Alginate lyases from alginate-degrading Vibrio splendidus 12B01 are endolytic

Applied and Environmental Microbiology

Volumn 81, Issue 5, 2015, Pages 1865-1873

  Badur, Ahmet H ^a   Jagtap, Sujit Sadashiv ^a,b   Yalamanchili, Geethika ^a   Lee, Jung Kul ^b   Zhao, Huimin ^a   Rao, Christopher V ^a  

^a UNIVERSITY OF ILLINOIS AT URBANA CHAMPAIGN   (United States)

^b Konkuk University   (South Korea)

Author keywords

[No Author keywords available]

Indexed keywords

ALGINATE; ALUMINUM COMPOUNDS; ENZYMES; OLIGOMERS;

GLYCOSIDIC BOND; MARINE BACTERIOPLANKTON; MARINE ENVIRONMENT; OPTIMAL ACTIVITY; SOLE CARBON SOURCE; TURNOVER NUMBER;

BORON COMPOUNDS;

ALGINATE; AQUATIC ORGANISM; BACTERIOPLANKTON; BIODEGRADATION; ENZYME;

VIBRIO SPLENDIDUS;

ALGINIC ACID; GLUCURONIC ACID; HEXURONIC ACID; LYASE;

CHEMICAL STRUCTURE; ENZYMOLOGY; ISOLATION AND PURIFICATION; KINETICS; METABOLISM; PH; PROTEIN CONFORMATION; TEMPERATURE; VIBRIO;

ALGINATES; GLUCURONIC ACID; HEXURONIC ACIDS; HYDROGEN-ION CONCENTRATION; KINETICS; LYASES; MODELS, MOLECULAR; PROTEIN CONFORMATION; TEMPERATURE; VIBRIO;

EID: 84922900688     PISSN: 00992240     EISSN: 10985336     Source Type: Journal    
DOI: 10.1128/AEM.03460-14     Document Type: Article

References (57)

1. Boyen C, Bertheau Y, Barbeyron T, Kloareg B. 1990. Preparation of guluronate lyase from Pseudomonas alginovora for protoplast isolation in Laminaria. Enzyme Microb Technol 12:885-890. http://dx.doi.org/10.1016/0141-0229(90)90027-N.
2. Matsubara Y, Kawada R, Iwasaki K, Kimura Y, Oda T, Muramatsu T. 2000. Cloning and sequence analysis of a gene (aly PG) encoding poly(alpha-L-guluronate)lyase from Corynebacterium sp. strain ALY-1. J Biosci Bioeng 89:199-202. http://dx.doi.org/10.1016/S1389-1723(00)88738-1.
3. Wong TY, Preston LA, Schiller NL. 2000. Alginate lyase: review of major sources and enzyme characteristics, structure-function analysis, biological roles, and applications. Annu Rev Microbiol 54:289-340. http://dx.doi.org/10.1146/annurev.micro.54.1.289.
4. Singh A, Nigam PS, Murphy JD. 2011. Renewable fuels from algae: an answer to debatable land based fuels. Bioresour Technol 102:10-16. http://dx.doi.org/10.1016/j.biortech.2010.06.032.
5. Enquist-Newman M, Faust AM, Bravo DD, Santos CN, Raisner RM, Hanel A, Sarvabhowman P, Le C, Regitsky DD, Cooper SR, Peereboom L, Clark A, Martinez Y, Goldsmith J, Cho MY, Donohoue PD, Luo L, Lamberson B, Tamrakar P, Kim EJ, Villari JL, Gill A, Tripathi SA, Karamchedu P, Paredes CJ, Rajgarhia V, Kotlar HK, Bailey RB, Miller DJ, Ohler NL, Swimmer C, Yoshikuni Y. 2014. Efficient ethanol production from brown macroalgae sugars by a synthetic yeast platform. Nature 505:239-243. http://dx.doi.org/10.1038/nature12771.
6. Stephens E, de Nys R, Ross IL, Hankamer B. 2013. Algae fuels as an alternative to petroleum. J Pet Environ Biotechnol 4:4. http://dx.doi.org/10.4172/2157-7463.1000148.
7. Ge L, Wang P, Mou H. 2011. Study on saccharification techniques of seaweed wastes for the transformation of ethanol. Renew Energy 36:84-89. http://dx.doi.org/10.1016/j.renene.2010.06.001.
8. Martone PT, Estevez JM, Lu F, Ruel K, Denny MW, Somerville C, Ralph J. 2009. Discovery of lignin in seaweed reveals convergent evolution of cell-wall architecture. Curr Biol 19:169-175. http://dx.doi.org/10.1016/j.cub.2008.12.031.
9. Hu X, Jiang X, Hwang HM. 2006. Purification and characterization of an alginate lyase from marine bacterium Vibrio sp. mutant strain 510-64. Curr Microbiol 53:135-140. http://dx.doi.org/10.1007/s00284-005-0347-9.
10. Kim DE, Lee EY, Kim HS. 2009. Cloning and characterization of alginate lyase from a marine bacterium Streptomyces sp. ALG-5. Mar Biotechnol 11:10-16. http://dx.doi.org/10.1007/s10126-008-9114-9.
11. Sawabe T, Ohtsuka M, Ezura Y. 1997. Novel alginate lyases from marine bacterium Alteromonas sp. strain H-4. Carbohydr Res 304:69-76. http://dx.doi.org/10.1016/S0008-6215(97)00194-8.
12. Yamasaki M, Moriwaki S, Miyake O, Hashimoto W, Murata K, Mikami B. 2004. Structure and function of a hypothetical Pseudomonas aeruginosa protein PA1167 classified into family PL-7: a novel alginate lyase with a beta-sandwich fold. J Biol Chem 279:31863-31872. http://dx.doi.org/10.1074/jbc.M402466200.
13. Lombard V, Bernard T, Rancurel C, Brumer H, Coutinho PM, Henrissat B. 2010. Ahierarchical classification of polysaccharide lyases for glycogenomics. Biochem J 432:437-444. http://dx.doi.org/10.1042/BJ20101185.
14. Garron ML, Cygler M. 2010. Structural and mechanistic classification of uronic acid-containing polysaccharide lyases. Glycobiology 20:1547-1573. http://dx.doi.org/10.1093/glycob/cwq122.
15. Yamasaki M, Ogura K, Hashimoto W, Mikami B, Murata K. 2005. A structural basis for depolymerization of alginate by polysaccharide lyase family-7. J Mol Biol 352:11-21. http://dx.doi.org/10.1016/j.jmb.2005.06.075.
16. Matsubara Y, Kawada R, Iwasaki K, Oda T, Muramatsu T. 1998. Extracellular poly(alpha-L-guluronate)lyase from Corynebacterium sp.: purification, characteristics, and conformational properties. J Protein Chem 17:29-36. http://dx.doi.org/10.1023/A:1022534429792.
17. Malissard M, Duez C, Guinand M, Vacheron MJ, Michel G, Marty N, Joris B, Thamm I, Ghuysen JM. 1993. Sequence of a gene encoding a (poly ManA) alginate lyase active on Pseudomonas aeruginosa alginate. FEMS Microbiol Lett 110:101-106. http://dx.doi.org/10.1111/j.1574-6968.1993.tb06302.x.
18. Gacesa P. 1987. Alginate-modifying enzymes: a proposed unified mechanism of action for the lyases and epimerases. FEBS Lett 212:199-202. http://dx.doi.org/10.1016/0014-5793(87)81344-3.
19. Han YH, Garron ML, Kim HY, Kim WS, Zhang Z, Ryu KS, Shaya D, Xiao Z, Cheong C, Kim YS, Linhardt RJ, Jeon YH, Cygler M. 2009. Structural snapshots of heparin depolymerization by heparin lyase I. J Biol Chem 284:34019-34027. http://dx.doi.org/10.1074/jbc.M109.025338.
20. Yip VL, Varrot A, Davies GJ, Rajan SS, Yang X, Thompson J, Anderson WF, Withers SG. 2004. An unusual mechanism of glycoside hydrolysis involving redox and elimination steps by a family 4 beta-glycosidase from Thermotoga maritima. J Am Chem Soc 126:8354-8355. http://dx.doi.org/10.1021/ja047632w.
21. Yip VL, Withers SG. 2006. Breakdown of oligosaccharides by the process of elimination. Curr Opin Chem Biol 10:147-155. http://dx.doi.org/10.1016/j.cbpa.2006.02.005.
22. Haug A, Larsen B, Smidsrød O. 1967. Studies on the sequence of uronic acid residues in alginic acid. Acta Chem Scand 21:691-704. http://dx.doi.org/10.3891/acta.chem.scand.21-0691.
23. Park D, Jagtap S, Nair SK. 2014. Structure of a PL17 family alginate lyase demonstrates functional similarities among exotype depolymerases. J Biol Chem 289:8645-8655. http://dx.doi.org/10.1074/jbc.M113.531111.
24. Kitamikado M, Tseng CH, Yamaguchi K, Nakamura T. 1992. Two types of bacterial alginate lyases. Appl Environ Microbiol 58:2474-2478.
25. Kawamoto H, Horibe A, Miki Y, Kimura T, Tanaka K, Nakagawa T, Kawamukai M, Matsuda H. 2006. Cloning and sequencing analysis of alginate lyase genes from the marine bacterium Vibrio sp. O2. Mar Biotechnol 8:481-490. http://dx.doi.org/10.1007/s10126-005-6157-z.
26. Hamza A, Piao YL, Kim MS, Choi CH, Zhan CG, Cho H. 2011. Insight into the binding of the wild type and mutated alginate lyase (AlyVI) with its substrate: a computational and experimental study. Biochim Biophys Acta 1814:1739-1747. http://dx.doi.org/10.1016/j.bbapap.2011.08.018.
27. Wang Y, Guo E, Yu W, Han F. 2013. Purification and characterization of a new alginate lyase from a marine bacterium Vibrio sp. Biotechnol Lett 35:703-708. http://dx.doi.org/10.1007/s10529-012-1134-x.
28. Fu XT, Lin H, Kim SM. 2007. Purification and characterization of a Na+/K+dependent alginate lyase from turban shell gut Vibrio sp. YKW-34. Enzyme Microb Technol 41:828-834. http://dx.doi.org/10.1016/j.enzmictec.2007.07.003.
29. Thomas F, Lundqvist LC, Jam M, Jeudy A, Barbeyron T, Sandstrom C, Michel G, Czjzek M. 2013. Comparative characterization of two marine alginate lyases from Zobellia galactanivorans reveals distinct modes of action and exquisite adaptation to their natural substrate. J Biol Chem 288: 23021-23037. http://dx.doi.org/10.1074/jbc.M113.467217.
30. Thompson FL, Gevers D, Thompson CC, Dawyndt P, Naser S, Hoste B, Munn CB, Swings J. 2005. Phylogeny and molecular identification of vibrios on the basis of multilocus sequence analysis. Appl Environ Microbiol 71:5107-5115. http://dx.doi.org/10.1128/AEM.71.9.5107-5115.2005.
31. Le Roux F, Zouine M, Chakroun N, Binesse J, Saulnier D, Bouchier C, Zidane N, Ma L, Rusniok C, Lajus A, Buchrieser C, Medigue C, Polz MF, Mazel D. 2009. Genome sequence of Vibrio splendidus: an abundant planctonic marine species with a large genotypic diversity. Environ Microbiol 11:1959-1970. http://dx.doi.org/10.1111/j.1462-2920.2009.01918.x.
32. Wargacki AJ, Leonard E, Win MN, Regitsky DD, Santos CN, Kim PB, Cooper SR, Raisner RM, Herman A, Sivitz AB, Lakshmanaswamy A, Kashiyama Y, Baker D, Yoshikuni Y. 2012. An engineered microbial platform for direct biofuel production from brown macroalgae. Science 335:308-313. http://dx.doi.org/10.1126/science.1214547.
33. Garrison T. Oceanography: an invitation to marine science, 8th ed. Cengage Learning, Boston, MA.
34. Gomez-Leon J, Villamil L, Lemos ML, Novoa B, Figueras A. 2005. Isolation of Vibrio alginolyticus and Vibrio splendidus from aquacultured carpet shell clam (Ruditapes decussatus) larvae associated with mass mortalities. Appl Environ Microbiol 71:98-104. http://dx.doi.org/10.1128/AEM.71.1.98-104.2005.
35. Biasini M, Bienert S, Waterhouse A, Arnold K, Studer G, Schmidt T, Kiefer F, Cassarino TG, Bertoni M, Bordoli L, Schwede T. 2014. SWISS-MODEL: modelling protein tertiary and quaternary structure using evolutionary information. Nucleic Acids Res 42:W252-W258. http://dx.doi.org/10.1093/nar/gku340.
36. Lundqvist LC, Jam M, Barbeyron T, Czjzek M, Sandstrom C. 2012. Substrate specificity of the recombinant alginate lyase from the marine bacteria Pseudomonas alginovora. Carbohydr Res 352:44-50. http://dx.doi.org/10.1016/j.carres.2012.02.014.
37. Humphrey W, Dalke A, Schulten K. 1996. VMD: visual molecular dynamics. J Mol Graph 14:27-38.
38. Petersen TN, Brunak S, von Heijne G, Nielsen H. 2011. SignalP 4.0: discriminating signal peptides from transmembrane regions. Nat Methods 8:785-786. http://dx.doi.org/10.1038/nmeth.1701.
39. Yuan W, Glekas GD, Allen GM, Walukiewicz HE, Rao CV, Ordal GW. 2012. The importance of the interaction of CheD with CheC and the chemoreceptors compared to its enzymatic activity during chemotaxis in Bacillus subtilis. PLoS One 7:e50689. http://dx.doi.org/10.1371/journal.pone.0050689.
40. Weissbach A, Hurwitz J. 1959. The formation of 2-keto-3-deoxyheptonic acid in extracts of Escherichia coli B. I. Identification. J Biol Chem 234:705-709.
41. Preiss J, Ashwell G. 1962. Alginic acid metabolism in bacteria. I. Enzymatic formation of unsaturated oligosaccharides and 4-deoxy-L-erythro-5-hexoseulose uronic acid. J Biol Chem 237:309-316.
42. Waravdekar VS, Saslaw LD. 1957. A method of estimation of 2-deoxyribose. Biochim Biophys Acta 24:439. http://dx.doi.org/10.1016/0006-3002(57)90224-X.
43. Ryu M, Lee EY. 2011. Saccharification of alginate by using exolytic oligoalginate lyase from marine bacterium Sphingomonas sp. MJ-3. J Indust Eng Chem 17:853-858. http://dx.doi.org/10.1016/j.jiec.2011.08.001.
44. Chhatbar M, Meena R, Prasad K, Siddhanta AK. 2009. Microwave assisted rapid method for hydrolysis of sodium alginate for M/G ratio determination. Carbohydr Res 76:650-656. http://dx.doi.org/10.1016/j.carbpol.2008.11.033.
45. Rozen S, Skaletsky H. 2000. Primer3 on theWWWfor general users and for biologist programmers. Methods Mol Biol 132:365-386.
46. Jagtap SS, Hehemann JH, Polz MF, Lee JK, Zhao H. 2014. Comparative biochemical characterization of three exolytic oligoalginate lyases from Vibrio splendidus reveals complementary substrate scope, temperature, andpHadaptations. Appl Environ Microbiol 80:4207-4214. http://dx.doi.org/10.1128/AEM.01285-14.
47. Kam N, Park YJ, Lee EY, Kim HS. 2011. Molecular identification of a polyM-specific alginate lyase from Pseudomonas sp. strain KS-408 for degradation of glycosidic linkages between two mannuronates or mannuronate and guluronate in alginate. Can J Microbiol 57:1032-1041. http://dx.doi.org/10.1139/w11-106.
48. Grasdalen H. 1983. High-field, 1H-n.m.r. spectroscopy of alginate: sequential structure and linkage conformations. Carbohydr Res 118:255-260. http://dx.doi.org/10.1016/0008-6215(83)88053-7.
49. Heyraud A, Gey C, Leonard C, Rochas C, Girond S, Kloareg B. 1996. NMR spectroscopy analysis of oligoguluronates and oligomannuronates prepared by acid or enzymatic hydrolysis of homopolymeric blocks of alginic acid. Application to the determination of the substrate specificity of Haliotis tuberculata alginate lyase. Carbohydr Res 289:11-23.
50. Grasdalen H, Larsen B, Smidsrod O. 1979. A p.m.r. study of the composition and sequence of uronate residues in alginates. Carbohydr Res 68:23-31. http://dx.doi.org/10.1016/S0008-6215(00)84051-3.
51. Ertesvag H, Erlien F, Skjak-Braek G, Rehm BH, Valla S. 1998. Biochemical properties and substrate specificities of a recombinantly produced Azotobacter vinelandii alginate lyase. J Bacteriol 180:3779-3784.
52. Zhang ZQ, Yu GL, Guan HS, Zhao X, Du YG, Jiang XL. 2004. Preparation and structure elucidation of alginate oligosaccharides degraded by alginate lyase from Vibrio sp. 510. Carbohydr Res 339:1475-1481. http://dx.doi.org/10.1016/j.carres.2004.03.010.
53. Holtan S, Zhang Q, Strand WI, Skjak-Braek G. 2006. Characterization of the hydrolysis mechanism of polyalternating alginate in weak acid and assignment of the resulting MG-oligosaccharides by NMR spectroscopy and ESI-mass spectrometry. Biomacromolecules 7:2108-2121. http://dx.doi.org/10.1021/bm050984q.
54. Ficko-Blean E, Boraston AB. 2006. The interaction of a carbohydrate-binding module from a Clostridium perfringens N-acetyl-betahexosaminidase with its carbohydrate receptor. J Biol Chem 281:37748-37757. http://dx.doi.org/10.1074/jbc.M606126200.
55. Duan G, Han F, Yu W. 2009. Cloning, sequence analysis, and expression of gene alyPI encoding an alginate lyase from marine bacterium Pseudoalteromonas sp. CY24. Can J Microbiol 55:1113-1118. http://dx.doi.org/10.1139/W09-051.
56. Favorov VV, Vozhova EI, Denisenko VA, Elyakova LA. 1979. A study of the reaction catalysed by alginate lyase VI from the sea mollusc, Littorina sp. Biochim Biophys Acta 569:259-266. http://dx.doi.org/10.1016/0005-2744(79)90061-5.
57. Haraguchi K, Kodama T. 1996. Purification and properties of poly(β-Dmannuronate) lyase from Azotobacter chroococcum. Appl Microbiol Biotechnol 44:576-581. http://dx.doi.org/10.1007/BF00172488.