Metabolic pathway of 3,6-anhydro-d-galactose in carrageenan-degrading microorganisms
Abstract
Complete hydrolysis of κ-carrageenan produces two sugars, D-galactose and 3,6-anhydro-D-galactose (D-AnG). At present, however, we do not know how carrageenan-degrading microorganisms metabolize D-AnG. In this study, we investigated the metabolic pathway of D-AnG degradation by comparative genomic analysis of Cellulophaga lytica LIM-21, Pseudoalteromonas atlantica T6c, and Epulopiscium sp. N.t. morphotype B, which represent the classes Flavobacteria, Gammaproteobacteria, and Clostridia, respectively. In this bioinformatic analysis, we found candidate common genes that were believed to be involved in D-AnG metabolism. We then experimentally confirmed the enzymatic function of each gene product in the D-AnG cluster. In all three microorganisms, D-AnG metabolizing genes were clustered and organized in operon-like arrangements, which we named as the dan operon (3,6-d-anhydro-galactose). Combining bioinformatic analysis and experimental data, we showed that D-AnG is metabolized to pyruvate and D-glyceraldehyde-3-phosphate via four enzyme-catalyzed reactions in the following route: 3,6-anhydro-D-galactose → 3,6-anhydro-D-galactonate → 2-keto-3-deoxy-D-galactonate (D-KDGal) → 2-keto-3-deoxy-6-phospho-D-galactonate → pyruvate + D-glyceraldehyde-3-phosphate. The pathway of D-AnG degradation is composed of two parts: transformation of D-AnG to D-KDGal using two D-AnG specific enzymes and breakdown of D-KDGal to two glycolysis intermediates using two DeLey-Doudoroff pathway enzymes. To our knowledge, this is the first report on the metabolic pathway of D-AnG degradation.
Integrity signals
Registry
Cites
Statistics
Claims the paper makes
Claims other papers make about this one
Each is checked against this paper’s own text: does it say what the citing paper says it does?
The enzymatic hydrolysis of agarose and carrageenan produces the non-fermentable sugars l-AnG and d-AnG, respectively.
“In addition to galactose, the enzymatic hydrolysis of agarose and carrageenan produces the non-fermentable sugars, 3,6-anhydrol-galactose (l-AnG) and 3,6-anhydro-d-galactose (d-AnG), respectively.”
From The Enzymatic Conversion of Major Algal and Cyanobacterial Carbohydrates to Bioethanol (2016) · cites this paper as Lee et al., 2016
Metabolic pathways for l-AnG and d-AnG are only common in agar- and carrageenan-degrading microorganisms, where they are converted to d-KDPGal through six and four enzyme-catalyzed reactions, respectively.
“Metabolic pathways for l-AnG and d-AnG are only common in agar-and carrageenan-degrading microorganisms.In these organisms, l-AnG and d-AnG are converted to 2-keto-3-deoxy-6-phospho-d-galactonate (d-KDPGal) through six and four enzyme-catalyzed reactions, respectively [see Figure 5 in Lee et al. (2014Lee et al. ( , 2016))].”
From The Enzymatic Conversion of Major Algal and Cyanobacterial Carbohydrates to Bioethanol (2016) · cites this paper as Lee et al., 2016
Cites
Molecular Cloning: A Laboratory Manual
Sambrook, J., Fritsch, E., & Maniatis, T. (1989) · UCLA - Biblioteca de Ciencias de la Salud · Cited by 133,589 · see citing works
Molecular cloning: A laboratory manual
Deininger, P. L. (1990) · Analytical Biochemistry · doi:10.1016/0003-2697(90)90595-z · Cited by 84,684 · see citing works
GLUCOSE AND GLUCONIC ACID OXIDATION OF PSEUDOMONAS SACCHAROPHILA
Entner, N., & Doudoroff, M. (1952) · Journal of Biological Chemistry · doi:10.1016/s0021-9258(19)52415-2 · Cited by 434 · see citing works
How Well is Enzyme Function Conserved as a Function of Pairwise Sequence Identity?
Tian, W., & Skolnick, J. (2003) · Journal of Molecular Biology · doi:10.1016/j.jmb.2003.08.057 · Cited by 434 · see citing works
Wilson, C. A., Kreychman, J., & Gerstein, M. (2000) · Journal of Molecular Biology · doi:10.1006/jmbi.2000.3550 · Cited by 367 · see citing works
Bioethanol production from Gracilaria verrucosa, a red alga, in a biorefinery approach
Kumar, S., Gupta, R., Kumar, G., Sahoo, D., & Kuhad, R. C. (2013) · Bioresource Technology · doi:10.1016/j.biortech.2012.10.120 · Cited by 319 · see citing works
(1991) · Choice Reviews Online · doi:10.5860/choice.28-6255 · Cited by 305 · see citing works
Skoza, L., & Mohos, S. C. (1976) · Biochemical Journal · doi:10.1042/bj1590457 · Cited by 267 · see citing works
Park, J., Hong, J.-Y., Jang, H. C., Oh, S. G., Kim, S., Yoon, J., & Kim, Y. J. (2011) · Bioresource Technology · doi:10.1016/j.biortech.2011.12.065 · Cited by 235 · see citing works
THE METABOLISM OF d-GALACTOSE IN PSEUDOMONAS SACCHAROPHILA
Ley, J. D., & Doudoroff, M. (1957) · Journal of Biological Chemistry · doi:10.1016/s0021-9258(18)70755-2 · Cited by 188 · see citing works
Carrageenan catabolism is encoded by a complex regulon in marine heterotrophic bacteria
Ficko‐Blean, E., Préchoux, A., Thomas, F., Rochat, T., Larocque, R., Zhu, Y., Stam, M. R., Genicot, S. M., Jam, M., Calteau, A., et al. (2017) · Nature Communications · doi:10.1038/s41467-017-01832-6 · Cited by 178 · see citing works
Meinita, M. D. N., Kang, J.-Y., Jeong, G., Koo, H. M., Park, S. M., & Hong, Y. (2011) · Journal of Applied Phycology · doi:10.1007/s10811-011-9705-0 · Cited by 150 · see citing works
A Functionally Diverse Enzyme Superfamily that Abstracts the α Protons of Carboxylic Acids
Babbitt, P. C., Mrachko, G. T., Hasson, M. S., et al. (1995) · Science · doi:10.1126/science.7855594 · Cited by 140 · see citing works
Johansen, J. E., Nielsen, P., & Sjøholm, C. (1999) · INTERNATIONAL JOURNAL OF SYSTEMATIC AND EVOLUTIONARY MICROBIOLOGY · doi:10.1099/00207713-49-3-1231 · Cited by 140 · see citing works
Buchanan, C. L., Connaris, H., Danson, M. J., et al. (1999) · Biochemical Journal · doi:10.1042/bj3430563 · Cited by 124 · see citing works
Meinita, M. D. N., Marhaeni, B., Winanto, T., Jeong, G., Khan, M. N. A., & Hong, Y. (2013) · Journal of Applied Phycology · doi:10.1007/s10811-013-0041-4 · Cited by 106 · see citing works
Production of ethanol 3G from Kappaphycus alvarezii: Evaluation of different process strategies
Hargreaves, P. I., Barcelos, C. A., da Costa, A. C. A., et al. (2013) · Bioresource Technology · doi:10.1016/j.biortech.2013.02.002 · Cited by 97 · see citing works
Yun, E. J., Lee, S., Kim, H. T., Pelton, J. G., Kim, S., Ko, H., Choi, I., & Kim, K. H. (2014) · Environmental Microbiology · doi:10.1111/1462-2920.12607 · Cited by 89 · see citing works
Self-citationKim, S., & Lee, S. B. (2005) · Biochemical Journal · doi:10.1042/bj20041053 · Cited by 82 · see citing works
Self-citationYaphe, W. (1957) · Canadian Journal of Microbiology · doi:10.1139/m57-109 · Cited by 78 · see citing works
Derivatives of 4-O-β-D-Galactopyranosyl-3,6-anhydro-D-galactose from κ-Carrageenin1
O'Neill, A. N. (1955) · Journal of the American Chemical Society · doi:10.1021/ja01628a074 · Cited by 74 · see citing works
Mutripah, S., Meinita, M. D. N., Kang, J.-Y., Jeong, G., Susanto, A., Prabowo, R. E., & Hong, Y. (2013) · Journal of Applied Phycology · doi:10.1007/s10811-013-0068-6 · Cited by 65 · see citing works
Thin-layer chromatographic analysis of enzymic hydrolysates of agar
Duckworth, M., & Yaphe, W. (1970) · Journal of Chromatography A · doi:10.1016/s0021-9673(00)93663-x · Cited by 64 · see citing works
Hwang, H. J., Lee, S. Y., Kim, S. M., & Lee, S. B. (2011) · Biotechnology and Bioprocess Engineering · doi:10.1007/s12257-011-0278-1 · Cited by 62 · see citing works
Self-citation3,6-Anhydro-D-galactose as a Constituent of κ-Carrageenin1
O'Neill, A. N. (1955) · Journal of the American Chemical Society · doi:10.1021/ja01615a050 · Cited by 60 · see citing works
115. The properties of 3 : 6-anhydrogalactose
Haworth, W. N., Jackson, J. E., & Smith, F. (1940) · Journal of the Chemical Society (Resumed) · doi:10.1039/jr9400000620 · Cited by 48 · see citing works
Kim, S., & Lee, S. B. (2006) · Bioscience Biotechnology and Biochemistry · doi:10.1271/bbb.50566 · Cited by 41 · see citing works
Self-citationThe utilisation of d-galactonate and d-2-oxo-3-deoxygalactonate by Escherichia coli K-12
Cooper, R. A. (1978) · Archives of Microbiology · doi:10.1007/bf00415730 · Cited by 38 · see citing works
Andberg, M. B., Maaheimo, H., Boer, H., et al. (2012) · Journal of Biological Chemistry · doi:10.1074/jbc.m111.335240 · Cited by 32 · see citing works
Metabolic pathway of 3,6-anhydro-l-galactose in agar-degrading microorganisms
Lee, S. B., Cho, S. J., Kim, J. A., Lee, S. Y., Kim, S. M., & Lim, H. S. (2014) · Biotechnology and Bioprocess Engineering · doi:10.1007/s12257-014-0622-3 · Cited by 28 · see citing works
Self-citationCharacterization and crystal structure of Escherichia coli KDPGal aldolase
Walters, M. J., Velupillai, S., McEwan, A. R., et al. (2007) · Bioorganic & Medicinal Chemistry · doi:10.1016/j.bmc.2007.10.043 · Cited by 26 · see citing works
Jung, J. H., & Lee, S. B. (2006) · Biochemical Journal · doi:10.1042/bj20051763 · Cited by 23 · see citing works
Self-citationMiller, D. A., Suen, G., Clements, K. D., et al. (2012) · BMC Genomics · doi:10.1186/1471-2164-13-265 · Cited by 22 · see citing works
Kim, S. M., Paek, K. H., & Lee, S. B. (2012) · Extremophiles · doi:10.1007/s00792-012-0444-1 · Cited by 19 · see citing works
Self-citationDucatti, D. R. B., Massi, A., Noseda, M. D., Duarte, M. E. R., & Dondoni, A. (2008) · Organic & Biomolecular Chemistry · doi:10.1039/b816606d · Cited by 19 · see citing works
Jung, J. H., & Lee, S. B. (2005) · Biotechnology and Bioprocess Engineering · doi:10.1007/bf02932290 · Cited by 16 · see citing works
Self-citationNoh, M., Jung, J. H., & Lee, S. B. (2006) · Biotechnology and Bioprocess Engineering · doi:10.1007/bf03026251 · Cited by 15 · see citing works
Self-citationKim, S., & Lee, S. B. (2008) · Biotechnology and Bioprocess Engineering · doi:10.1007/s12257-008-0152-y · Cited by 14 · see citing works
Self-citationBae, J., Kim, S. M., & Lee, S. B. (2015) · Extremophiles · doi:10.1007/s00792-015-0731-8 · Cited by 14 · see citing works
Self-citationPostechiella marina gen. nov., sp. nov., isolated from seawater
Lee, D.-H., Cho, S. J., Kim, S. M., et al. (2011) · INTERNATIONAL JOURNAL OF SYSTEMATIC AND EVOLUTIONARY MICROBIOLOGY · doi:10.1099/ijs.0.031302-0 · Cited by 13 · see citing works
Structure of 2-oxo-3-deoxygalactonate kinase fromKlebsiella pneumoniae
Michalska, K., Cuff, M. E., Tesar, C., et al. (2011) · Acta Crystallographica Section D Biological Crystallography · doi:10.1107/s0907444911021834 · Cited by 6 · see citing works
Cho, S. J., & Lee, S. B. (2014) · Biotechnology and Bioprocess Engineering · doi:10.1007/s12257-014-0830-x · Cited by 5 · see citing works
Self-citationCho, S. J., Kim, J. A., & Lee, S. B. (2015) · Biotechnology and Bioprocess Engineering · doi:10.1007/s12257-015-0359-7 · Cited by 4 · see citing works
Self-citationLee, S. B. (2015) · Biotechnology and Bioprocess Engineering · doi:10.1007/s12257-015-0440-2 · Cited by 2 · see citing works
Self-citationAldehydic nature and conformation of 3,6-anhydro-L-galactose monomer
Lee, S. B., Lee, S. Y., Lee, S. Y., et al. (2015) · Biotechnology and Bioprocess Engineering · doi:10.1007/s12257-015-0520-3 · Cited by 2 · see citing works
Self-citation
Flagged first, then by citations
Cited by
Sorted by citations
The Enzymatic Conversion of Major Algal and Cyanobacterial Carbohydrates to Bioethanol
Al Abdallah, Q., Nixon, B. T., & Fortwendel, J. R. (2016) · Frontiers in Energy Research · doi:10.3389/fenrg.2016.00036 · Cited by 102 · see citing works
- Authors
- Lee, S. B., Kim, J. A., & Lim, H. S.
- Affiliations
- Pohang University of Science and Technology (KR)
- Corresponding author
- Lee, Sun Bok
- ORCID
- Kim, Jeong Ah
- Venue
- Applied Microbiology and Biotechnology
- Published
- 2016-02-15
- Volume
- 100
- Issue
- 9
- Pages
- 4109-4121
- ISSN
- 0175-7598 (ISSN-L)
- 1432-0614
- OpenAlex
- W2275029241
- Cited by
- 22
- References
- 45
- Citations by year
- 2024: 4 · 2022: 4 · 2021: 1 · 2020: 2 · 2019: 1 · 2018: 5 · 2017: 2 · 2016: 3
- FWCI
- 3.20
- Type
- journal article
- Language
- en
- Open access
- closed
- Licence
- www.springer.com/tdm (tdm)
- Locations
- Applied Microbiology and Biotechnology (publishedVersion)
- PubMed (publishedVersion)
- Open Access System for Information Sharing (Pohang University of Science and Technology) (submittedVersion)
- Funders
- POSCO
- Korea Institute for Advancement of Technology (2015 Establishment of GEM, No. H2001-13-1001)
- Topics
- Life Sciences › Biochemistry, Genetics and Molecular Biology › Biotechnology › Enzyme Production and Characterization
- Life Sciences › Biochemistry, Genetics and Molecular Biology › Molecular Biology › Genomics and Phylogenetic Studies
- Life Sciences › Agricultural and Biological Sciences › Plant Science › Polysaccharides and Plant Cell Walls
- Keywords
- carrageenan degradation, Cellulophaga lytica, Pseudoalteromonas atlantica, pyruvate, D-glyceraldehyde-3-phosphate, carbohydrate catabolism, operon organization
- MeSH terms
- Clostridiales, Eubacteriales, Biotransformation, Carrageenan, Galactose, Multigene Family, Glyceraldehyde 3-Phosphate, Operon, Pyruvic Acid, Computational Biology, Pseudoalteromonas, Flavobacteriaceae, Metabolic Networks and Pathways
About these checks
Registry, retraction, Cites and statistics results are computed, not judged, with one exception: a printed reference that no index lists is read once by a model before it counts as a citation error. Claims are extracted by a model and kept only when their quote appears verbatim in the text; each cited source is then checked, with a model’s help, for whether it says what the claim relies on. Those verdicts can be wrong — read the claim’s quote and the cited source before relying on one.
Statistics and arithmetic are recomputed, not judged.
Confidence bands are shown only for fields calibrated on our annotated test set. None is calibrated yet, so no band is shown.
What counts as a claim ›How we measure confidence ›How we check this ›
Are you an author, or do you see a problem with this page? Request a review