The novel catabolic pathway of 3,6-anhydro-L-galactose, the main component of red macroalgae, in a marine bacterium

Environmental Microbiology

Volumn 17, Issue 5, 2015, Pages 1677-1688

  Yun, Eun Ju ^a   Lee, Saeyoung ^a   Kim, Hee Taek ^a   Pelton, Jeffrey G ^b   Kim, Sooah ^a   Ko, Hyeok Jin ^a   Choi, In Geol ^a   Kim, Kyoung Heon ^a  

^a Korea University   (South Korea)

^b LAWRENCE BERKELEY NATIONAL LABORATORY   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

BACTERIA (MICROORGANISMS); ESCHERICHIA COLI; VIBRIO SP.;

3,6-ANHYDROGALACTOSE; BIOFUEL; GALACTOSE;

ANALOGS AND DERIVATIVES; AQUATIC SPECIES; CARBOHYDRATE METABOLISM; ENERGY METABOLISM; ENZYMOLOGY; ESCHERICHIA COLI; FERMENTATION; GENE EXPRESSION PROFILING; GENETICS; METABOLISM; SEAWEED; VIBRIO;

AQUATIC ORGANISMS; BIOFUELS; CARBOHYDRATE METABOLISM; ENERGY METABOLISM; ESCHERICHIA COLI; FERMENTATION; GALACTOSE; GENE EXPRESSION PROFILING; METABOLIC NETWORKS AND PATHWAYS; SEAWEED; VIBRIO;

EID: 84928288752     PISSN: 14622912     EISSN: 14622920     Source Type: Journal    
DOI: 10.1111/1462-2920.12607     Document Type: Article

References (48)

1. Andberg, M., Maaheimo, H., Boer, H., Penttila, M., Koivula, A., and Richard, P. (2012) Characterization of a novel Agrobacterium tumefaciens galactarolactone cycloisomerase enzyme for direct conversion of D-galactarolactone to 3-deoxy-2-keto-L-threo-hexarate. J Biol Chem 287: 17662-17671.
2. Anders, S., and Huber, W. (2010) Differential expression analysis for sequence count data. Genome Biol 11: R106.
3. Duckworth, M., and Yaphe, W. (1971) The structure of agar: Part I. Fractionation of a complex mixture of polysaccharides. Carbohydr Res 16: 189-197.
4. T. Appl Environ Microbiol 72: 3396-3405.
5. Enquist-Newman, M., Faust, A.M.E., Bravo, D.D., Santos, C.N.S., Raisner, R.M., Hanel, A., etal. (2014) Efficient ethanol production from brown macroalgae sugars by a synthetic yeast platform. Nature 505: 239-243.
6. Fiehn, O., Wohlgemuth, G., Scholz, M., Kind, T., Lee, D.Y., Lu, Y., etal. (2008) Quality control for plant metabolomics: reporting MSI-compliant studies. Plant J 53: 691-704.
7. Fong, S., Machajewski, T.D., Mak, C.C., and Wong, C.-H. (2000) Directed evolution of D-2-keto-3-deoxy-6-phosphogluconate aldolase to new variants for the efficient synthesis of D- and L-sugars. Chem Biol 7: 873-883.
8. Gentleman, R.C., Carey, V.J., Bates, D.M., Bolstad, B., Dettling, M., Dudoit, S., etal. (2004) Bioconductor: open software development for computational biology and bioinformatics. Genome Biol 5: R80.
9. Goh, C.S., and Lee, K.T. (2010) A visionary and conceptual macroalgae-based third-generation bioethanol (TGB) biorefinery in Sabah, Malaysia as an underlay for renewable and sustainable development. Renew Sust Energ Rev 14: 842-848.
10. Ha, S.C., Lee, S., Lee, J., Kim, H.T., Ko, H.-J., Kim, K.H., etal. (2012) Crystal structure of a key enzyme in the agarolytic pathway, α-neoagarobiose hydrolase from Saccharophagus degradans 2-40. Biochem Biophys Res Commun 412: 238-244.
11. Ha, S.J., Galazka, J.M., Kim, S.R., Choi, J.H., Yang, X., Seo, J.-H., etal. (2011) Engineered Saccharomyces cerevisiae capable of simultaneous cellobiose and xylose fermentation. Proc Natl Acad Sci USA 108: 504-509.
12. Hasson, M.S., Schlichting, I., Moulai, J., Taylor, K., Barrett, W., Kenyon, G.L., etal. (1998) Evolution of an enzyme active site: the structure of a new crystal form of muconate lactonizing enzyme compared with mandelate racemase and enolase. Proc Natl Acad Sci USA 95: 10396-10401.
13. Heath, J.D., Perkins, J.D., Sharma, B., and Weinstock, G.M. (1992) NotI genomic cleavage map of Escherichia coli K-12 strain MG1655. J Bacteriol 174: 558-567.
14. Hehemann, J.-H., Smyth, L., Yadav, A., Vocadlo, D.J., and Boraston, A.B. (2012) Analysis of keystone enzyme in agar hydrolysis provides insight into the degradation of a polysaccharide from red seaweeds. J Biol Chem 287: 13985-13995.
15. Jeong, H., Tombor, B., Albert, R., Oltvai, Z.N., and Barabasi, A.-L. (2000) The large-scale organization of metabolic networks. Nature 407: 651-654.
16. Kim, C., Ryu, H.J., Kim, S.H., Yoon, J.-J., Kim, H.S., and Kim, Y.J. (2010a) Acidity tunable ionic liquids as catalysts for conversion of agar into mixed sugars. Bull Korean Chem Soc 31: 511-514.
17. Kim, H.T., Lee, S., Lee, D., Kim, H.-S., Bang, W.-G., Kim, K.H., etal. (2010b) Overexpression and molecular characterization of Aga50D from Saccharophagus degradans 2-40: an exo-type β-agarase producing neoagarobiose. Appl Microbiol Biotechnol 86: 227-234.
18. Kim, H.T., Lee, S., Kim, K.H., and Choi, I.-G. (2012) The complete enzymatic saccharification of agarose and its application to simultaneous saccharification and fermentation of agarose for ethanol production. Bioresour Technol 107: 301-306.
19. Kim, N.-J., Li, H., Jung, K., Chang, H.N., and Lee, P.C. (2011) Ethanol production from marine algal hydrolysates using Escherichia coli KO11. Bioresour Technol 102: 7466-7469.
20. Langmead, B., and Salzberg, S.L. (2012) Fast gapped-read alignment with Bowtie 2. Nat Methods 9: 357-359.
21. Lee, C.H., Kim, H.T., Yun, E.J., Lee, A.R., Kim, S.R., Kim, J.-H., etal. (2014) A novel agarolytic β-galactosidase acts on agarooligosaccharides for complete hydrolysis of agarose into monomers. Appl Environ Microbiol 80: 5965-5973.
22. Lee, D.Y., and Fiehn, O. (2008) High quality metabolomic data for Chlamydomonas reinhardtii. Plant Methods 4: 7.
23. Lee, S., Lee, J.Y., Ha, S.C., Jung, J., Shin, D.H., Kim, K.H., etal. (2009) Crystallization and preliminary X-ray analysis of neoagarobiose hydrolase from Saccharophagus degradans 2-40. Acta Crystallogr Sect F Struct Biol Cryst Commun 65: 1299-1301.
24. McCandless, E.L., and Craigie, J.S. (1979) Sulfated polysaccharides in red and brown algae. Annu Rev Plant Physiol Plant Mol Biol 30: 41-53.
25. Michel, G., Nyval-Collen, P., Barbeyron, T., Czjzek, M., and Helbert, W. (2006) Bioconversion of red seaweed galactans: a focus on bacterial agarases and carrageenases. Appl Microbiol Biotechnol 71: 23-33.
26. Morgan, M., Anders, S., Lawrence, M., Aboyoun, P., Pages, H., and Gentleman, R. (2009) ShortRead: a bioconductor package for input, quality assessment and exploration of high-throughput sequence data. Bioinformatics 25: 2607-2608.
27. Morrice, L.M., McLean, M.W., Long, W.F., and Williamson, F.B. (1983) β-Agarase I and II from Pseudmonas atlantica: substrate specificities. Eur J Biochem 137: 149-154.
28. Ohta, K., Beall, D.S., Mejia, J.P., Shanmugam, K.T., and Ingram, L.O. (1991) Genetic improvement of Escherichia coli for ethanol production: chromosomal integration of Zymomonas mobilis genes encoding pyruvate decarboxylase and alcohol dehydrogenase II. Appl Environ Microbiol 57: 893-900.
29. Park, J.-H., Hong, J.-Y., Jang, H.C., Oh, S.G., Kim, S.-H., Yoon, J.-J., etal. (2012) Use of Gelidium amansii as a promising resource for bioethanol: a practical approach for continuous dilute-acid hydrolysis and fermentation. Bioresour Technol 108: 83-88.
30. Roesijadi, G., Jones, S.B., Snowden-Swan, L.J., and Zhu, Y. (2010) Macroalgae as a Biomass Feedstock: A Preliminary Analysis. Technical Report (AC05-76RL01830) for U.S. Department of Energy. Richland, WA, USA: Pacific Northwest National Laboratory.
31. Roh, H., Yun, E.J., Lee, S., Ko, H.-J., Kim, S., Kim, B.-Y., etal. (2012) Genome sequence of Vibrio sp. strain EJY3, an agarolytic marine bacterium metabolizing 3, 6-anhydro-L-galactose as a sole carbon source. J Bacteriol 194: 2773-2774.
32. Shin, M.H., Lee, D.Y., Wohlgemuth, G., Choi, I.-G., Fiehn, O., and Kim, K.H. (2010) Global metabolite profiling of agarose degradation by Saccharophagus degradans 2-40. N Biotechnol 27: 156-168.
33. Solyanikova, I.P., Maltseva, O.V., Vollmer, M.D., Golovleva, L.A., and Schlomann, M. (1995) Characterization of muconate and chloromuconate cycloisomerase from Rhodococcus erythropolis 1CP: indications for functionally convergent evolution among bacterial cycloisomerases. J Bacteriol 177: 2821-2826.
34. Sugano, Y., Kodama, H., Terada, I., Yamazaki, Y., and Noma, M. (1994) Purification and characterization of a novel enzyme, α-neoagrooligosaccharide hydrolase (α-NAOS hydrolase), from a marine bacterium, Vibrio sp. strain JT0107. J Bacteriol 176: 6812-6818.
35. Suzuki, H., Sawai, Y., Suzuki, T., and Kawai, K. (2003) Purification and characterization of an extracellular β-agarase from Bacillus sp. MK03. J Biosci Bioeng 95: 328-334.
36. Szumilo, T. (1981) Pathway for D-galactonate catabolism in non-pathogenic mycobacteria. J Bacteriol 148: 368-370.
37. Takase, R., Ochiai, A., Mikami, B., Hashimoto, W., and Murata, K. (2010) Molecular identification of unsaturated uronate reductase prerequisite for alginate metabolism in Sphingomonas sp. A1. Biochim Biophys Acta 1804: 1925-1936.
38. Takeda, H., Yoneyama, F., Kawai, S., Hashimoto, W., and Murata, K. (2011) Bioethanol production from marine biomass alginate by metabolically engineered bacteria. Energy Environ Sci 4: 2575-2581.
39. Wagner, A., and Fell, D.A. (2001) The small world inside large metabolic networks. Proc R Soc Lond B 268: 1803-1810.
40. Wargacki, A.J., Leonard, E., Win, M.N., Regitsky, D.D., Santos, C.N.S., Kim, P.B., etal. (2012) An engineered microbial platform for direct biofuel production from brown macroalgae. Science 335: 308-313.
41. Wei, N., Quarterman, J., and Jin, Y.-S. (2013) Marine macroalgae: an untapped resource for producing fuels and chemicals. Trends Biotechnol 31: 70-77.
42. Wi, S.G., Kim, H.J., Mahadevan, S.A., Yang, D.-J., and Bae, H.J. (2009) The potential value of the seaweed Ceylon moss (Gelidium amansii) as an alternative bioenergy resource. Bioresour Technol 100: 6658-6660.
43. Wong, T.Y., and Yao, X.T. (1994) The DeLey-Doudoroff pathway of galactose metabolism in Azotobacter vinelandii. Appl Environ Microbiol 60: 2065-2068.
44. Xie, W., Lin, B., Zhou, Z., Lu, G., Lun, J., Xia, C., etal. (2013) Characterization of a novel β-agarase from an agar-degrading bacterium Catenovulum sp. X3. Appl Microbiol Biotechnol 97: 4907-4915.
45. Xu, P., Gu, Q., Wang, W., Wong, L., Bower, A.G.W., Collins, C.H., etal. (2013) Modular optimization of multi-gene pathways for fatty acids production in E.coli. Nat Commun 4: 1409.
46. Yang, B., Yu, G., Zhao, X., Jiao, G., Ren, S., and Chai, W. (2009) Mechanism of mild acid hydrolysis of galactan polysaccharides with highly ordered disaccharide repeats leading to a complete series of exclusively odd-numbered oligosaccharides. FEBS J 276: 2125-2137.
47. Yun, E.J., Lee, S., Kim, J.H., Kim, B.B., Kim, H.T., Lee, S.H., etal. (2013) Enzymatic production of 3, 6-anhydro-L-galactose from agarose and its purification and in vitro skin whitening and anti-inflammatory activities. Appl Microbiol Biotechnol 97: 2961-2970.
48. Zhang, M., Eddy, C., Deanda, K., Finkelstein, M., and Picataggio, S. (1995) Metabolic engineering of pentose phosphate metabolism pathway in ethanologenic Zymomonas mobilis. Science 267: 240-243.