Intraspecific and interspecific interactions among proteins regulating exopolysaccharide synthesis in streptococcus thermophilus, streptococcus iniae, and lactococcus lactis subsp. cremoris and the assessment of potential lateral gene transfer

Canadian Journal of Microbiology

Volumn 57, Issue 12, 2011, Pages 1002-1015

  Cefalo, Angela D ^a   Broadbent, Jeffery R ^b   Welker, Dennis L ^a  

^a UTAH STATE UNIVERSITY   (United States)

^b Dietetics and Food Sciences ^*  (United States)

Author keywords

Exopolysaccharide biosynthesis; Interspecific protein protein interactions; Lactic acid bacteria; Lactobacillales; Tyrosine kinase phosphatase regulatory system

Indexed keywords

EXOPOLYSACCHARIDES; GENETIC EXCHANGE; INDUSTRIAL USE; INTERSPECIFIC INTERACTIONS; INTRA-SPECIFIC INTERACTIONS; LACTIC ACID BACTERIA; LACTOBACILLALES; LACTOCOCCUS LACTIS SUBSP. CREMORIS; NATURALLY OCCURRING; PHOSPHOTYROSINE; PROTEIN INTERACTION; PROTEIN TYROSINE KINASE; PROTEIN-PROTEIN INTERACTIONS; REGULATORY COMPLEXES; REGULATORY SYSTEMS; SEQUENCE COMPARISONS; STREPTOCOCCUS THERMOPHILUS; TRANSMEMBRANES; TYROSINE KINASE; YEAST TWO-HYBRID SYSTEM;

AMINO ACIDS; BIOCHEMISTRY; ENZYME INHIBITION; GENE TRANSFER; GENES; HYBRID SYSTEMS; INDUSTRIAL APPLICATIONS; LACTIC ACID; OCEAN HABITATS; PHOSPHATASES; PROTEINS;

BIOSYNTHESIS;

BACTERIAL POLYSACCHARIDE; CAPSULAR POLYSACCHARIDE; CAPSULAR POLYSACCHARIDE A; CAPSULAR POLYSACCHARIDE B; CAPSULAR POLYSACCHARIDE D; EXOPOLYSACCHARIDE; EXOPOLYSACCHARIDE A; EXOPOLYSACCHARIDE B; EXOPOLYSACCHARIDE C; GLYCOSYL 1 PHOSPHATE TRANSFERASE; MEMBRANE PROTEIN; PROTEIN TYROSINE KINASE; PROTEIN TYROSINE PHOSPHATASE; TRANSFERASE; UNCLASSIFIED DRUG;

BACTERIUM; GENE TRANSFER; INTERSPECIFIC INTERACTION; INTRASPECIFIC INTERACTION; POLYSACCHARIDE; PROTEIN; RECOMBINATION;

AMINO ACID SEQUENCE; ARTICLE; BACTERIAL GENE; GENE TRANSFER; INTERSPECIFIC INTERACTION; INTRASPECIFIC INTERACTION; LACTOCOCCUS LACTIS CREMORIS; NONHUMAN; NUCLEOTIDE SEQUENCE; ORGANISMAL INTERACTION; PRIORITY JOURNAL; PROTEIN PROTEIN INTERACTION; STREPTOCOCCUS INIAE; STREPTOCOCCUS THERMOPHILUS;

AMINO ACID SEQUENCE; BACTERIAL CAPSULES; BACTERIAL PROTEINS; ENZYMES; GENE TRANSFER, HORIZONTAL; LACTOCOCCUS LACTIS; MOLECULAR SEQUENCE DATA; SEQUENCE ALIGNMENT; SEQUENCE HOMOLOGY, AMINO ACID; SPECIES SPECIFICITY; STREPTOCOCCUS; STREPTOCOCCUS THERMOPHILUS; TWO-HYBRID SYSTEM TECHNIQUES;

EID: 82955167930     PISSN: 00084166     EISSN: 14803275     Source Type: Journal    
DOI: 10.1139/W11-090     Document Type: Article

References (57)

1. Ammann, A., Neve, H., Geis, A., and Heller, K.J. 2008. Plasmid transfer via transduction from Streptococcus thermophilus to Lactococcus lactis. J. Bacteriol. 190(8): 3083-3087. doi:10.1128/JB.01448-07.
2. Aravind, L., andKoonin, E.V. 1998. Phosphoesterase domains associated with DNA polymerase of diverse origins. Nucleic Acids Res. 26(16): 3746-3752. doi:10.1093/nar/26.16.3746.
3. Bechet, E., Guiral, S., Torres, S., Mijakovic, I., Cozzone, A.J., and Grangeasse, C. 2009. Tyrosine-kinases in bacteria: from a matter of controversy to the status of key regulatory enzymes. Amino Acids, 37(3): 499-507. doi:10.1007/s00726-009-0237-8.
4. Becker, A., Niehaus, K., and Pühler, A. 1995. Low-molecular-weight succinoglycan is predominantly produced by Rhizobium meliloti strains carrying a mutated ExoP protein characterized by a periplasmic N-terminal domain and a missing C-terminal domain. Mol. Microbiol. 16(2): 191-203. doi:10.1111/j.1365-2958.1995. tb02292.x.
5. Bender, M.H., and Yother, J. 2001. CpsB is a modulator of capsuleassociated tyrosine kinase activity in Streptococcus pneumoniae. J. Biol. Chem. 276(51): 47966-47974.
6. Bender, M.H., Cartee, R.T., and Yother, J. 2003. Positive correlation between tyrosine phosphorylation of CpsD and capsular polysaccharide production in Streptococcus pneumoniae. J. Bacteriol. 185(20): 6057-6066. doi:10.1128/JB.185.20.6057-6066.2003.
7. Blomqvist, T., Steinmoen, H., and Havarstein, L.S. 2006. Natural genetic transformation: a novel tool for efficient genetic engineering of the dairy bacterium Streptococcus thermophilus. Appl. Environ. Microbiol. 72(10): 6751-6756. doi:10.1128/AEM.01156-06.
8. Bolotin, A., Quinquis, B., Renault, P., Sorokin, A., Ehrlich, S.D., Kulakauskas, S., et al. 2004. Complete sequence and comparative genome analysis of the dairy bacterium Streptococcus thermophilus. Nat. Biotechnol. 22(12): 1554-1558. doi:10.1038/nbt1034.
9. Bourgoin, F., Guédon, G., Pébay, M., Roussel, Y., Panis, C., and Decaris, B. 1996. Characterization of a mosaic ISS1 element and evidence for the recent horizontal transfer of two different types of ISS1 between Streptococcus thermophilus and Lactococcus lactis. Gene, 178(1-2): 15-23. doi:10.1016/0378-1119(96)00316-2.
10. Bourgoin, F., Pluvinet, A., Gintz, B., Decaris, B., and Guedon, G. 1999. Are horizontal transfers involved in the evolution of the Streptococcus thermophilus exopolysaccharide synthesis loci? Gene, 233(1-2): 151-161. doi:10.1016/S0378-1119(99)00144-4.
11. Broadbent, J.R., McMahon, D.J., Welker, D.L., Oberg, C.J., and Moineau, S. 2003. Biochemistry, genetics, and applications of exopolysaccharide production in Streptococcus thermophilus: a review. J. Dairy Sci. 86(2): 407-423. doi:10.3168/jds.S0022-0302(03)73619-4.
12. Burrus, V., Pavlovic, G., Decaris, B., and Guedon, G. 2002. The ICESt1 element of Streptococcus thermophilus belongs to a large family of integrative and conjugative elements that exchange modules and change their specificity of integration. Plasmid, 48(2): 77-97. doi:10.1016/S0147-619X(02)00102-6.
13. Cefalo, A.D., Broadbent, J.R., and Welker, D.L. 2011. Protein-protein interactions among the components of the biosynthetic machinery responsible for exopolysaccharide production in Streptococcus thermophilus MR-1C. J. Appl. Microbiol. 110(3): 801-812. doi:10.1111/j.1365-2672.2010.04935.x.
14. Chien, C.T., Bartel, P.L., Sternglanz, R., and Fields, S. 1991. The two-hybrid system: a method to identify and clone genes for proteins that interact with a protein of interest. Proc. Natl. Acad. Sci. U.S.A. 88(21): 9578-9582. doi:10.1073/pnas.88.21.9578.
15. Cieslewicz, M.J., Kasper, D.L., Wang, Y., and Wessels, M.R. 2001. Functional analysis in type 1a Group B Streptococcus of a cluster of genes involved in extracellular polysaccharide production by diverse species of streptococci. J. Biol. Chem. 276(1): 139-146. doi:10.1074/jbc.M005702200.
16. Coffey, T.J., Enright, M.C., Daniels, M., Morona, J.K., Morona, R., Hryniewicz, W., et al. 1998. Recombinational exchanges at the capsular polysaccharide biosynthetic locus lead to frequent serotype changes among natural isolates of Streptococcus pneumoniae. Mol. Microbiol. 27(1): 73-83. doi:10.1046/j.1365-2958.1998.00658.x.
17. Collins, R.F., Beis, K., Clarke, B.R., Ford, R.C., Hulley, M., Naismith, J.H., and Whitfield, C. 2006. Periplasmic protein-protein contacts in the inner membrane protein Wzc form a tetrameric complex required for the assembly of Escherichia coli group 1 capsules. J. Biol. Chem. 281(4): 2144-2150. doi:10.1074/jbc.M508078200.
18. Delorme, C., Poyart, C., Ehrlich, S.D., and Renault, P. 2007. Extent of horizontal gene transfer in evolution of Streptococci of the salivarius group. J. Bacteriol. 189(4): 1330-1341. doi:10.1128/JB.01058-06.
19. Doublet, P., Grangeasse, C., Obadia, B., Vaganay, E., and Cozzone, A.J. 2002. Structural organization of the protein-tyrosine autokinase Wzc within Escherichia coli cells. J. Biol. Chem. 277(40): 37339-37348. doi:10.1074/jbc.M204465200.
20. Durfee, T., Becherer, K., Chen, P.L., Yeh, S.H., Yang, Y., Kilburn, A. E., et al. 1993. The retinoblastoma protein associates with the protein phosphatase type 1 catalytic subunit. Genes Dev. 7(4): 555-569. doi:10.1101/gad.7.4.555.
21. Eng, C., Thibessard, A., Danielsen, M., Rasmussen, T.B., Mari, J.F., and Leblond, P. 2011. In silico prediction of horizontal gene transfer in Streptococcus thermophilus. Arch. Microbiol. 193(4): 287-297. doi:10.1007/s00203-010-0671-8.
22. Fields, S., and Song, O. 1989. A novel genetic system to detect protein-protein interaction. Nature, 340(6230): 245-246. doi:10.1038/340245a0.
23. Fontaine, L., Boutry, C., de Frahan, M.H., Delplace, B., Fremaux, C., Horvath, P., et al. 2010. A novel pheromone quorum-sensing system controls the development of natural competence in Streptococcus thermophilus and Streptococcus salivarius. J. Bacteriol. 192(5): 1444-1454. doi:10.1128/JB.01251-09.
24. Fuller, J.D., Bast, D.J., Nizet, V., Low, D.E., and de Azavedo, J.C. 2001. Streptococcus iniae virulence is associated with a distinct genetic profile. Infect. Immun. 69(4): 1994-2000. doi:10.1128/IAI.69.4.1994-2000.2001.
25. Grangeasse, C., Doublet, P., Vincent, C., Vaganay, E., Riberty, M., Duclos, B., and Cozzone, A.J. 1998. Functional characterization of the low-moleular-mass phosphotyrosine-protein phosphatase of Acinetobacter johnsonii. J. Mol. Biol. 278(2): 339-347. doi:10.1006/jmbi.1998.1650.
26. Grangeasse, C., Doublet, P., and Cozzone, A.J. 2002. Tyrosine phosphorylation of protein kinase Wzc from Escherichia coli K12 occurs through a two-step process. J. Biol. Chem. 277(9): 7127-7135. doi:10.1074/jbc.M110880200.
27. Guédon, G., Bourgoin, F., Pébay, M., Roussel, Y., Colmin, C., Simonet, J.M., and Decaris, B. 1995. Characterization and distribution of two insertion sequences, IS1191 and iso-IS981, in Streptococcus thermophilus: Does intergeneric transfer of insertion sequences occur in lactic acid bacteria co-cultures? Mol. Microbiol. 16(1): 69-78. doi:10.1111/j.1365-2958.1995.tb02392.x.
28. Hassan, A.N., Frank, J.F., and Elsoda, M. 2003. Observation of bacterial exopolysaccharides in dairy products using cryoscanning electron microscopy. Int. Dairy J. 13(9): 755-762. doi:10.1016/S0958-6946(03)00101-8.
29. Hols, P., Hancy, F., Fontaine, L., Grossiord, B., Prozzi, D., Leblond-Bourget, N., et al. 2005. New insights in the molecular biology and physiology of Streptococcus thermophilus revealed by comparative genomics. FEMS Microbiol. Rev. 29(3): 435-463.
30. Jadeau, F., Bechet, E., Cozzone, A.J., Deléage, G., Grangeasse, C., and Combet, C. 2008. Identification of the idiosyncratic bacterial protein tyrosine kinase (BY-kinase) family signature. Bioinformatics, 24(21): 2427-2430. doi:10.1093/bioinformatics/btn462.
31. LaPointe, G., Atlan, D., and Gilbert, C. 2008. Characterization and site-directed mutagenesis of Wzb, an O-phosphatase from Lactobacillus rhamnosus. BMC Biochem. 9(1): 10. doi:10.1186/1471-2091-9-10.
32. Larkin, M.A., Blackshields, G., Brown, N.P., Chenna, R., McGettigan, P.A., McWilliam, H., et al. 2007. ClustalW and ClustalX version 2. Bioinformatics, 23(21): 2947-2948. doi:10.1093/bioinformatics/btm404.
33. Lin, M.H., Hsu, T.L., Lin, S.Y., Pan, Y.J., Jan, J.T., Wang, J.T., et al. 2009. Phosphoproteomics of Klebsiella pneumoniae NTUHK2044 reveals a tight link between tyrosine phosphorylation and virulence. Mol. Cell. Proteomics, 8(12): 2613-2623. doi:10.1074/mcp.M900276-MCP200.
34. Liu, M., Siezen, R.J., and Nauta, A. 2009. In silico prediction of horizontal gene transfer events in Lactobacillus bulgaricus and Streptococcus thermophilus reveals protocooperation in yogurt manufacturing. Appl. Environ. Microbiol. 75(12): 4120-4129. doi:10.1128/AEM.02898-08.
35. Low, D., Ahlgren, J.A., Horne, D., McMahon, D.J., Oberg, C.J., and Broadbent, J.R. 1998. Role of Streptococcus thermophilus MR-1C capsular exopolysaccharide in cheese moisture retention. Appl. Environ. Microbiol. 64(6): 2147-2151.
36. Lowe, B.A., Miller, J.D., and Neely, M.N. 2007. Analysis of the polysaccharide capsule of the systemic pathogen Streptococcus iniae and its implications in virulence. Infect. Immun. 75(3): 1255-1264. doi:10.1128/IAI.01484-06.
37. Minic, Z., Marie, C., Delorme, C., Faurie, J.M., Mercier, G., Ehrlich, D., and Renault, P. 2007. Control of EpsE, the phosphoglycosyltransferase initiating exopolysaccharide synthesis in Streptococcus thermophilus, by EpsD tyrosine kinase. J. Bacteriol. 189(4): 1351-1357. doi:10.1128/JB.01122-06.
38. Morona, J.K., Paton, J.C., Miller, D.C., and Morona, R. 2000. Tyrosine phosphorylation of CpsD negatively regulates capsular polysaccharide biosynthesis in Streptococcus pneumoniae. Mol. Microbiol. 35(6): 1431-1442. doi:10.1046/j.1365-2958.2000.01808.x.
39. Morona, J.K., Morona, R., Miller, D.C., and Paton, J.C. 2002. Streptococcus pneumoniae capsule biosynthesis protein CpsB is a novel manganese-dependent phosphotyrosine-protein phosphatase. J. Bacteriol. 184(2): 577-583. doi:10.1128/JB.184.2.577-583.2002.
40. Morona, J.K., Morona, R., Miller, D.C., and Paton, J.C. 2003. Mutational analysis of the carboxy-terminal (YGX)4 repeat domain of CpsD, an autophosphorylating tyrosine kinase required for capsule biosynthesis in Streptococcus pneumoniae. J. Bacteriol. 185(10): 3009-3019. doi:10.1128/JB.185.10.3009-3019.2003.
41. Morona, J.K., Miller, D.C., Morona, R., and Paton, J.C. 2004. The effect that mutations in the conserved capsular polysaccharide biosynthesis genes cpsA, cpsB, and cpsD have on virulence of Streptococcus pneumoniae. J. Infect. Dis. 189(10): 1905-1913. doi:10.1086/383352.
42. Obadia, B., Lacour, S., Doublet, P., Baubichon-Cortay, H., Cozzone, A. J., and Grangeasse, C. 2007. Influence of tyrosine-kinase wzc activity on colonic acid production in Escherichia coli K12 cells. J.Mol. Biol. 367(1): 42-53. doi:10.1016/j.jmb.2006.12.048.
43. Olivares-Illana, V., Meyer, P., Bechet, E., Gueguen-Chaignon, V., Soulat, D., Lazereg-Riquier, S., et al. 2008. Structural basis for the regulation mechanism of the tyrosine kinase CapB from Staphylococcus aureus. PLoS Biol. 6(6): e143. doi:10.1371/journal.pbio.0060143.
44. Paiment, A., Hocking, J., and Whitfield, C. 2002. Impact of phosphorylation of specific residues in the tyrosine autokinase, Wzc, on its activity in assembly of group I capsules in Escherichia coli. J. Bacteriol. 184(23): 6437-6447. doi:10.1128/JB.184.23.6437-6447.2002.
45. Perry, D.B., McMahon, D.J., and Oberg, C.J. 1997. Effect of exopolysaccharide-producing cultures on moisture retention in low-fat Mozzarella cheese. J. Dairy Sci. 80(5): 799-805. doi:10.3168/jds.S0022-0302(97)76000-4.
46. Pluvinet, A., Charron-Bourgoin, F., Morel, C., and Decaris, B. 2004. Polymorphism of eps loci in Streptococcus thermophilus: sequence replacement by putative horizontal transfer in S. thermophilus IP6757. Int. Dairy J. 14(7): 627-634. doi:10.1016/j.idairyj.2003.12.009.
47. Preneta, R., Jarraud, S., Vincent, C., Doublet, P., Duclos, B., Etienne, J., and Cozzone, A.J. 2002. Isolation and characterization of a protein-tyrosine kinase and a phosphotyrosine-protein phosphatase from Klebsiella pneumoniae. Comp. Biochem. Physiol. B Biochem. Mol. Biol. 131(1): 103-112. doi:10.1016/S1096-4959(01)00490-0.
48. Rasmussen, T.B., Danielsen, M., Valina, O., Garrigues, C., Johansen, E., and Pedersen, M.B. 2008. Streptococcus thermophilus core genome:comparative genome hybridization study of 47 strains. Appl. Environ. Microbiol. 74(15): 4703-4710. doi:10.1128/AEM.00132-08.
49. Shi, L. 2004. Manganese-dependent protein O-phosphatases in prokaryotes and their biological functions. Front. Biosci. 9(1-3): 1382-1397. doi:10.2741/1318.
50. Soulat, D., Jault, J.M., Duclos, B., Geourjon, C., Cozzone, A.J., and Grangeasse, C. 2006. Staphylococcus aureus operates protein-tyrosine phosphorylation through a specific mechanism. J. Biol. Chem. 281 (20): 14048-14056. doi:10.1074/jbc.M513600200.
51. Soulat, D., Jault, J.M., Geourjon, C., Gouet, P., Cozzone, A.J., and Grangeasse, C. 2007. Tyrosine-kinase Wzc from Escherichia coli possesses an ATPase activity regulated by autophosphorylation. FEMS Microbiol. Lett. 274(2): 252-259. doi:10.1111/j.1574-6968.2007.00841.x.
52. Terzaghi, B.E., and Sandine, W.E. 1975. Improved medium for lactic streptococci and their bacteriophages. Appl. Microbiol. 29(6): 807-813.
53. Tocilj, A., Munger, C., Proteau, A., Morona, R., Purins, L., Ajamian, E., et al. 2008. Bacterial polysaccharide co-polymerases share a common framework for control of polymer length. Nat. Struct. Mol. Biol. 15(2): 130-138. doi:10.1038/nsmb.1374.
54. Tyvaert, G., Morel, C., Joly, J.-P., Decaris, B., and Charron-Bourgoin, F. 2006. The eps locus of Streptococcus thermophiles IP6756 is not involved in exopolysaccharide production. Int. Dairy J. 16(5): 467-473. doi:10.1016/j.idairyj.2005.06.003.
55. Vincent, C., Doublet, P., Grangeasse, C., Vaganay, E., Cozzone, A.J., and Duclos, B. 1999. Cells of Escherichia coli contain a proteintyrosine kinase, Wzc, and a phosphotyrosine protein phosphatase, Wzb. J. Bacteriol. 181(11): 3472-3477.
56. Walker, J.E., Saraste, M., Runswick, M.J., and Gay, N.J. 1982. Distantly related sequences in the alpha- and beta-subunits of ATP synthase, myosin, kinases and other ATP-requiring enzymes and a common nucleotide binding fold. EMBO J. 1(8): 945-951.
57. Wugeditsch, T., Paiment, A., Hocking, J., Drummelsmith, J., Forrester, C., and Whitfield, C. 2001. Phosphorylation of Wzc, a tyrosine autokinase, is essential for assembly of group 1 capsular polysaccharides in Escherichia coli. J. Biol. Chem. 276(4): 2361-2371. doi:10.1074/jbc.M009092200.