A functional glycogen biosynthesis pathway in Lactobacillus acidophilus: Expression and analysis of the glg operon

Molecular Microbiology

Volumn 89, Issue 6, 2013, Pages 1187-1200

  Goh, Yong Jun ^a   Klaenhammer, Todd R ^a  

^a NORTH CAROLINA STATE UNIVERSITY   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

1,4 ALPHA GLUCAN BRANCHING ENZYME; AMYLASE; GLUCOSE; GLUCOSE 1 PHOSPHATE ADENYLYLTRANSFERASE; GLYCOGEN; GLYCOGEN PHOSPHORYLASE; GLYCOGEN SYNTHASE; PHOSPHOGLUCOMUTASE; RAFFINOSE; THIOREDOXIN REDUCTASE; TREHALOSE;

ALPHA AMYLASE GENE; ARTICLE; BACTERIAL GENE; BACTERIAL GROWTH; BILE; BIOACCUMULATION; CARBON SOURCE; CELL GROWTH; CONTROLLED STUDY; DNA SEQUENCE; EXCINUCLEASE SUBUNIT B GENE; GASTROINTESTINAL SECRETION; GENE CLUSTER; GENE IDENTIFICATION; GENE INACTIVATION; GENE REPRESSION; GLUCOSE 1 PHOSPHATE ADENYLYLTRANSFERASE GENE; GLYCOGEN ANALYSIS; GLYCOGEN BRANCHING ENZYME GENE; GLYCOGEN SYNTHASE GENE; GLYCOGEN SYNTHESIS; LACTOBACILLUS ACIDOPHILUS; NONHUMAN; NUCLEOTIDE SEQUENCE; OPERON; PHENOTYPE; PHOSPHOGLUCOMUTASE GENE; PRIORITY JOURNAL; SENSITIVITY ANALYSIS; SEQUENCE ANALYSIS; THIOREDOXIN REDUCTASE GENE;

LACTOBACILLUS ACIDOPHILUS; PROKARYOTA;

1,4-ALPHA-GLUCAN BRANCHING ENZYME; BILE; BIOSYNTHETIC PATHWAYS; CARBON; ENERGY METABOLISM; GENE DELETION; GENE EXPRESSION REGULATION, BACTERIAL; GLUCOSE; GLYCOGEN; GLYCOGEN PHOSPHORYLASE; GLYCOGEN SYNTHASE; HUMANS; LACTOBACILLUS ACIDOPHILUS; OPERON; RAFFINOSE; TREHALOSE;

EID: 84884281618     PISSN: 0950382X     EISSN: 13652958     Source Type: Journal    
DOI: 10.1111/mmi.12338     Document Type: Article

References (48)

1. Alonso-Casajus, N., Dauvillee, D., Viale, A.M., Munoz, F.J., Baroja-Fernandez, E., Moran-Zorzano, M.T., etal. (2006) Glycogen phosphorylase, the product of the glgP gene, catalyzes glycogen breakdown by removing glucose units from the nonreducing ends in Escherichia coli. J Bacteriol 188: 5266-5272.
2. Altermann, E., Russell, W.M., Azcarate-Peril, M.A., Barrangou, R., Buck, B.L., McAuliffe, O., etal. (2005) Complete genome sequence of the probiotic lactic acid bacterium Lactobacillus acidophilus NCFM. Proc Natl Acad Sci USA 102: 3906-3912.
3. Andersen, J.M., Barrangou, R., Hachem, M.A., Lahtinen, S.J., Goh, Y.J., Svensson, B., and Klaenhammer, T.R. (2012) Transcriptional analysis of prebiotic uptake and catabolism by Lactobacillus acidophilus NCFM. PLoS ONE 7: e44409.
4. Barefoot, S.F., and Klaenhammer, T.R. (1983) Detection and activity of lactacin B, a bacteriocin produced by Lactobacillus acidophilus. Appl Environ Microbiol 45: 1808-1815.
5. Barrangou, R., Azcarate-Peril, M.A., Duong, T., Conners, S.B., Kelly, R.M., and Klaenhammer, T.R. (2006) Global analysis of carbohydrate utilization by Lactobacillus acidophilus using cDNA microarrays. Proc Natl Acad Sci USA 103: 3816-3821.
6. Belanger, A.E., and Hatfull, G.F. (1999) Exponential-phase glycogen recycling is essential for growth of Mycobacterium smegmatis. J Bacteriol 181: 6670-6678.
7. Bonafonte, M.A., Solano, C., Sesma, B., Alvarez, M., Montuenga, L., Garcia-Ros, D., and Gamazo, C. (2000) The relationship between glycogen synthesis, biofilm formation and virulence in Salmonella enteritidis. FEMS Microbiol Lett 191: 31-36.
8. Busuioc, M., Mackiewicz, K., Buttaro, B.A., and Piggot, P.J. (2009) Role of intracellular polysaccharide in persistence of Streptococcus mutans. J Bacteriol 191: 7315-7322.
9. Charteris, W.P., Kelly, P.M., Morelli, L., and Collins, J.K. (1998) Development and application of an in vitro methodology to determine the transit tolerance of potentially probiotic Lactobacillus and Bifidobacterium species in the upper human gastrointestinal tract. J Appl Microbiol 84: 759-768.
10. Dauvillee, D., Kinderf, I.S., Li, Z., Kosar-Hashemi, B., Samuel, M.S., Rampling, L., etal. (2005) Role of the Escherichia coli glgX gene in glycogen metabolism. J Bacteriol 187: 1465-1473.
11. Duong, T., Barrangou, R., Russell, W.M., and Klaenhammer, T.R. (2006) Characterization of the tre locus and analysis of trehalose cryoprotection in Lactobacillus acidophilus NCFM. Appl Environ Microbiol 72: 1218-1225.
12. Eydallin, G., Viale, A.M., Moran-Zorzano, M.T., Munoz, F.J., Montero, M., Baroja-Fernandez, E., and Pozueta-Romero, J. (2007) Genome-wide screening of genes affecting glycogen metabolism in Escherichia coli K-12. FEBS Lett 581: 2947-2953.
13. Eydallin, G., Montero, M., Almagro, G., Sesma, M.T., Viale, A.M., Munoz, F.J., etal. (2010) Genome-wide screening of genes whose enhanced expression affects glycogen accumulation in Escherichia coli. DNA Res 17: 61-71.
14. Felis, G.E., Dellaglio, F., and Torriani, S. (2009) Taxonomy of probiotic microorganisms. In Prebiotics and Probiotics Science and Technology. Charalampopoulos, D., and Rastall, R.A. (eds). New York: Springer, LLC., pp. 591-637.
15. Frece, J., Kos, B., Svetec, I.K., Zgaga, Z., Mrsa, V., and Suskovic, J. (2005) Importance of S-layer proteins in probiotic activity of Lactobacillus acidophilus M92. J Appl Microbiol 98: 285-292.
16. Goh, Y.J., and Klaenhammer, T.R. (2010) Functional roles of aggregation-promoting-like factor in stress tolerance and adherence of Lactobacillus acidophilus NCFM. Appl Environ Microbiol 76: 5005-5012.
17. Goh, Y.J., Zhang, C., Benson, A.K., Schlegel, V., Lee, J.H., and Hutkins, R.W. (2006) Identification of a putative operon involved in fructooligosaccharide utilization by Lactobacillus paracasei. Appl Environ Microbiol 72: 7518-7530.
18. Goh, Y.J., Azcarate-Peril, M.A., O'Flaherty, S., Durmaz, E., Valence, F., Jardin, J., etal. (2009) Development and application of a upp-based counterselective gene replacement system for the study of the S-layer protein SlpX of Lactobacillus acidophilus NCFM. Appl Environ Microbiol 75: 3093-3105.
19. Govons, S., Vinopal, R., Ingraham, J., and Preiss, J. (1969) Isolation of mutants of Escherichia coli B altered in their ability to synthesize glycogen. J Bacteriol 97: 970-972.
20. Horton, R.M., Hunt, H.D., Ho, S.N., Pullen, J.K., and Pease, L.R. (1989) Engineering hybrid genes without the use of restriction enzymes: gene splicing by overlap extension. Gene 77: 61-68.
21. Jones, S.A., Jorgensen, M., Chowdhury, F.Z., Rodgers, R., Hartline, J., Leatham, M., etal. (2008) Glycogen and maltose utilization by Escherichia coli O157:H7 in the mouse intestine. Infect Immun 76: 2531-2540.
22. Kajikawa, A., Zhang, L., Long, J., Nordone, S., Stoeker, L., LaVoy, A., etal. (2012) Construction and immunological evaluation of dual cell surface display of HIV-1 Gag and Salmonella enterica serovar Typhimurium FliC in Lactobacillus acidophilus for vaccine delivery. Clin Vaccine Immunol 19: 1374-1381.
23. Khazaie, K., Zadeh, M., Khan, M.W., Bere, P., Gounari, F., Dennis, K., etal. (2012) Abating colon cancer polyposis by Lactobacillus acidophilus deficient in lipoteichoic acid. Proc Natl Acad Sci USA 109: 10462-10467.
24. Kiel, J.A., Boels, J.M., Beldman, G., and Venema, G. (1994) Glycogen in Bacillus subtilis: molecular characterization of an operon encoding enzymes involved in glycogen biosynthesis and degradation. Mol Microbiol 11: 203-218.
25. Kim, H.S., and Gilliland, S.E. (1983) Lactobacillus acidophilus as a dietary adjunct for milk to aid lactose digestion in humans. J Dairy Sci 66: 959-966.
26. Kimmel, S.A., and Roberts, R.F. (1998) Development of a growth medium suitable for exopolysaccharide production by Lactobacillus delbrueckii ssp. bulgaricus RR. Int J Food Microbiol 40: 87-92.
27. Kingsford, C.L., Ayanbule, K., and Salzberg, S.L. (2007) Rapid, accurate, computational discovery of Rho-independent transcription terminators illuminates their relationship to DNA uptake. Genome Biol 8: R22.
28. Konstantinov, S.R., Smidt, H., de Vos, W.M., Bruijns, S.C., Singh, S.K., Valence, F., etal. (2008) S layer protein A of Lactobacillus acidophilus NCFM regulates immature dendritic cell and T cell functions. Proc Natl Acad Sci USA 105: 19474-19479.
29. Larkin, M.A., Blackshields, G., Brown, N.P., Chenna, R., McGettigan, P.A., McWilliam, H., etal. (2007) Clustal W and Clustal X version 2.0. Bioinformatics 23: 2947-2948.
30. Law, J., Buist, G., Haandrikman, A., Kok, J., Venema, G., and Leenhouts, K. (1995) A system to generate chromosomal mutations in Lactococcus lactis which allows fast analysis of targeted genes. J Bacteriol 177: 7011-7018.
31. Leyer, G.J., Li, S., Mubasher, M.E., Reifer, C., and Ouwehand, A.C. (2009) Probiotic effects on cold and influenza-like symptom incidence and duration in children. Pediatrics 124: e172-e179.
32. Mohamadzadeh, M., Duong, T., Sandwick, S.J., Hoover, T., and Klaenhammer, T.R. (2009) Dendritic cell targeting of Bacillus anthracis protective antigen expressed by Lactobacillus acidophilus protects mice from lethal challenge. Proc Natl Acad Sci USA 106: 4331-4336.
33. Mohamadzadeh, M., Pfeiler, E.A., Brown, J.B., Zadeh, M., Gramarossa, M., Managlia, E., etal. (2011) Regulation of induced colonic inflammation by Lactobacillus acidophilus deficient in lipoteichoic acid. Proc Natl Acad Sci USA 108 (Suppl. 1): 4623-4630.
34. Moreno-Bruna, B., Baroja-Fernandez, E., Munoz, F.J., Bastarrica-Berasategui, A., Zandueta-Criado, A., Rodriguez-Lopez, M., etal. (2001) Adenosine diphosphate sugar pyrophosphatase prevents glycogen biosynthesis in Escherichia coli. Proc Natl Acad Sci USA 98: 8128-8132.
35. Parrou, J.L., and Francois, J. (1997) A simplified procedure for a rapid and reliable assay of both glycogen and trehalose in whole yeast cells. Anal Biochem 248: 186-188.
36. Pfeiler, E.A., and Klaenhammer, T.R. (2009) Role of transporter proteins in bile tolerance of Lactobacillus acidophilus. Appl Environ Microbiol 75: 6013-6016.
37. Preiss, J. (1984) Bacterial glycogen synthesis and its regulation. Annu Rev Microbiol 38: 419-458.
38. Rousseaux, C., Thuru, X., Gelot, A., Barnich, N., Neut, C., Dubuquoy, L., etal. (2007) Lactobacillus acidophilus modulates intestinal pain and induces opioid and cannabinoid receptors. Nat Med 13: 35-37.
39. Sambou, T., Dinadayala, P., Stadthagen, G., Barilone, N., Bordat, Y., Constant, P., etal. (2008) Capsular glucan and intracellular glycogen of Mycobacterium tuberculosis: biosynthesis and impact on the persistence in mice. Mol Microbiol 70: 762-774.
40. Sanders, M.E., and Klaenhammer, T.R. (2001) Invited review: the scientific basis of Lactobacillus acidophilus NCFM functionality as a probiotic. J Dairy Sci 84: 319-331.
41. Seibold, G., Dempf, S., Schreiner, J., and Eikmanns, B.J. (2007) Glycogen formation in Corynebacterium glutamicum and role of ADP-glucose pyrophosphorylase. Microbiology 153: 1275-1285.
42. Seibold, G.M., and Eikmanns, B.J. (2007) The glgX gene product of Corynebacterium glutamicum is required for glycogen degradation and for fast adaptation to hyperosmotic stress. Microbiology 153: 2212-2220.
43. Shim, J.H., Park, J.T., Hong, J.S., Kim, K.W., Kim, M.J., Auh, J.H., etal. (2009) Role of maltogenic amylase and pullulanase in maltodextrin and glycogen metabolism of Bacillus subtilis 168. J Bacteriol 191: 4835-4844.
44. Spatafora, G., Rohrer, K., Barnard, D., and Michalek, S. (1995) A Streptococcus mutans mutant that synthesizes elevated levels of intracellular polysaccharide is hypercariogenic in vivo. Infect Immun 63: 2556-2563.
45. Tamura, K., Peterson, D., Peterson, N., Stecher, G., Nei, M., and Kumar, S. (2011) MEGA5: molecular evolutionary genetics analysis using maximum likelihood, evolutionary distance, and maximum parsimony methods. Mol Biol Evol 28: 2731-2739.
46. Tompkins, T.A., Barreau, G., and Broadbent, J.R. (2012) Complete genome sequence of Lactobacillus helveticus R0052, a commercial probiotic strain. J Bacteriol 194: 6349.
47. Tzvetkov, M., Klopprogge, C., Zelder, O., and Liebl, W. (2003) Genetic dissection of trehalose biosynthesis in Corynebacterium glutamicum: inactivation of trehalose production leads to impaired growth and an altered cell wall lipid composition. Microbiology 149: 1659-1673.
48. Wang, L., and Wise, M.J. (2011) Glycogen with short average chain length enhances bacterial durability. Naturwissenschaften 98: 719-729.