Engineering the xylan utilization system in Bacillus subtilis for production of acidic xylooligosaccharides

Applied and Environmental Microbiology

Volumn 80, Issue 3, 2014, Pages 917-927

  Rhee, Mun Su ^a   Wei, Lusha ^a   Sawhney, Neha ^a   Rice, John D ^a   St John, Franz J ^b   Hurlbert, Jason C ^c   Preston, James F ^a  

^a UNIVERSITY OF FLORIDA   (United States)

^b FOREST PRODUCTS LABORATORY   (United States)

^c WINTHROP UNIVERSITY   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

AVERAGE DEGREE; BACILLUS SUBTILIS; DEGREES OF POLYMERIZATIONS; GLYCOSIDE HYDROLASES; POTENTIAL SOURCES; UTILIZATION SYSTEMS; XYLOOLIGOSACCHARIDES; XYLOSE RESIDUES;

GENES; POLYSACCHARIDES; VETERINARY MEDICINE;

ORGANIC POLYMERS;

BACTERIUM; BIOLOGICAL PRODUCTION; BIOTECHNOLOGY; FUNCTIONAL ROLE; GENE EXPRESSION; GENETIC ENGINEERING; MEDICINE; POLYMERIZATION; POLYSACCHARIDE; SUGAR;

GLUCURONIC ACID; GLYCOSIDASE; OLIGOSACCHARIDE; XYLAN; XYLAN 1,4 BETA XYLOSIDASE; XYLOOLIGOSACCHARIDE;

ARTICLE; BACILLUS SUBTILIS; ENZYMOLOGY; GENE DELETION; GENETICS; METABOLISM;

BACILLUS SUBTILIS; GENE DELETION; GLUCURONATES; GLYCOSIDE HYDROLASES; OLIGOSACCHARIDES; XYLANS; XYLOSIDASES;

EID: 84892955892     PISSN: 00992240     EISSN: 10985336     Source Type: Journal    
DOI: 10.1128/AEM.03246-13     Document Type: Article

References (45)

1. Aachary AA, Prapulla SG. 2011. Xylooligosaccharides (XOS) as an emerging prebiotic: microbial synthesis, utilization, structural characterization, bioactive properties, and applications. Compr. Rev. Food Sci. 10: 2-16. http://dx.doi.org/10.1111/j.1541-4337.2010.00135.x.
2. Vazquez MJ, Alonso JL, Dominguez H, Parajo JC. 2000. Xylooligosaccharides: manufacture and applications. Trends Food Sci. Technol. 11: 387-393. http://dx.doi.org/10.1016/S0924-2244(01)00031-0.
3. Otieno DO, Ahring BK. 2012. The potential for oligosaccharide production from the hemicellulose fraction of biomasses through pretreatment processes: xylooligosaccharides (XOS), arabinooligosaccharides (AOS), and mannooligosaccharides (MOS). Carbohydr. Res. 360:84-92. http: //dx.doi.org/10.1016/j.carres.2012.07.017.
4. Chen HH, Chen YK, Chang HC, Lin SY. 2012. Immunomodulatory effects of xylooligosaccharides. Food Sci. Technol. Res. 18:195-199. http: //dx.doi.org/10.3136/fstr.18.195.
5. Ebringerova A, Hromadkova Z. 1999. Xylans of industrial and biomedical importance. Biotechnol. Genet. Eng. Rev. 16:325-346. http://dx.doi .org/10.1080/02648725.1999.10647982.
6. Anderson VR, Perry CM. 2006. Pentosan polysulfate: a review of its use in the relief of bladder pain or discomfort in interstitial cystitis. Drugs 66: 821-835. http://dx.doi.org/10.2165/00003495-200666060-00006.
7. Schuchman EH, Ge Y, Lai A, Borisov Y, Faillace M, Eliyahu E, He XX, Iatridis J, Vlassara H, Striker G, Simonaro CM. 2013. Pentosan polysulfate: a novel therapy for the mucopolysaccharidoses. PLoS One 8:e54459. http://dx.doi.org/10.1371/journal.pone.0054459.
8. Goodrich LR, Nixon AJ. 2006. Medical treatment of osteoarthritis in the horse-a review. Vet. J. 171:51-69. http://dx.doi.org/10.1016/j.tvjl.2004 .07.008.
9. Carpita NC. 1996. Structure and biogenesis of the cell walls of grasses. Annu. Rev. Plant Physiol. Plant Mol. Biol. 47:445-476. http://dx.doi.org /10.1146/annurev.arplant.47.1.445.
10. Ebringerova A, Hromadkova Z, Heinze T. 2005. Hemicellulose. Adv. Polym. Sci. 186:1-67. http://dx.doi.org/10.1007/b136816.
11. Biely P, Vrsanska M, Tenkanen M, Kluepfel D. 1997. Endo-beta-1,4- xylanase families: differences in catalytic properties. J. Biotechnol. 57:151-166. http://dx.doi.org/10.1016/S0168-1656(97)00096-5.
12. Preston JF, Hurlbert JC, Rice JD, Ragunathan A, St. John FJ. 2003. Microbial strategies for the depolymerization of glucuronoxylan: leads to biotechnological applications of endoxylanases. Appl. Enzymes Lignocellulosics 855:191-210. http://dx.doi.org/10.1021/bk-2003-0855.ch012.
13. Collins T, Gerday C, Feller G. 2005. Xylanases, xylanase families and extremophilic xylanases. FEMS Microbiol. Rev. 29:3-23. http://dx.doi.org /10.1016/j.femsre.2004.06.005.
14. St. John FJ, Rice JD, Preston JF. 2006. Paenibacillus sp. strain JDR-2 and XynA1: a novel system for methylglucuronoxylan utilization. Appl. Environ. Microbiol. 72:1496-1506. http://dx.doi.org/10.1128/AEM.72.2.1496 -1506.2006.
15. St. John FJ, Hurlbert JC, Rice J, Preston JF, Pozharski E. 2011. Ligand bound structures of a glycosyl hydrolase family 30 glucuronoxylan xylanohydrolase. J. Mol. Biol. 407:92-109. http://dx.doi.org/10.1016/j.jmb.2011 .01.010.
16. St. John FJ, Rice JD, Preston JF. 2006. Characterization of XynC from Bacillus subtilis subsp. subtilis strain 168 and analysis of its role in depolymerization of glucuronoxylan. J. Bacteriol. 188:8617-8626. http://dx.doi .org/10.1128/JB.01283-06.
17. St. John FJ, Gonzalez JM, Pozharski E. 2010. Consolidation of glycosyl hydrolase family 30: a dual domain 4/7 hydrolase family consisting of two structurally distinct groups. FEBS Lett. 584:4435-4441. http://dx.doi.org /10.1016/j.febslet.2010.09.051.
18. Tjalsma H, Antelmann H, Jongbloed JDH, Braun PG, Darmon E, Dorenbos R, Dubois JYF, Westers H, Zanen G, Quax WJ, Kuipers OP, Bron S, Hecker M, van Dijl JM. 2004. Proteomics of protein secretion by Bacillus subtilis: separating the "secrets" of the secretome. Microbiol. Mol. Biol. Rev. 68:207-233. http://dx.doi.org/10.1128/MMBR .68.2.207-233.2004.
19. Ay J, Gotz F, Borriss R, Heinemann U. 1998. Structure and function of the Bacillus hybrid enzyme GluXyn-1: native-like jellyroll fold preserved after insertion of autonomous globular domain. Proc. Natl. Acad. Sci. U. S. A. 95:6613-6618. http://dx.doi.org/10.1073/pnas.95.12.6613.
20. Vandermarliere E, Bourgois TM, Rombouts S, Van Campenhout S, Volckaert G, Strelkov SV, Delcour JA, Rabijns A, Courtin CM. 2008. Crystallographic analysis shows substrate binding at the -3 to 1 active-site subsites and at the surface of glycoside hydrolase family11endo-1,4-beta-xylanases.Biochem.J. 410: 71-79. http://dx.doi.org/10.1042/BJ20071128.
21. Schallmey M, Singh A, Ward OP. 2004. Developments in the use of Bacillus species for industrial production. Can. J. Microbiol. 50:1-17. http: //dx.doi.org/10.1139/w03-076.
22. Pohl S, Harwood CR. 2010. Heterologous protein secretion by Bacillus species: from the cradle to the grave. Adv. Appl. Microbiol. 73:1-25. http: //dx.doi.org/10.1016/S0065-2164(10)73001-X.
23. Spizizen J. 1958. Transformation of biochemically deficient strains of Bacillus subtilis by deoxyribonucleate. Proc. Natl. Acad. Sci. U. S. A. 44: 1072-1078. http://dx.doi.org/10.1073/pnas.44.10.1072.
24. Rhee MS, Kim JW, Qian YL, Ingram LO, Shanmugam KT. 2007. Development of plasmid vector and electroporation condition for gene transfer in sporogenic lactic acid bacterium, Bacillus coagulans. Plasmid 58:13-22. http://dx.doi.org/10.1016/j.plasmid.2006.11.006.
25. Hurlbert JC, Preston JF. 2001. Functional characterization of a novel xylanase from a corn strain of Erwinia chrysanthemi. J. Bacteriol. 183: 2093-2100. http://dx.doi.org/10.1128/JB.183.6.2093-2100.2001.
26. Dubois M, Gilles KA, Hamilton JK, Rebers PA, Smith F. 1956. Colorimetric method for determination of sugars and related substances. Anal. Chem. 28:350-356. http://dx.doi.org/10.1021/ac60111a017.
27. Blumenkrantz N, Asboe-Hansen G. 1973. New method for quantitative determination of uronic acids. Anal. Biochem. 54:484-489. http://dx.doi .org/10.1016/0003-2697(73)90377-1.
28. Nelson N. 1944. A photometric adaptation of the Somogyi method for the determination of glucose. J. Biol. Chem. 153:375-380.
29. Kenealy WR, Jeffries TW. 2003. Rapid 2,2=-bicinchoninic-based xylanase assay compatible with high throughput screening. Biotechnol. Lett. 25: 1619-1623. http://dx.doi.org/10.1023/A:1025668031928.
30. Zhou SD, Ingram LO. 2001. Simultaneous saccharification and fermentation of amorphous cellulose to ethanol by recombinant Klebsiella oxytoca SZ21 without supplemental cellulase. Biotechnol. Lett. 23:1455-1462. http://dx.doi.org/10.1023/A:1011623509335.
31. Kardosova A, Matulova M, Malovikova A. 1998. (4-O-Methyl-alpha-Dglucurono)- D-xylan from Rudbeckia fulgida, var. sullivantii (Boynton et Beadle). Carbohydr. Res. 308:99-105. http://dx.doi.org/10.1016/S0008 -6215(98)00072-X.
32. Zuobi-Hasona K, St John FJ, Rice JD, Preston JF. 2001. Oligosaccharides containing glucuronoxylose as substrates for selecting bacteria for depolymerization of hemicellulose, p 534. Abstr. 101st Gen. Meet. Am. Soc. Microbiol., Orlando, FL. American Society for Microbiology, Washington, DC.
33. Cavagna F, Deger H, Puls J. 1984. 2D-NMR analysis of the structure of an aldotriouronic acid obtained from birch wood. Carbohydr. Res. 129:1-8. http://dx.doi.org/10.1016/0008-6215(84)85293-3.
34. Koutaniemi S, Guillon F, Tranquet O, Bouchet B, Tuomainen P, Virkki L, Petersen HL, Willats WGT, Saulnier L, Tenkanen M. 2012. Substituent-specific antibody against glucuronoxylan reveals close association of glucuronic acid and acetyl substituents and distinct labeling patterns in tree species. Planta 236:739-751. http://dx.doi.org/10.1007/s00425-012-1653-7.
35. St. John FJ, Preston JF, Pozharski E. 2012. Novel structural features of xylanase A1 from Paenibacillus sp. JDR-2. J. Struct. Biol. 180:303-311. http://dx.doi.org/10.1016/j.jsb.2012.09.007.
36. Chow V, Nong G, Preston JF. 2007. Structure, function, and regulation of the aldouronate utilization gene cluster from Paenibacillus sp. strain JDR-2. J. Bacteriol. 189:8863-8870. http://dx.doi.org/10.1128/JB.01141-07.
37. Nishitani K, Nevins DJ. 1991. Glucuronoxylan xylanohydrolase-a unique xylanase with requirement for appendant glucuronosyl units. J. Biol. Chem. 266:6539-6543.
38. Rice J, Nong G, Ragunathan A, St. John FJ, Preston JF. 2005. Depolymerization processes catalyzed by the GH5 endoxylanase secreted by Erwinia chrysanthemi PI, p 52. Abstr. 105th Gen. Meet. Am. Soc. Microbiol., Atlanta, GA. American Society for Microbiology, Washington, DC.
39. Vrsanska M, Kolenova K, Puchart V, Biely P. 2007. Mode of action of glycoside hydrolase family 5 glucuronoxylan xylanohydrolase from Erwinia chrysanthemi. FEBS J. 274:1666-1677. http://dx.doi.org/10.1111/j .1742-4658.2007.05710.x.
40. Ebringerova A, Kardosova A, Hromadkova Z, Malovikova A, Hribalova V. 2002. Immunomodulatory activity of acidic xylans in relation to their structural and molecular properties. Int. J. Biol. Macromol. 30:1-6. http: //dx.doi.org/10.1016/S0141-8130(01)00186-6.
41. Christakopoulos P, Katapodis P, Kalogeris E, Kekos D, Macris BJ, Stamatis H, Skaltsa H. 2003. Antimicrobial activity of acidic xylo-oligosaccharides produced by family 10 and 11 endoxylanases. Int. J. Biol. Macromol. 31:171-175. http://dx .doi.org/10.1016/S0141-8130(02)00079-X.
42. Kwan C, Bell R, Koenig T, Bischofberger A, Horadagoda N, Perkins NR, Jeffcott LB, Dart AJ. 2012. Effects of intra-articular sodium pentosan polysulfate and glucosamine on the cytology, total protein concentration and viscosity of synovial fluid in horses. Aust. Vet. J. 90:315-320. http://dx .doi.org/10.1111/j.1751-0813.2012.00959.x.
43. Daus S, Petzold-Welcke K, Kötteritzsch M, Baumgaertel A, Schubert US, Heinze T. 2011. Homogeneous sulfation of xylan from different sources. Macromol. Mater. Eng. 296:551-561. http://dx.doi.org/10.1002 /mame.201000390.
44. Bryan EM, Bae T, Kleerebezem H, Dunny GM. 2000. Improved vectors for nisin-controlled expression in gram-positive bacteria. Plasmid 44: 183-190. http://dx.doi.org/10.1006/plas.2000.1484.
45. Wilson AC, Perego M, Hoch JA. 2007. New transposon delivery plasmids for insertional mutagenesis in Bacillus anthracis. J. Microbiol. Methods 71:332-335. http://dx.doi.org/10.1016/j.mimet.2007.09.006.