Cooperative degradation of chitin by extracellular and cell surface-expressed chitinases from Paenibacillus sp. strain FPU-7

Applied and Environmental Microbiology

Volumn 79, Issue 23, 2013, Pages 7482-7490

  Itoh, Takafumi ^a   Hibi, Takao ^a   Fujii, Yutaka ^b   Sugimoto, Ikumi ^a   Fujiwara, Akihiro ^a   Suzuki, Fumiko ^a   Iwasaki, Yukimoto ^a   Kim, Jin Kyung ^c   Taketo, Akira ^d   Kimoto, Hisashi ^a  

^a FUKUI PREFECTURAL UNIVERSITY   (Japan)

^b UNIVERSITY OF FUKUI   (Japan)

^c Catholic University of Daegu   (South Korea)

^d FUKUI UNIVERSITY OF TECHNOLOGY   (Japan)

Author keywords

[No Author keywords available]

Indexed keywords

BACTERIAL CELL SURFACE; BIOCHEMICAL CHARACTERIZATION; CHITINOLYTIC ACTIVITY; DEGRADATION PRODUCTS; ENVIRONMENTALLY FRIENDLY PROCESSING; ESCHERICHIA COLI CELLS; EXTRACELLULAR CHITINASES; PHYLOGENETIC ANALYSIS;

CELL MEMBRANES; CLONING; DEGRADATION; DIAGNOSIS; ESCHERICHIA COLI; GENE EXPRESSION; PROCESSING;

CHITIN;

BIOCHEMICAL COMPOSITION; BIODEGRADATION; CELL ORGANELLE; CELLULOSE; CHITIN; ENZYME ACTIVITY; PHYLOGENETICS; POLYSACCHARIDE; PROTEIN;

BACTERIAL DNA; CHITIN; CHITINASE;

ARTICLE; CHEMISTRY; CLASSIFICATION; CULTURE MEDIUM; DNA SEQUENCE; ENZYMOLOGY; ESCHERICHIA COLI; GENE EXPRESSION; GENETICS; ISOLATION AND PURIFICATION; MASS SCREENING; METABOLISM; METHODOLOGY; MICROBIOLOGICAL EXAMINATION; MICROBIOLOGY; MOLECULAR CLONING; MOLECULAR GENETICS; NUCLEOTIDE SEQUENCE; PAENIBACILLUS;

BACTERIOLOGICAL TECHNIQUES; CHITIN; CHITINASE; CLONING, MOLECULAR; CULTURE MEDIA; DNA, BACTERIAL; ESCHERICHIA COLI; GENE EXPRESSION; MASS SCREENING; MOLECULAR SEQUENCE DATA; PAENIBACILLUS; SEQUENCE ANALYSIS, DNA; SOIL MICROBIOLOGY;

EID: 84888233018     PISSN: 00992240     EISSN: 10985336     Source Type: Journal    
DOI: 10.1128/AEM.02483-13     Document Type: Article

References (54)

1. Aam BB, Heggset EB, Norberg AL, Sorlie M, Varum KM, Eijsink VG. 2010. Production of chitooligosaccharides and their potential applications in medicine. Mar. Drugs 8:1482-1517.
2. Chen JK, Shen CR, Liu CL. 2010. N-acetylglucosamine: production and applications. Mar. Drugs 8:2493-2516.
3. Park BK, Kim MM. 2010. Applications of chitin and its derivatives in biological medicine. Int. J. Mol. Sci. 11:5152-5164.
4. El Hadrami A, Adam LR, El Hadrami I, Daayf F. 2010. Chitosan in plant protection. Mar. Drugs 8:968-987.
5. Watanabe T, Oyanagi W, Suzuki K, Tanaka H. 1990. Chitinase system of Bacillus circulans WL-12 and importance of chitinase A1 in chitin degradation. J. Bacteriol. 172:4017-4022.
6. Fuchs RL, McPherson SA, Drahos DJ. 1986. Cloning of a Serratia marcescens gene encoding chitinase. Appl. Environ. Microbiol. 51:504-509.
7. Saito A, Fujii T, Yoneyama T, Miyashita K. 1998. glkA is involved in glucose repression of chitinase production in Streptomyces lividans. J. Bacteriol. 180:2911-2914.
8. Sitrit Y, Vorgias CE, Chet I, Oppenheim AB. 1995. Cloning and primary structure of the chiA gene from Aeromonas caviae. J. Bacteriol. 177:4187-4189.
9. Techkarnjanaruk S, Goodman AE. 1999. Multiple genes involved in chitin degradation from the marine bacterium Pseudoalteromonas sp. strain S91. Microbiology 145:925-934.
10. Montgomery MT, Kirchman DL. 1993. Role of chitin-binding proteins in the specific attachment of the marine bacterium Vibrio harveyi to chitin. Appl. Environ. Microbiol. 59:373-379.
11. Vaaje-Kolstad G, Horn SJ, Sorlie M, Eijsink VG. 2013. The chitinolytic machinery of Serratia marcescens-a model system for enzymatic degradation of recalcitrant polysaccharides. FEBS J. 280:3028-3049.
12. 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:D233-D238.
13. Dahiya N, Tewari R, Hoondal GS. 2006. Biotechnological aspects of chitinolytic enzymes: a review. Appl. Microbiol. Biotechnol. 71:773-782.
14. Eijsink V, Hoell I, Vaaje-Kolstada G. 2010. Structure and function of enzymes acting on chitin and chitosan. Biotechnol. Genet. Eng. Rev. 27:331-366.
15. Okazaki K, Yamashita Y, Noda M, Sueyoshi N, Kameshita I, Hayakawa S. 2004. Molecular cloning and expression of the gene encoding family 19 chitinase from Streptomyces sp. J-13-3. Biosci. Biotechnol. Biochem. 68:341-351.
16. Ueda M, Kojima M, Yoshikawa T, Mitsuda N, Araki K, Kawaguchi T, Miyatake K, Arai M, Fukamizo T. 2003. A novel type of family 19 chitinase from Aeromonas s. no. 10S-24. Cloning, sequence, expression, and the enzymatic properties. Eur. J. Biochem. 270:2513-2520.
17. Beintema JJ. 1994. Structural features of plant chitinases and chitinbinding proteins. FEBS Lett. 350:159-163.
18. Iseli B, Armand S, Boller T, Neuhaus JM, Henrissat B. 1996. Plant chitinases use two different hydrolytic mechanisms. FEBS Lett. 382:186-188.
19. Wohlkonig A, Huet J, Looze Y, Wintjens R. 2010. Structural relationships in the lysozyme superfamily: significant evidence for glycoside hydrolase signature motifs. PLoS One 5:e15388.doi:10.1371/journal.pone.0015388.
20. Liu T, Zhang H, Liu F, Chen L, Shen X, Yang Q. 2011. Active-pocket size differentiating insectile from bacterial chitinolytic beta-N-acetyl-Dhexosaminidases. Biochem. J. 438:467-474.
21. Fujita K, Shimomura K, Yamamoto K, Yamashita T, Suzuki K. 2006. A chitinase structurally related to the glycoside hydrolase family 48 is indispensable for the hormonally induced diapause termination in a beetle. Biochem. Biophys. Res. Commun. 345:502-507.
22. Bhattacharya D, Nagpure A, Gupta RK. 2007. Bacterial chitinases: properties and potential. Crit. Rev. Biotechnol. 27:21-28.
23. Patil RS, Ghormade VV, Deshpande MV. 2000. Chitinolytic enzymes: an exploration. Enzyme Microb. Technol. 26:473-483.
24. Gooday GW. 1994. Physiology of microbial degradation of chitin and chitosan. Kluwer Academic Publishers, Dordrecht, The Netherlands.
25. Slepecky R, Hemphill E. 1992. The genus Bacillus-nonmedical, p 1663-1696. In Balows A, Trüper HG, Dworkin M, Harder W, Schleifer KH (ed), The prokaryotes, 2nd ed. Springer, New York, NY.
26. Claus D, Berkeley RCW. 1986. Genus Bacillus Cohn 1872, 174AL, p 1105-1139. In Sneath PHA, Mair NS, Sharpe ME, Holt JG (ed), Bergey's manual of systematic bacteriology, vol 2, 1st ed. Williams & Wilkins, Baltimore, MD
27. von der Weid I, Alviano DS, Santos AL, Soares RM, Alviano CS, Seldin L. 2003. Antimicrobial activity of Paenibacillus peoriae strain NRRL BD-62 against a broad spectrum of phytopathogenic bacteria and fungi. J. Appl. Microbiol. 95:1143-1151.
28. Spizizen J. 1958. Transformation of biochemically deficient strains of Bacillus Subtilis by deoxyribonucleate. Proc. Natl. Acad. Sci. U. S. A. 44:1072-1078.
29. Miller LC, Tainter ML. 1944. Estimation of ED50 and its error by means of logarithmic probit graph paper. Proc. Soc. Exp. Biol. Med. 57:261-264.
30. Kimoto H, Kusaoke H, Yamamoto I, Fujii Y, Onodera T, Taketo A. 2002. Biochemical and genetic properties of Paenibacillus glycosyl hydrolase having chitosanase activity and discoidin domain. J. Biol. Chem. 277:14695-14702.
31. Kimoto H, Taketo A. 1997. Initial stage of DNA-electrotransfer into E. coli cells. J. Biochem. 122:237-242.
32. Punta M, Coggill PC, Eberhardt RY, Mistry J, Tate J, Boursnell C, Pang N, Forslund K, Ceric G, Clements J, Heger A, Holm L, Sonnhammer EL, Eddy SR, Bateman A, Finn RD. 2012. The Pfam protein families database. Nucleic Acids Res. 40:D290-D301.
33. Kimoto H, Fujii Y, Yokota Y, Taketo A. 2005. Molecular characterization of NADase-streptolysin O operon of hemolytic streptococci. Biochim. Biophys. Acta 1681:134-149.
34. Laemmli UK. 1970. Cleavage of structural proteins during the assembly of the head of bacteriophage T4. Nature 227:680-685.
35. Hamady M, Knight R. 2009. Microbial community profiling for human microbiome projects: tools, techniques, and challenges. Genome Res. 19:1141-1152.
36. Shida O, Takagi H, Kadowaki K, Nakamura LK, Komagata K. 1997. Transfer of Bacillus alginolyticus, Bacillus chondroitinus, Bacillus curdlanolyticus, Bacillus glucanolyticus, Bacillus kobensis, and Bacillus thiaminolyticus to the genus Paenibacillus and emended description of the genus Paenibacillus. Int. J. Syst. Bacteriol. 47:289-298.
37. Heyndrickx M, Vandemeulebroecke K, Scheldeman P, Hoste B, Kersters K, De Vos P, Logan NA, Aziz AM, Ali N, Berkeley RC. 1995. Paenibacillus (formerly Bacillus) gordonae (Pichinoty et a. 1986) Ash et al. 1994 is a later subjective synonym of Paenibacillus (formerly Bacillus) validus (Nakamura 1984) Ash et al. 1994: emended description of P. validus. Int. J. Syst. Bacteriol. 45:661-669.
38. Sonnhammer EL, Eddy SR, Durbin R. 1997. Pfam: a comprehensive database of protein domain families based on seed alignments. Proteins 28:405-420.
39. Finn RD, Mistry J, Tate J, Coggill P, Heger A, Pollington JE, Gavin OL, Gunasekaran P, Ceric G, Forslund K, Holm L, Sonnhammer EL, Eddy SR, Bateman A. 2010. The Pfam protein families database. Nucleic Acids Res. 38:D211-D222.
40. Fukuda M, Watanabe S, Yoshida S, Itoh H, Itoh Y, Kamio Y, Kaneko J. 2010. Cell surface xylanases of the glycoside hydrolase family 10 are essential for xylan utilization by Paenibacillus sp. W-61 as generators of xylo-oligosaccharide inducers for the xylanase genes. J. Bacteriol. 192:2210-2219.
41. Huang QS, Xie XL, Liang G, Gong F, Wang Y, Wei XQ, Wang Q, Ji ZL, Chen QX. 2012. The GH18 family of chitinases: their domain architectures, functions and evolutions. Glycobiology 22:23-34.
42. Hiramatsu S, Fujie M, Usami S, Sakai K, Yamada T. 2000. Two catalytic domains of Chlorella virus CVK2 chitinase. J. Biosci. Bioeng. 89:252-257.
43. Tanaka T, Fukui T, Imanaka T. 2001. Different cleavage specificities of the dual catalytic domains in chitinase from the hyperthermophilic archaeon Thermococcus kodakaraensis KOD1. J. Biol. Chem. 276:35629-35635.
44. Howard MB, Ekborg NA, Taylor LE, II, Weiner RM, Hutcheson SW. 2004. Chitinase B of "Microbulbifer degradans" 2-40 contains two catalytic domains with different chitinolytic activities. J. Bacteriol. 186:1297-1303.
45. Babu MM, Priya ML, Selvan AT, Madera M, Gough J, Aravind L, Sankaran K. 2006. A database of bacterial lipoproteins (DOLOP) with functional assignments to predicted lipoproteins. J. Bacteriol. 188:2761-2773.
46. Singh AK, Ghodke I, Chhatpar HS. 2009. Pesticide tolerance of Paenibacillus sp. D1 and its chitinase. J. Environ. Manage. 91:358-362.
47. Pason P, Kyu KL, Ratanakhanokchai K. 2006. Paenibacillus curdlanolyticus strain B-6 xylanolytic-cellulolytic enzyme system that degrades insoluble polysaccharides. Appl. Environ. Microbiol. 72:2483-2490.
48. DasGupta SM, Khan N, Nautiyal CS. 2006. Biologic control ability of plant growth-promoting Paenibacillus lentimorbus NRRL B-30488 isolated from milk. Curr. Microbiol. 53:502-505.
49. Aktuganov G, Melentjev A, Galimzianova N, Khalikova E, Korpela T, Susi P. 2008. Wide-range antifungal antagonism of Paenibacillus ehimensis IB-X-b and its dependence on chitinase and beta-1,3-glucanase production. Can. J. Microbiol. 54:577-587.
50. Kimoto H, Akamatsu M, Fujii Y, Tatsumi H, Kusaoke H, Taketo A. 2010. Discoidin domain of chitosanase is required for binding to the fungal cell wall. J. Mol. Microbiol. Biotechnol. 18:14-23.
51. Purushotham P, Arun PV, Prakash JS, Podile AR. 2012. Chitin binding proteins act synergistically with chitinases in Serratia proteamaculans 568. PLoS One 7:e36714.doi:10.1371/journal.pone.0036714.
52. Vaaje-Kolstad G, Bohle LA, Gaseidnes S, Dalhus B, Bjoras M, Mathiesen G, Eijsink VG. 2012. Characterization of the chitinolytic machinery of Enterococcus faecalis V583 and high-resolution structure of its oxidative CBM33 enzyme. J. Mol. Biol. 416:239-254.
53. Vaaje-Kolstad G, Westereng B, Horn SJ, Liu Z, Zhai H, Sorlie M, Eijsink VG. 2010. An oxidative enzyme boosting the enzymatic conversion of recalcitrant polysaccharides. Science 330:219-222.
54. OECD. 2001. Guideline 423. OECD guideline for testing of chemicals. Acute oral toxicity-acute toxic class method. OECD, Paris, France.