Regulation of oxidative response and extracellular polysaccharide synthesis by a diadenylate cyclase in Streptococcus mutans

Environmental Microbiology

Volumn 18, Issue 3, 2016, Pages 904-922

  Cheng, Xingqun ^a   Zheng, Xin ^a   Zhou, Xuedong ^a   Zeng, Jumei ^b   Ren, Zhi ^a   Xu, Xin ^a   Cheng, Lei ^a   Li, Mingyun ^a   Li, Jiyao ^a   Li, Yuqing ^a  

^a SICHUAN UNIVERSITY   (China)

^b BOSTON CHILDREN S HOSPITAL   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

BACTERIAL PROTEIN; CYCLIC DIADENOSINE PHOSPHATE; DINUCLEOSIDE PHOSPHATE; GLUCOSYLTRANSFERASE; POLYSACCHARIDE;

BIOSYNTHESIS; CARBOHYDRATE METABOLISM; DENTAL CARIES; ENZYMOLOGY; GENETICS; HUMAN; METABOLISM; MICROBIOLOGY; OXIDATION REDUCTION REACTION; STREPTOCOCCUS MUTANS; UPREGULATION;

BACTERIAL PROTEINS; CARBOHYDRATE METABOLISM; DENTAL CARIES; DINUCLEOSIDE PHOSPHATES; GLUCOSYLTRANSFERASES; HUMANS; OXIDATION-REDUCTION; POLYSACCHARIDES; STREPTOCOCCUS MUTANS; UP-REGULATION;

EID: 84961146509     PISSN: 14622912     EISSN: 14622920     Source Type: Journal    
DOI: 10.1111/1462-2920.13123     Document Type: Article

References (71)

1. Abdul-Sater, A.A., Tattoli, I., Jin, L., Grajkowski, A., Levi, A., Koller, B.H., etal. (2013) Cyclic-di-GMP and cyclic-di-AMP activate the NLRP3 inflammasome. EMBO Rep 14: 900-906.
2. Ajdić, D., McShan, W.M., McLaughlin, R.E., Savić, G., Chang, J., Carson, M.B., etal. (2002) Genome sequence of Streptococcus mutans UA159, a cariogenic dental pathogen. Proc Natl Acad Sci USA 99: 14434-14439.
3. Ayala, E., Downey, J.S., Mashburn-Warren, L., Senadheera, D.B., Cvitkovitch, D.G., and Goodman, S.D. (2014) A biochemical characterization of the DNA binding activity of the response regulator VicR from Streptococcus mutans. PLoS ONE 9: e108027.
4. Bai, Y., Yang, J., Zhou, X., Ding, X., Eisele, L.E., and Bai, G. (2012) Mycobacterium tuberculosis Rv3586 (DacA) is a diadenylate cyclase that converts ATP or ADP into c-di-AMP. PLoS ONE 7: e35206.
5. Bai, Y., Yang, J., Zarrella, T.M., Zhang, Y., Metzger, D.W., and Bai, G. (2014) Cyclic di-AMP impairs potassium uptake mediated by a cyclic di-AMP binding protein in Streptococcus pneumoniae. J Bacteriol 196: 614-623.
6. Biswas, S., and Biswas, I. (2006) Regulation of the glucosyltransferase (gtfBC) operon by CovR in Streptococcus mutans. J Bacteriol 188: 988-998.
7. Burhenne, H., and Kaever, V. (2013) Quantification of cyclic dinucleotides by reversed-phase LC-MS/MS. Methods Mol Biol 1016: 27-37.
8. Chattoraj, P., Banerjee, A., Biswas, S., and Biswas, I. (2010) ClpP of Streptococcus mutans differentially regulates expression of genomic islands, mutacin production, and antibiotic tolerance. J Bacteriol 192: 1312-1323.
9. Chen, Z., Saxena, D., Caufield, P.W., Ge, Y., Wang, M., and Li, Y. (2007) Development of species-specific primers for detection of Streptococcus mutans in mixed bacterial samples. FEMS Microbiol Lett 272: 154-162.
10. Cheng, X., Xu, X., Chen, J., Zhou, X., Cheng, L., Li, M., etal. (2014) Effects of simulated microgravity on Streptococcus mutans physiology and biofilm structure. FEMS Microbiol Lett 359: 94-101.
11. Corrigan, R.M., and Gründling, A. (2013) Cyclic di-AMP: another second messenger enters the fray. Nat Rev Microbiol 11: 513-524.
12. Corrigan, R.M., Abbott, J.C., Burhenne, H., Kaever, V., and Gründling, A. (2011) c-di-AMP is a new second messenger in Staphylococcus aureus with a role in controlling cell size and envelope stress. PLoS Pathog 7: e1002217.
13. Deng, D.M., Liu, M.J., ten Cate, J.M., and Crielaard, W. (2007) The VicRK system of Streptococcus mutans responds to oxidative stress. J Dent Res 86: 606-610.
14. Dengler, V., McCallum, N., Kiefer, P., Christen, P., Patrignani, A., Vorholt, J.A., etal. (2013) Mutation in the C-di-AMP cyclase dacA affects fitness and resistance of methicillin resistant Staphylococcus aureus. PLoS ONE 8: e73512.
15. Dmitriev, A., Mohapatra, S.S., Chong, P., Neely, M., Biswas, S., and Biswas, I. (2011) CovR-controlled global regulation of gene expression in Streptococcus mutans. PLoS ONE 6: e20127.
16. Dong, G., Tian, X.L., Gomez, Z.A., and Li, Y.H. (2014) Regulated proteolysis of the alternative sigma factor SigX in Streptococcus mutans: implication in the escape from competence. BMC Microbiol 14: 183.
17. Flemming, H.C., and Wingender, J. (2010) The biofilm matrix. Nat Rev Microbiol 8: 623-633.
18. Gándara, C., and Alonso, J.C. (2015) DisA and c-di-AMP act at the intersection between DNA-damage response and stress homeostasis in exponentially growing Bacillus subtilis cells. DNA Repair (Amst) 27C: 1-8.
19. Gao, A., and Serganov, A. (2014) Structural insights into recognition of c-di-AMP by the ydaO riboswitch. Nat Chem Biol 10: 787-792.
20. Gill, S.C., and von Hippel, P.H. (1989) Calculation of protein extinction coefficients from amino acid sequence data. Anal Biochem 182: 319-326.
21. Guo, Q., Ahn, S.J., Kaspar, J., Zhou, X., and Burne, R.A. (2014) Growth phase and pH influence peptide signaling for competence development in Streptococcus mutans. J Bacteriol 196: 227-236.
22. Hussain, H., Branny, P., and Allan, E. (2006) A eukaryotic-type serine/threonine protein kinase is required for biofilm formation, genetic competence, and acid resistance in Streptococcus mutans. J Bacteriol 188: 1628-1632.
23. Huynh, T.N., Luo, S., Pensinger, D., Sauer, J.D., Tong, L., and Woodward, J.J. (2015) An HD-domain phosphodiesterase mediates cooperative hydrolysis of c-di-AMP to affect bacterial growth and virulence. Proc Natl Acad Sci USA 112: E747-E756.
24. Jones, C.P., and Ferré-D'Amaré, A.R. (2014) Crystal structure of a c-di-AMP riboswitch reveals an internally pseudo-dimeric RNA. EMBO J 33: 2692-2703.
25. Kaplan Zeevi, M., Shafir, N.S., Shaham, S., Friedman, S., Sigal, N., Nir Paz, R., etal. (2013) Listeria monocytogenes multidrug resistance transporters and cyclic di-AMP, which contribute to type I interferon induction, play a role in cell wall stress. J Bacteriol 195: 5250-5261.
26. Klein, M.I., Hwang, G., Santos, P.H., Campanella, O.H., and Koo, H. (2015) Streptococcus mutans-derived extracellular matrix in cariogenic oral biofilms. Front Cell Infect Microbiol 5: 1-8.
27. Kreth, J., Merritt, J., Shi, W., and Qi, F. (2005) Competition and coexistence between Streptococcus mutans and Streptococcus sanguinis in the dental biofilm. J Bacteriol 187: 7193-7203.
28. LeBlanc, D.J., Lee, L.N., and Abu-Al-Jaibat, A. (1992) Molecular, genetic, and functional analysis of the basic replicon of pVA380-1, a plasmid of oral streptococcal origin. Plasmid 28: 130-145.
29. Li, M.Y., Huang, R.J., Zhou, X.D., and Gregory, R.L. (2013) Role of sortase in Streptococcus mutans under the effect of nicotine. Int J Oral Sci 5: 206-211.
30. Li, Y., Zeng, J., Zhang, H., and He, Z.G. (2010) The characterization of conserved binding motifs and potential target genes for M. tuberculosis MtrAB reveals a link between the two-component system and the drug resistance of M. smegmatis. BMC Microbiol 10: 242.
31. Liu, X.D., Duan, J., and Guo, L.H. (2009) Role of phosphoglucosamine mutase on virulence properties of Streptococcus mutans. Oral Microbiol Immunol 24: 272-277.
32. Luo, Y., and Helmann, J.D. (2012) Analysis of the role of Bacillus subtilis σ(M) in β-lactam resistance reveals an essential role for c-di-AMP in peptidoglycan homeostasis. Mol Microbiol 83: 623-639.
33. Manikandan, K., Sabareesh, V., Singh, N., Saigal, K., Mechold, U., and Sinha, K.M. (2014) Two-step synthesis and hydrolysis of cyclic di-AMP in Mycobacterium tuberculosis. PLoS ONE 9: e86096.
34. Mattos-Graner, R.O., Napimoga, M.H., Fukushima, K., Duncan, M.J., and Smith, D.J. (2004) Comparative analysis of Gtf isozyme production and diversity in isolates of Streptococcus mutans with different biofilm growth phenotypes. J Clin Microbiol 42: 4586-4592.
35. Mehne, F.M., Gunka, K., Eilers, H., Herzberg, C., Kaever, V., and Stülke, J. (2013) Cyclic di-AMP homeostasis in Bacillus subtilis: both lack and high level accumulation of the nucleotide are detrimental for cell growth. J Biol Chem 288: 2004-2017.
36. Mehne, F.M., Schröder-Tittmann, K., Eijlander, R.T., Herzberg, C., Hewitt, L., Kaever, V., etal. (2014) Control of the diadenylate cyclase CdaS in Bacillus subtilis: an autoinhibitory domain limits cyclic di-AMP production. J Biol Chem 289: 21098-21107.
37. Mengin-Lecreulx, D., and van Heijenoort, J. (1996) Characterization of the essential gene glmM encoding phosphoglucosamine mutase in Escherichia coli. J Biol Chem 271: 32-39.
38. Nelson, J.W., Sudarsan, N., Furukawa, K., Weinberg, Z., Wang, J.X., and Breaker, R.R. (2013) Riboswitches in eubacteria sense the second messenger c-di-AMP. Nat Chem Biol 9: 834-839.
39. Ng, W.L., Kazmierczak, K.M., and Winkler, M.E. (2004) Defective cell wall synthesis in Streptococcus pneumoniae R6 depleted for the essential PcsB putative murein hydrolase or the VicR (YycF) response regulator. Mol Microbiol 53: 1161-1175.
40. Oppenheimer-Shaanan, Y., Wexselblatt, E., Katzhendler, J., Yavin, E., and Ben-Yehuda, S. (2011) c-di-AMP reports DNA integrity during sporulation in Bacillus subtilis. EMBO Rep 12: 594-601.
41. Ren, A., and Patel, D.J. (2014) c-di-AMP binds the ydaO riboswitch in two pseudo-symmetry-related pockets. Nat Chem Biol 10: 780-786.
42. Ren, Z., Cui, T., Zeng, J., Chen, L., Zhang, W., Xu, X., etal. (2015) Molecule targeting glucosyltransferase inhibits Streptococcus mutans biofilm formation and virulence. Antimicrob Agents Chemother in press.
43. Rosenberg, J., Dickmanns, A., Neumann, P., Gunka, K., Arens, J., Kaever, V., etal. (2015) Structural and biochemical analysis of the essential diadenylate cyclase CdaA from Listeria monocytogenes. J Biol Chem 290: 6596-6606.
44. Römling, U. (2008) Great times for small molecules: c-di-AMP, a second messenger candidate in Bacteria and Archaea. Sci Signal 1: pe39.
45. Römling, U., and Balsalobre, C. (2012) Biofilm infections, their resilience to therapy and innovative treatment strategies. J Intern Med 272: 541-561.
46. Römling, U., Galperin, M.Y., and Gomelsky, M. (2013) Cyclic di-GMP: the first 25 years of a universal bacterial second messenger. Microbiol Mol Biol Rev 77: 1-52.
47. Senadheera, D.B., Cordova, M., Ayala, E.A., Chávez de Paz, L.E., Singh, K., Downey, J.S., etal. (2012) Regulation of bacteriocin production and cell death by the VicRK signaling system in Streptococcus mutans. J Bacteriol 194: 1307-1316.
48. Senadheera, M.D., Guggenheim, B., Spatafora, G.A., Huang, Y.C., Choi, J., Hung, D.C., etal. (2005) A VicRK signal transduction system in Streptococcus mutans affects gtfBCD, gbpB, and ftf expression, biofilm formation, and genetic competence development. J Bacteriol 187: 4064-4076.
49. Serbanescu, M.A., Cordova, M., Krastel, K., Flick, R., Beloglazova, N., Latos, A., etal. (2015) Role of the Streptococcus mutans CRISPR-Cas systems in immunity and cell physiology. J Bacteriol 197: 749-761.
50. Shimazu, K., Takahashi, Y., Uchikawa, Y., Shimazu, Y., Yajima, A., Takashima, E., etal. (2008) Identification of the Streptococcus gordonii glmM gene encoding phosphoglucosamine mutase and its role in bacterial cell morphology, biofilm formation, and sensitivity to antibiotics. FEMS Immunol Med Microbiol 53: 166-177.
51. Smith, E.G., and Spatafora, G.A. (2012) Gene regulation in S.mutans: complex control in a complex environment. J Dent Res 91: 133-141.
52. Smith, W.M., Pham, T.H., Lei, L., Dou, J., Soomro, A.H., Beatson, S.A., etal. (2012) Heat resistance and salt hypersensitivity in Lactococcus lactis due to spontaneous mutation of llmg_1816 (gdpP) induced by high-temperature growth. Appl Environ Microbiol 78: 7753-7759.
53. Sureka, K., Choi, P.H., Precit, M., Delince, M., Pensinger, D.A., Huynh, T.N., etal. (2014) The cyclic dinucleotide c-di-AMP is an allosteric regulator of metabolic enzyme function. Cell 158: 1389-1401.
54. Thibessard, A., Borges, F., Fernandez, A., Gintz, B., Decaris, B., and Leblond-Bourget, N. (2004) Identification of Streptococcus thermophilus CNRZ368 genes involved in defense against superoxide stress. Appl Environ Microbiol 70: 2220-2229.
55. Underwood, A.J., Zhang, Y., Metzger, D.W., and Bai, G. (2014) Detection of cyclic di-AMP using a competitive ELISA with a unique pneumococcal cyclic di-AMP binding protein. J Microbiol Methods 107: 58-62.
56. Whiteley, A.T., Pollock, A.J., and Portnoy, D.A. (2015) The PAMP c-di-AMP is essential for Listeria growth in macrophages and rich but not minimal media due to a toxic increase in (p)ppGpp. Cell Host Microbe 17: 788-798.
57. Witte, C.E., Whiteley, A.T., Burke, T.P., Sauer, J.D., Portnoy, D.A., and Woodward, J.J. (2013) Cyclic di-AMP is critical for Listeria monocytogenes growth, cell wall homeostasis, and establishment of infection. MBio 4: e00282-13.
58. Witte, G., Hartung, S., Büttner, K., and Hopfner, K.P. (2008) Structural biochemistry of a bacterial checkpoint protein reveals diadenylate cyclase activity regulated by DNA recombination intermediates. Mol Cell 30: 167-178.
59. Woodward, J.J., Iavarone, A.T., and Portnoy, D.A. (2010) c-di-AMP secreted by intracellular Listeria monocytogenes activates a host type I interferon response. Science 328: 1703-1705.
60. 2 tolerance. Appl Environ Microbiol 76: 5815-5826.
61. Xiao, J., Klein, M.I., Falsetta, M.L., Lu, B., Delahunty, C.M., Yates, J.R., 3rd, etal. (2012) The exopolysaccharide matrix modulates the interaction between 3D architecture and virulence of a mixed-species oral biofilm. PLoS Pathog 8: e1002623.
62. Xie, Z., Okinaga, T., Qi, F., Zhang, Z., and Merritt, J. (2011) Cloning-independent and counterselectable markerless mutagenesis system in Streptococcus mutans. Appl Environ Microbiol 77: 8025-8033.
63. Xu, P., Ge, X., Chen, L., Wang, X., Dou, Y., Xu, J.Z., etal. (2011) Genome-wide essential gene identification in Streptococcus sanguinis. Sci Rep 1: 1-9.
64. Yan, W., Qu, T., Zhao, H., Su, L., Yu, Q., Gao, J., and Wu, B. (2010) The effect of c-di-GMP (3'-5'-cyclic diguanylic acid) on the biofilm formation and adherence of Streptococcus mutans. Microbiol Res 165: 87-96.
65. Yang, J., Bai, Y., Zhang, Y., Gabrielle, V.D., Jin, L., and Bai, G. (2014) Deletion of the cyclic di-AMP phosphodiesterase gene (cnpB) in Mycobacterium tuberculosis leads to reduced virulence in a mouse model of infection. Mol Microbiol 93: 65-79.
66. Ye, M., Zhang, J.J., Fang, X., Lawlis, G.B., Troxell, B., Zhou, Y., etal. (2014) DhhP, a cyclic di-AMP phosphodiesterase of Borrelia burgdorferi, is essential for cell growth and virulence. Infect Immun 82: 1840-1849.
67. Zhang, L., Li, W., and He, Z.G. (2013) DarR, a TetR-like transcriptional factor, is a cyclic di-AMP-responsive repressor in Mycobacterium smegmatis. J Biol Chem 288: 3085-3096.
68. Zheng, C., Ma, Y., Wang, X., Xie, Y., Ali, M.K., and He, J. (2015) Functional analysis of the sporulation-specific diadenylate cyclase CdaS in Bacillus thuringiensis. Front Microbiol 6: 1-15.
69. Zheng, X., Zhang, K., Zhou, X., Liu, C., Li, M., Li, Y., etal. (2013) Involvement of gshAB in the interspecies competition within oral biofilm. J Dent Res 92: 819-824.
70. Zheng, Y., Zhou, J., Sayre, D.A., and Sintim, H.O. (2014) Identification of bromophenol thiohydantoin as an inhibitor of DisA, a c-di-AMP synthase, from a 1000 compound library, using the coralyne assay. Chem Commun (Camb) 50: 11234-11237.
71. Zhou, J., Sayre, D.A., Zheng, Y., Szmacinski, H., and Sintim, H.O. (2014) Unexpected complex formation between coralyne and cyclic diadenosine monophosphate providing a simple fluorescent turn-on assay to detect this bacterial second messenger. Anal Chem 86: 2412-2420.