KL, Black GW, Hazlewood GP, Ali BR, Gilbert HJ (1995) A non-modular endo-beta-1,4-mannanase from Pseudomonas fluorescens subspecies cellulosa. Biochem J 305:1005–1010CrossRefGoogle Scholar
  11. Braithwaite KL et al (1997) Evidence that galactanase A from Pseudomonas fluorescens subspecies cellulosa is a retaining family 53 glycosyl hydrolase in which E161 and E270 are the catalytic residues. Biochemistry 36:15489–15500CrossRefGoogle Scholar
  12. Brown IE, Mallen MH, Charnock SJ, Davies GJ, Black GW (2001) Pectate lyase 10A from Pseudomonas cellulosa is a modular enzyme containing a family 2a carbohydrate-binding module. Biochem J 355:155–165CrossRefGoogle Scholar
  13. Cantarel BL, Coutinho PM, Rancurel C, Bernard T, Lombard V, Henrissat B (2009) The Carbohydrate-Active EnZymes database (CAZy): an expert resource for glycogenomics. Nucleic Acids Res 37:233–238CrossRefGoogle Scholar
  14. Cartmell A, Topakas E, Ducros VM, Suits MD, Davies GJ, Gilbert HJ (2008) The Cellvibrio japonicus mannanase CjMan26C displays a unique exo-mode of action that is conferred by subtle changes to the distal region of the active site. J Biol Chem 283:34403–34413CrossRefGoogle Scholar
  15. Cartmell A et al (2011) The structure and function of an arabinan-specific alpha-1,2-arabinofuranosidase identified from screening the activities of bacterial GH43 glycoside hydrolases. J Biol Chem 286:15483–15495CrossRefGoogle Scholar
  16. Charnock SJ et al (1997) Key residues in subsite F play a critical role in the activity of Pseudomonas fluorescens subspecies cellulosa xylanase A against xylooligosaccharides but not against highly polymeric substrates such as xylan. J Biol Chem 272:2942–2951CrossRefGoogle Scholar
  17. Charnock SJ, Brown IE, Turkenburg JP, Black GW, Davies GJ (2001) Characterization of a novel pectate lyase, Pel10A, from Pseudomonas cellulosa. Acta Crystallogr D Biol Crystallogr 57:1141–1143CrossRefGoogle Scholar
  18. Cohen-Kupiec R, Chet I (1998) The molecular biology of chitin digestion. Curr Opin Biotechnol 9:270–277CrossRefGoogle Scholar
  19. DeBoy RT et al (2008) Insights into plant cell wall degradation from the genome sequence of the soil bacterium Cellvibrio japonicus. J Bacteriol 190:5455–5463CrossRefGoogle Scholar
  20. Dees C, Ringelberg D, Scott TC, Phelps TJ (1995) Characterization of the cellulose degrading bacterium NCIMB 20462. Appl Biochem Biotechnol 51:263–274CrossRefGoogle Scholar
  21. Emami K, Nagy T, Fontes CM, Ferreira LM, Gilbert HJ (2002) Evidence for temporal regulation of the two Pseudomonas cellulosa xylanases belonging to glycoside hydrolase family 11. J Bacteriol 184:4124–4133CrossRefGoogle Scholar
  22. Emami K et al (2009) Regulation of the xylan-degrading apparatus of Cellvibrio japonicus by a novel two-component system. J Biol Chem 284:1086–1096CrossRefGoogle Scholar
  23. Faulds CB, Ralet MC, Williamson G, Hazlewood GP, Gilbert HJ (1995) Specificity of an esterase (XYLD) from Pseudomonas fluorescens subsp. cellulosa. Biochim Biophys Acta 1243:265–269CrossRefGoogle Scholar
  24. Ferreira LM, Durrant AJ, Hall J, Hazlewood GP, Gilbert HJ (1990) Spatial separation of protein domains is not necessary for catalytic activity or substrate binding in a xylanase. Biochem J 269:261–264CrossRefGoogle Scholar
  25. Ferreira LM, Hazlewood GP, Barker PJ, Gilbert HJ (1991) The cellodextrinase from Pseudomonas fluorescens subsp. cellulosa consists of multiple functional domains. Biochem J 279(Pt 3):793–799CrossRefGoogle Scholar
  26. Ferreira LM, Wood TM, Williamson G, Faulds C, Hazlewood GP, Black GW, Gilbert HJ (1993) A modular esterase from Pseudomonas fluorescens subsp. cellulosa contains a non-catalytic cellulose-binding domain. Biochem J 294:349–355CrossRefGoogle Scholar
  27. Fontes CM, Hall J, Hirst BH, Hazlewood GP, Gilbert HJ (1995) The resistance of cellulases and xylanases to proteolytic inactivation. Appl Microbiol Biotechnol 43:52–57CrossRefGoogle Scholar
  28. Fontes CM et al (2000) A novel Cellvibrio mixtus family 10 xylanase that is both intracellular and expressed under non-inducing conditions. Microbiology 146:1959–1967CrossRefGoogle Scholar
  29. Forsberg Z et al (2016) Structural and functional analysis of a lytic polysaccharide monooxygenase important for efficient utilization of chitin in Cellvibrio japonicus. J Biol Chem. doi:10.1074/jbc.M115.700161 Google Scholar
  30. Gardner JG, Keating DH (2010) Requirement of the type II secretion system for utilization of cellulosic substrates by Cellvibrio japonicus. Appl Environ Microbiol 76:5079–5087CrossRefGoogle Scholar
  31. Gardner JG et al (2014) Systems biology defines the biological significance of redox-active proteins during cellulose degradation in an aerobic bacterium. Mol Microbiol 95(5):418–433Google Scholar
  32. Gilbert HJ, Jenkins G, Sullivan DA, Hall J (1987) Evidence for multiple carboxymethylcellulase genes in Pseudomonas fluorescens subsp. cellulosa. Mol Gen Genet 210:551–556CrossRefGoogle Scholar
  33. Gilbert HJ, Sullivan DA, Jenkins G, Kellett LE, Minton NP, Hall J (1988) Molecular cloning of multiple xylanase genes from Pseudomonas fluorescens subsp. cellulosa. J Gen Microbiol 134:3239–3247Google Scholar
  34. Gilbert HJ, Hall J, Hazlewood GP, Ferreira LM (1990) The N-terminal region of an endoglucanase from Pseudomonas fluorescens subspecies cellulosa constitutes a cellulose-binding domain that is distinct from the catalytic centre. Mol Microbiol 4:759–767CrossRefGoogle Scholar
  35. Gilbert HJ, Knox JP, Boraston AB (2013) Advances in understanding the molecular basis of plant cell wall polysaccharide recognition by carbohydrate-binding modules. Curr Opin Struct Biol 23:669–677CrossRefGoogle Scholar
  36. Gill J et al (1999) The type II and X cellulose-binding domains of Pseudomonas xylanase A potentiate catalytic activity against complex substrates by a common mechanism. Biochem J 342:473–480CrossRefGoogle Scholar
  37. Hall J, Gilbert HJ (1988) The nucleotide sequence of a carboxymethylcellulase gene from Pseudomonas fluorescens subsp. cellulosa. Mol Gen Genet 213:112–117CrossRefGoogle Scholar
  38. Hall J, Hazlewood GP, Huskisson NS, Durrant AJ, Gilbert HJ (1989) Conserved serine-rich sequences in xylanase and cellulase from Pseudomonas fluorescens subspecies cellulosa: internal signal sequence and unusual protein processing. Mol Microbiol 3:1211–1219CrossRefGoogle Scholar
  39. Hall J, Black GW, Ferreira LM, Millward-Sadler SJ, Ali BR, Hazlewood GP, Gilbert HJ (1995) The non-catalytic cellulose-binding domain of a novel cellulase from Pseudomonas fluorescens subsp. cellulosa is important for the efficient hydrolysis of Avicel. Biochem J 309:749–756CrossRefGoogle Scholar
  40. Halstead JR, Fransen MP, Eberhart RY, Park AJ, Gilbert HJ, Hazlewood GP (2000) Alpha-galactosidase A from Pseudomonas fluorescens subsp. cellulosa: cloning, high level expression and its role in galactomannan hydrolysis. FEMS Microbiol Lett 192:197–203Google Scholar
  41. Harris GW et al (1994) Structure of the catalytic core of the family F xylanase from Pseudomonas fluorescens and identification of the xylopentaose-binding sites. Structure 2:1107–1116CrossRefGoogle Scholar
  42. Harris GW, Jenkins JA, Connerton I, Pickersgill RW (1996) Refined crystal structure of the catalytic domain of xylanase A from Pseudomonas fluorescens at 1.8 A resolution. Acta Crystallogr D Biol Crystallogr 52:393–401CrossRefGoogle Scholar
  43. Hazlewood GP, Gilbert HJ (1998) Structure and function analysis of Pseudomonas plant cell wall hydrolases. Prog Nucleic Acid Res Mol Biol 61:211–241CrossRefGoogle Scholar
  44. Hazlewood GP, Laurie JI, Ferreira LM, Gilbert HJ (1992) Pseudomonas fluorescens subsp. cellulosa: an alternative model for bacterial cellulase. J Appl Bacteriol 72:244–251CrossRefGoogle Scholar
  45. Hemsworth GR, Davies GJ, Walton PH (2013) Recent insights into copper-containing lytic polysaccharide mono-oxygenases. Curr Opin Struct Biol 23:660–668CrossRefGoogle Scholar
  46. Hemsworth GR, Johnston EM, Davies GJ, Walton PH (2015) Lytic polysaccharide monooxygenases in biomass conversion. Trends Biotechnol 33:747–761CrossRefGoogle Scholar
  47. Hemsworth GR, Dejean G, Davies GJ, Brumer H (2016) Learning from microbial strategies for polysaccharide degradation. Biochem Soc Trans 44:94–108CrossRefGoogle Scholar
  48. Henrissat B, Teeri TT, Warren RA (1998) A scheme for designating enzymes that hydrolyse the polysaccharides in the cell walls of plants. FEBS Lett 425:352–354CrossRefGoogle Scholar
  49. Hogg D, Woo EJ, Bolam DN, McKie VA, Gilbert HJ, Pickersgill RW (2001) Crystal structure of mannanase 26A from Pseudomonas cellulosa and analysis of residues involved in substrate binding. J Biol Chem 276:31186–31192CrossRefGoogle Scholar
  50. Hogg D, Pell G, Dupree P, Goubet F, Martin-Orue SM, Armand S, Gilbert HJ (2003) The modular architecture of Cellvibrio japonicus mannanases in glycoside hydrolase families 5 and 26 points to differences in their role in mannan degradation. Biochem J 371:1027–1043CrossRefGoogle Scholar
  51. Humphry DR, Black GW, Cummings SP (2003) Reclassification of ‘Pseudomonas fluorescens subsp. cellulosa’ NCIMB 10462 (Ueda et al. 1952) as Cellvibrio japonicus sp. nov. and revival of Cellvibrio vulgaris sp. nov., nom. rev. and Cellvibrio fulvus sp. nov., nom. rev. Int J Syst Evol Microbiol 53:393–400CrossRefGoogle Scholar
  52. Jung SK, Parisutham V, Jeong SH, Lee SK (2012) Heterologous expression of plant cell wall degrading enzymes for effective production of cellulosic biofuels. J Biomed Biotechnol 2012:405842CrossRefGoogle Scholar
  53. Kellett LE, Poole DM, Ferreira LM, Durrant AJ, Hazlewood GP, Gilbert HJ (1990) Xylanase B and an arabinofuranosidase from Pseudomonas fluorescens subsp. cellulosa contain identical cellulose-binding domains and are encoded by adjacent genes. Biochem J 272:369–376CrossRefGoogle Scholar
  54. Larsbrink J, Izumi A, Ibatullin FM, Nakhai A, Gilbert HJ, Davies GJ, Brumer H (2011) Structural and enzymatic characterization of a glycoside hydrolase family 31 alpha-xylosidase from Cellvibrio japonicus involved in xyloglucan saccharification. Biochem J 436:567–580CrossRefGoogle Scholar
  55. Larsbrink J, Izumi A, Hemsworth GR, Davies GJ, Brumer H (2012) Structural enzymology of Cellvibrio japonicus Agd31B protein reveals alpha-transglucosylase activity in glycoside hydrolase family 31. J Biol Chem 287:43288–43299CrossRefGoogle Scholar
  56. Larsbrink J et al (2014a) A discrete genetic locus confers xyloglucan metabolism in select human gut Bacteroidetes. Nature 506:498–502CrossRefGoogle Scholar
  57. Larsbrink J, Thompson AJ, Lundqvist M, Gardner JG, Davies GJ, Brumer H (2014b) A complex gene locus enables xyloglucan utilization in the model saprophyte Cellvibrio japonicus. Mol Microbiol 94:418–433CrossRefGoogle Scholar
  58. Leggio LL, Jenkins J, Harris GW, Pickersgill RW (2000) X-ray crystallographic study of xylopentaose binding to Pseudomonas fluorescens xylanase A. Proteins 41:362–373CrossRefGoogle Scholar
  59. Lejeune A, Courtois S, Colson C (1988a) Characterization of an endoglucanase from Pseudomonas fluorescens subsp. cellulosa produced in Escherichia coli and regulation of the expression of its cloned gene. Appl Environ Microbiol 54:302–308Google Scholar
  60. Lejeune A, Dartois V, Colson C (1988b) Characterization and expression in Escherichia coli of an endoglucanase gene of Pseudomonas fluorescens subsp. cellulosa. Biochim Biophys Acta 950:204–214CrossRefGoogle Scholar
  61. Lejeune A, Eveleigh DE, Colson C (1988c) Expression of an endoglucanse gene of Pseudomonas fluorescens var. cellulosa in Zymomonas mobilis. FEMS Microbiol Lett 49:363–366CrossRefGoogle Scholar
  62. Levasseur A, Drula E, Lombard V, Coutinho PM, Henrissat B (2013) Expansion of the enzymatic repertoire of the CAZy database to integrate auxiliary redox enzymes. Biotechnol Biofuels 6:41. doi:10.1186/1754-6834-6-41 CrossRefGoogle Scholar
  63. Lombard V, Bernard T, Rancurel C, Brumer H, Coutinho PM, Henrissat B (2010) A hierarchical classification of polysaccharide lyases for glycogenomics. Biochem J 432:437–444CrossRefGoogle Scholar
  64. Lombard V, Golaconda Ramulu H, Drula E, Coutinho PM, Henrissat B (2014) The carbohydrate-active enzymes database (CAZy) in 2013. Nucleic Acids Res 42:490–495CrossRefGoogle Scholar
  65. Lynd LR, Weimer PJ, van Zyl WH, Pretorius IS (2002) Microbial cellulose utilization: fundamentals and biotechnology. Microbiol Mol Biol Rev 66:506–577CrossRefGoogle Scholar
  66. McClendon SD, Shin HD, Chen RR (2011) Novel bacterial ferulic acid esterase from Cellvibrio japonicus and its application in ferulic acid release and xylan hydrolysis. Biotechnol Lett 33:47–54CrossRefGoogle Scholar
  67. McKie VA, Black GW, Millward-Sadler SJ, Hazlewood GP, Laurie JI, Gilbert HJ (1997) Arabinanase A from Pseudomonas fluorescens subsp. cellulosa exhibits both an endo- and an exo-mode of action. Biochem J 323:547–555CrossRefGoogle Scholar
  68. McKie VA, Vincken JP, Voragen AG, van den Broek LA, Stimson E, Gilbert HJ (2001) A new family of rhamnogalacturonan lyases contains an enzyme that binds to cellulose. Biochem J 355:167–177CrossRefGoogle Scholar
  69. Mewis K, Lenfant N, Lombard V, Henrissat B (2016) Dividing the large glycoside hydrolase family 43 into subfamilies: a motivation for detailed enzyme characterization. Appl Environ Microbiol. doi:10.1128/AEM.03453-15 Google Scholar
  70. Millward-Sadler SJ, Davidson K, Hazlewood GP, Black GW, Gilbert HJ, Clarke JH (1995) Novel cellulose-binding domains, NodB homologues and conserved modular architecture in xylanases from the aerobic soil bacteria Pseudomonas fluorescens subsp. cellulosa and Cellvibrio mixtus. Biochem J 312:39–48CrossRefGoogle Scholar
  71. Mohnen D (2008) Pectin structure and biosynthesis. Curr Opin Plant Biol 11:266–277CrossRefGoogle Scholar
  72. Montanier C et al (2009) The active site of a carbohydrate esterase displays divergent catalytic and noncatalytic binding functions. PLoS Biol 7:e71. doi:10.1371/journal.pbio.1000071 CrossRefGoogle Scholar
  73. Nagy T, Emami K, Fontes CM, Ferreira LM, Humphry DR, Gilbert HJ (2002) The membrane-bound alpha-glucuronidase from Pseudomonas cellulosa hydrolyzes 4-O-methyl-d-glucuronoxylooligosaccharides but not 4-O-methyl-d-glucuronoxylan. J Bacteriol 184:4925–4929CrossRefGoogle Scholar
  74. Nagy T, Nurizzo D, Davies GJ, Biely P, Lakey JH, Bolam DN, Gilbert HJ (2003) The alpha-glucuronidase, GlcA67A, of Cellvibrio japonicus utilizes the carboxylate and methyl groups of aldobiouronic acid as important substrate recognition determinants. J Biol Chem 278:20286–20292CrossRefGoogle Scholar
  75. Nelson CE, Gardner JG (2015) In-frame deletions allow functional characterization of complex cellulose degradation phenotypes in Cellvibrio japonicus. Appl Environ Microbiol 81(17):5968–5975CrossRefGoogle Scholar
  76. Nurizzo D, Nagy T, Gilbert HJ, Davies GJ (2002a) The structural basis for catalysis and specificity of the Pseudomonas cellulosa alpha-glucuronidase GlcA67A. Structure 10:547–556CrossRefGoogle Scholar
  77. Nurizzo D et al (2002b) Cellvibrio japonicus alpha-l-arabinanase 43A has a novel five-blade beta-propeller fold. Nat Struct Biol 9:665–668CrossRefGoogle Scholar
  78. Pauly M, Keegstra K (2008) Cell-wall carbohydrates and their modification as a resource for biofuels. Plant J Cell Mol Biol 54:559–568CrossRefGoogle Scholar
  79. Pell G, Williamson MP, Walters C, Du H, Gilbert HJ, Bolam DN (2003) Importance of hydrophobic and polar residues in ligand binding in the family 15 carbohydrate-binding module from Cellvibrio japonicus Xyn10C. Biochemistry 42:9316–9323CrossRefGoogle Scholar
  80. Pell G, Szabo L, Charnock SJ, Xie H, Gloster TM, Davies GJ, Gilbert HJ (2004) Structural and biochemical analysis of Cellvibrio japonicus xylanase 10C: how variation in substrate-binding cleft influences the catalytic profile of family GH-10 xylanases. J Biol Chem 279:11777–11788CrossRefGoogle Scholar
  81. Pickersgill RW, Jenkins JA, Scott M, Connerton I, Hazlewood GP, Gilbert HJ (1993) Crystallization and preliminary X-ray analysis of the catalytic domain of xylanase a from Pseudomonas fluorescens subspecies cellulosa. J Mol Biol 229:246–248CrossRefGoogle Scholar
  82. Proctor MR et al (2005) Tailored catalysts for plant cell-wall degradation: redesigning the exo/endo preference of Cellvibrio japonicus arabinanase 43A. Proc Natl Acad Sci USA 102:2697–2702CrossRefGoogle Scholar
  83. Raghothama S, Simpson PJ, Szabo L, Nagy T, Gilbert HJ, Williamson MP (2000) Solution structure of the CBM10 cellulose binding module from Pseudomonas xylanase A. Biochemistry 39:978–984CrossRefGoogle Scholar
  84. Rixon JE, Ferreira LM, Durrant AJ, Laurie JI, Hazlewood GP, Gilbert HJ (1992) Characterization of the gene celD and its encoded product 1,4-beta-d-glucan glucohydrolase D from Pseudomonas fluorescens subsp. cellulosa. Biochem J 285:947–955CrossRefGoogle Scholar
  85. Scheller HV, Ulvskov P (2010) Hemicelluloses. Annu Rev Plant Biol 61:263–289CrossRefGoogle Scholar
  86. Scott M, Pickersgill RW, Hazlewood GP, Bolam D, Gilbert HJ, Harris GW (1998) Crystallization and preliminary X-ray diffraction studies of a family 26 endo-beta-1,4 mannanase (ManA) from Pseudomonas fluorescens subspecies cellulosa. Acta Crystallogr D Biol Crystallogr 54:129–131CrossRefGoogle Scholar
  87. Scott M, Pickersgill RW, Hazlewood GP, Gilbert HJ, Harris GW (1999) Crystallization and preliminary X-ray analysis of arabinanase A from Pseudomonas fluorescens subspecies cellulosa. Acta Crystallogr D Biol Crystallogr 55:544–546CrossRefGoogle Scholar
  88. Silipo A, Larsbrink J, Marchetti R, Lanzetta R, Brumer H, Molinaro A (2012) NMR spectroscopic analysis reveals extensive binding interactions of complex xyloglucan oligosaccharides with the Cellvibrio japonicus glycoside hydrolase family 31 alpha-xylosidase. Chemistry 18:13395–13404CrossRefGoogle Scholar
  89. Stitt M, Zeeman SC (2012) Starch turnover: pathways, regulation and role in growth. Curr Opin Plant Biol 15:282–292CrossRefGoogle Scholar
  90. Topakas E, Kyriakopoulos S, Biely P, Hirsch J, Vafiadi C, Christakopoulos P (2010) Carbohydrate esterases of family 2 are 6-O-deacetylases. FEBS Lett 584:543–548CrossRefGoogle Scholar
  91. Tunnicliffe RB, Bolam DN, Pell G, Gilbert HJ, Williamson MP (2005) Structure of a mannan-specific family 35 carbohydrate-binding module: evidence for significant conformational changes upon ligand binding. J Mol Biol 347:287–296CrossRefGoogle Scholar
  92. Tuomivaara ST, Yaoi K, O’Neill MA, York WS (2015) Generation and structural validation of a library of diverse xyloglucan-derived oligosaccharides, including an update on xyloglucan nomenclature. Carbohydr Res 402:56–66CrossRefGoogle Scholar
  93. Ueda K, Ishikawa S, Itami T, Asai T (1952) Studies on the aerobic mesophilic cellulose-decomposing bacteria. Part 5-2. Taxonomical study on genus Pseudomonas. J Agric Chem Soc 26:35–41Google Scholar
  94. Wolff BR, Mudry TA, Glick BR, Pasternak JJ (1986) Isolation of endoglucanase genes from Pseudomonas fluorescens subsp. cellulosa and a Pseudomonas sp. Appl Environ Microbiol 51:1367–1369Google Scholar
  95. Wolff BR, Glick BR, Pasternak JJ (1990) DNA sequence analysis of endoglucanase genes from Pseudomonas fluorescens subsp. cellulosa and Pseudomonas sp. NCIB 8634. J Ind Microbiol 6:285–290CrossRefGoogle Scholar
  96. Yamane K, Suzuki H, Hirotani M, Ozawa H, Nisizawa K (1970a) Effect of nature and supply of carbon sources on cellulase formation in Pseudomonas fluorescens var. cellulosa. J Biochem 67:9–18Google Scholar
  97. Yamane K, Suzuki H, Nisizawa K (1970b) Purification and properties of extracellular and cell-bound cellulase components of Pseudomonas fluorescens var. cellulosa. J Biochem 67:19–35Google Scholar
  98. Yamane K, Yoshikawa T, Suzuki H, Nisizawa K (1971) Localization of cellulase components in Pseudomonas fluorescens var. cellulosa. J Biochem 69:771–780Google Scholar
  99. Yoshikawa T, Suzuki H, Nisizawa K (1974) Biogenesis of multiple cellulase components of Pseudomonas fluorescens var. cellulosa. I. Effects of culture conditions on the multiplicity of cellulase. J Biochem 75:531–540Google Scholar
  100. Zhang X, Rogowski A, Zhao L, Hahn MG, Avci U, Knox JP, Gilbert HJ (2014) Understanding how the complex molecular architecture of mannan-degrading hydrolases contributes to plant cell wall degradation. J Biol Chem 289:2002–2012CrossRefGoogle Scholar

Copyright information

© Springer Science+Business Media Dordrecht 2016

Authors and Affiliations

  1. 1.Department of Biological SciencesUniversity of Maryland - Baltimore CountyBaltimoreUSA

Personalised recommendations