N-acetylgalactosamine utilization pathway and regulon in proteobacteria: Genomic reconstruction and experimental characterization in Shewanella

Journal of Biological Chemistry

Volumn 287, Issue 33, 2012, Pages 28047-28056

  Leyn, Semen A ^a,b   Gao, Fang ^c   Yang, Chen ^c   Rodionov, Dmitry A ^a,b  

^a BURNHAM INSTITUTE   (United States)

^b INSTITUTE FOR INFORMATION TRANSMISSION PROBLEMS   (Russian Federation)

^c Shanghai Jiao Tong University Affiliated Sixth People s Hospital   (China)

Author keywords

[No Author keywords available]

Indexed keywords

CATABOLIC ENZYMES; COMPARATIVE GENOMICS; DEACETYLASE; DEACETYLATION; ENZYMATIC ASSAY; EXPERIMENTAL CHARACTERIZATION; GENETIC TECHNIQUES; IN-VITRO; N-ACETYL-D-GALACTOSAMINE; PROTEOBACTERIA; REGULATORY REGIONS; SHEWANELLA; SHEWANELLA SP; SUGAR TRANSPORT;

ACETYLATION; ALGAE; BIOINFORMATICS; ENZYMES; ESCHERICHIA COLI; PHOSPHORYLATION; POLYSACCHARIDES;

GENES;

BACTERIAL ENZYME; GALACTOSAMINE; N ACETYLGALACTOSAMINE; PROTEIN AGAA; PROTEIN AGAK; PROTEIN AGAS; PROTEIN AGAY; PROTEIN AGAZ; UNCLASSIFIED DRUG;

AGAI GENE; AGAK GENE; AGAS GENE; ARTICLE; BACTERIAL GENE; BIOINFORMATICS; CATABOLISM; DEACETYLATION; DNA BINDING MOTIF; ENZYME ASSAY; ENZYME RECONSTITUTION; ESCHERICHIA COLI; EXPERIMENTAL STUDY; FUNCTIONAL GENOMICS; GENE FUNCTION; GLUCOSE UTILIZATION; IN VITRO STUDY; METABOLIC REGULATION; NONHUMAN; PHOSPHORYLATION; PRIORITY JOURNAL; PROTEIN FUNCTION; PROTEOBACTERIA; REGULON; SEQUENCE HOMOLOGY; SHEWANELLA; SUGAR TRANSPORT; TRANSCRIPTION REGULATION;

ACETYLGALACTOSAMINE; BIOLOGICAL TRANSPORT, ACTIVE; CARBOXYLIC ESTER HYDROLASES; ESCHERICHIA COLI K12; GENE EXPRESSION REGULATION, BACTERIAL; GENE EXPRESSION REGULATION, ENZYMOLOGIC; REGULON; REPRESSOR PROTEINS; SHEWANELLA;

EID: 84864976363     PISSN: 00219258     EISSN: 1083351X     Source Type: Journal    
DOI: 10.1074/jbc.M112.382333     Document Type: Article

References (38)

1. Freymond, P. P., Lazarevic, V., Soldo, B., and Karamata, D. (2006) Poly(glucosyl-N-acetylgalactosamine 1-phosphate), a wall teichoic acid of Bacillus subtilis 168: its biosynthetic pathway and mode of attachment to peptidoglycan. Microbiology 152, 1709-1718
2. Bernatchez, S., Szymanski, C. M., Ishiyama, N., Li, J., Jarrell, H. C., Lau, P. C., Berghuis, A. M., Young, N. M., and Wakarchuk, W. W. (2005) A single bifunctional UDP-GlcNAc/Glc 4-epimerase supports the synthesis of three cell surface glycoconjugates in Campylobacter jejuni. J. Biol. Chem. 280, 4792-4802
3. Carraway, K. L., and Hull, S. R. (1991) Cell surface mucin-type glycoproteins and mucin-like domains. Glycobiology 1, 131-138
4. Abu-Qarn, M., Eichler, J., and Sharon, N. (2008) Not just for Eukarya anymore: protein glycosylation in Bacteria and Archaea. Curr. Opin. Struct. Biol. 18, 544-550
5. Barr, J., and Nordin, P. (1980) Biosynthesis of glycoproteins by membranes of Acer pseudoplatanus: incorporation of mannose and N-acetylglucosamine. Biochem. J. 192, 569-577
6. Davis, C. G., Elhammer, A., Russell, D. W., Schneider, W. J., Kornfeld, S., Brown, M. S., and Goldstein, J. L. (1986) Deletion of clustered O-linked carbohydrates does not impair function of low density lipoprotein receptor in transfected fibroblasts. J. Biol. Chem. 261, 2828-2838
7. Sadler, J. E., Paulson, J. C., and Hill, R. L. (1979) The role of sialic acid in the expression of human MN blood group antigens. J. Biol. Chem. 254, 2112-2119
8. Reizer, J., Ramseier, T. M., Reizer, A., Charbit, A., and Saier, M. H., Jr. (1996) Novel phosphotransferase genes revealed by bacterial genome sequencing: a gene cluster encoding a putative N-acetylgalactosamine metabolic pathway in Escherichia coli. Microbiology 142, 231-250
9. Brinkkötter, A., Klöss, H., Alpert, C., and Lengeler, J. W. (2000) Pathways for the utilization of N-acetylgalactosamine and galactosamine in Escherichia coli. Mol. Microbiol. 37, 125-135
10. Nobelmann, B., and Lengeler, J. W. (1996) Molecular analysis of the gat genes from Escherichia coli and of their roles in galactitol transport and metabolism. J. Bacteriol. 178, 6790-6795
11. Brinkkötter, A., Shakeri-Garakani, A., and Lengeler, J. W. (2002) Two class II mD-tagatose-bisphosphate aldolases from enteric bacteria. Arch. Microbiol. 177, 410-419
12. Ray, W. K., and Larson, T. J. (2004) Application of AgaR repressor and dominant repressor variants for verification of a gene cluster involved in N-acetylgalactosamine metabolism in Escherichia coli K-12. Mol. Microbiol. 51, 813-826
13. Rodionov, D. A., Yang, C., Li, X., Rodionova, I. A., Wang, Y., Obraztsova, A. Y., Zagnitko, O. P., Overbeek, R., Romine, M. F., Reed, S., Fredrickson, J. K., Nealson, K. H., and Osterman, A. L. (2010) Genomic encyclopedia of sugar utilization pathways in the Shewanella genus. BMC Genomics 11, 494
14. Dehal, P. S., Joachimiak, M. P., Price, M. N., Bates, J. T., Baumohl, J. K., Chivian, D., Friedland, G. D., Huang, K. H., Keller, K., Novichkov, P. S., Dubchak, I. L., Alm, E. J., and Arkin, A. P. (2010) MicrobesOnline: an integrated portal for comparative and functional genomics. Nucleic Acids Res. 38, D396-400
15. Altschul, S. F., Madden, T. L., Schäffer, A. A., Zhang, J., Zhang, Z., Miller, W., and Lipman, D. J. (1997) Gapped BLAST and PSI-BLAST: a new generation of protein database search programs. Nucleic Acids Res. 25, 3389-3402
16. Overbeek, R., Begley, T., Butler, R. M., Choudhuri, J. V., Chuang, H. Y., Cohoon, M., de Crécy-Lagard, V., Diaz, N., Disz, T., Edwards, R., Fonstein, M., Frank, E. D., Gerdes, S., Glass, E. M., Goesmann, A., Hanson, A., Iwata-Reuyl, D., Jensen, R., Jamshidi, N., Krause, L., Kubal, M., Larsen, N., Linke, B., McHardy, A. C., Meyer, F., Neuweger, H., Olsen, G., Olson, R., Osterman, A., Portnoy, V., Pusch, G. D., Rodionov, D. A., Rückert, C., Steiner, J., Stevens, R., Thiele, I., Vassieva, O., Ye, Y., Zagnitko, O., and Vonstein, V. (2005) The subsystems approach to genome annotation and its use in the project to annotate 1000 genomes. Nucleic Acids Res. 33, 5691-5702
17. Saier, M. H., Jr., Yen, M. R., Noto, K., Tamang, D. G., and Elkan, C. (2009) The Transporter Classification Database: recent advances. Nucleic Acids Res. 37, D274-278
18. Cantarel, B. L., Coutinho, P. M., Rancurel, C., Bernard, T., Lombard, V., and Henrissat, B. (2009) The Carbohydrate-Active EnZymes database (CAZy): an expert resource for glycogenomics. Nucleic Acids Res. 37, D233-238
19. Punta, M., Coggill, P. C., Eberhardt, R. Y., Mistry, J., Tate, J., Boursnell, C., Pang, N., Forslund, K., Ceric, G., Clements, J., Heger, A., Holm, L., Sonnhammer, E. L., Eddy, S. R., Bateman, A., and Finn, R. D. (2012) The Pfam protein families database. Nucleic Acids Res. 40, D290-301
20. Edgar, R. C. (2004) MUSCLE: a multiple sequence alignment method with reduced time and space complexity. BMC Bioinformatics 5, 113
21. Felsenstein, J. (1996) Inferring phylogenies from protein sequences by parsimony, distance, and likelihood methods. Methods Enzymol. 266, 418-427
22. Huson, D. H., Richter, D. C., Rausch, C., Dezulian, T., Franz, M., and Rupp, R. (2007) Dendroscope: an interactive viewer for large phylogenetic trees. BMC Bioinformatics 8, 460
23. Petersen, T. N., Brunak, S., von Heijne, G., and Nielsen, H. (2011) SignalP 4.0: discriminating signal peptides from transmembrane regions. Nat. Methods 8, 785-786
24. Rodionov, D. A. (2007) Comparative genomic reconstruction of transcriptional regulatory networks in bacteria. Chem. Rev. 107, 3467-3497
25. Novichkov, P. S., Rodionov, D. A., Stavrovskaya, E. D., Novichkova, E. S., Kazakov, A. E., Gelfand, M. S., Arkin, A. P., Mironov, A. A., and Dubchak, I. (2010) RegPredict: an integrated system for regulon inference in prokaryotes by comparative genomics approach. Nucleic Acids Res. 38, W299-307
26. Crooks, G. E., Hon, G., Chandonia, J. M., and Brenner, S. E. (2004) WebLogo: a sequence logo generator. Genome Res. 14, 1188-1190
27. Novichkov, P. S., Laikova, O. N., Novichkova, E. S., Gelfand, M. S., Arkin, A. P., Dubchak, I., and Rodionov, D. A. (2010) RegPrecise: a database of curated genomic inferences of transcriptional regulatory interactions in prokaryotes. Nucleic Acids Res. 38, D111-118
28. Pinchuk, G. E., Ammons, C., Culley, D. E., Li, S. M., McLean, J. S., Romine, M. F., Nealson, K. H., Fredrickson, J. K., and Beliaev, A. S. (2008) Utilization of DNA as a sole source of phosphorus, carbon, and energy by Shewanella spp.: ecological and physiological implications for dissimilatory metal reduction. Appl. Environ. Microbiol. 74, 1198-1208
29. Sambrook, J., Russell, D. W. (2001) Molecular Cloning: A Laboratory Manual, Cold Spring Harbor Laboratory, Cold Spring Harbor, NY
30. Datsenko, K. A., and Wanner, B. L. (2000) One-step inactivation of chromosomal genes in Escherichia coli K-12 using PCR products. Proc. Natl. Acad. Sci. U.S.A. 97, 6640-6645
31. Yang, C., Rodionov, D. A., Rodionova, I. A., Li, X., and Osterman, A. L. (2008) Glycerate 2-kinase of Thermotoga maritima and genomic reconstruction of related metabolic pathways. J. Bacteriol. 190, 1773-1782
32. Reissig, J. L. (1956) Phosphoacetylglucosamine mutase of Neurospora. J. Biol. Chem. 219, 753-767
33. Osterman, A., and Overbeek, R. (2003) Missing genes in metabolic pathways: a comparative genomics approach. Curr. Opin. Chem. Biol. 7, 238-251
34. Qin, Z. S., McCue, L. A., Thompson, W., Mayerhofer, L., Lawrence, C. E., and Liu, J. S. (2003) Identification of co-regulated genes through Bayesian clustering of predicted regulatory-binding sites. Nat. Biotechnol. 21, 435-439
35. Mukherjee, A., Mammel, M. K., LeClerc, J. E., and Cebula, T. A. (2008) Altered utilization of N-acetyl-mD-galactosamine by Escherichia coli O157:H7 from the 2006 spinach outbreak. J. Bacteriol. 190, 1710-1717
36. Yang, C., Rodionov, D. A., Li, X., Laikova, O. N., Gelfand, M. S., Zagnitko, O. P., Romine, M. F., Obraztsova, A. Y., Nealson, K. H., and Osterman, A. L. (2006) Comparative genomics and experimental characterization of N-acetylglucosamine utilization pathway of Shewanella oneidensis. J. Biol. Chem. 281, 29872-29885
37. Liu, Q. P., Sulzenbacher, G., Yuan, H., Bennett, E. P., Pietz, G., Saunders, K., Spence, J., Nudelman, E., Levery, S. B., White, T., Neveu, J. M., Lane, W. S., Bourne, Y., Olsson, M. L., Henrissat, B., and Clausen, H. (2007) Bacterial glycosidases for the production of universal red blood cells. Nat. Biotechnol. 25, 454-464
38. Rosey, E. L., Oskouian, B., and Stewart, G. C. (1991) Lactose metabolism by Staphylococcus aureus: characterization of lacABCD, the structural genes of the tagatose 6-phosphate pathway. J. Bacteriol. 173, 5992-5998