Functional profiling in Streptococcus mutans: Construction and examination of a genomic collection of gene deletion mutants

Molecular Oral Microbiology

Volumn 30, Issue 6, 2015, Pages 474-495

  Quivey, R G ^a   Grayhack, E J ^a   Faustoferri, R C ^a   Hubbard, C J ^a,c   Baldeck, J D ^a,d   Wolf, A S ^a   Macgilvray, M E ^a,e   Rosalen, P L ^a,f   Scott Anne, K ^a   Santiago, B ^a   Gopal, S ^b,g   Payne, J ^a,d   Marquis, R E ^a  

^a UNIVERSITY OF ROCHESTER MEDICAL CENTER   (United States)

^b ROCHESTER INSTITUTE OF TECHNOLOGY   (United States)

^c GWA Gregory Wentworth Advertising   (United States)

^d University of Campinas ^*  (United States)

^e UNIVERSITY OF CAMPINAS   (Brazil)

^f UNIVERSITY OF WISCONSIN MADISON   (United States)

^g BROAD INSTITUTE OF MIT AND HARVARD   (United States)

Author keywords

Genomics; Pathogenesis; Physiology

Indexed keywords

GLUCOSE; SUCROSE; BACTERIAL PROTEIN;

ACIDITY; ACIDURIA; ANIMAL EXPERIMENT; ANIMAL MODEL; ARTICLE; BACTERIAL GENE; BACTERIAL STRAIN; BACTERIAL SURVIVAL; BACTERIAL VIRULENCE; BACTERIUM CULTURE; BACTERIUM ISOLATION; BACTERIUM MUTANT; BIOFILM; CHEMOSTAT; COCULTURE; CONTROLLED STUDY; DELETION MUTANT; GENE DELETION; GENOMICS; IN VITRO STUDY; MOUTH FLORA; MOUTH INFECTION; NONHUMAN; OPEN READING FRAME; OXIDATIVE STRESS; PH; RAT; STEADY STATE; STREPTOCOCCUS MUTANS; TOOTH; ANIMAL; BACTERIAL GENOME; DNA BARCODING; GENE EXPRESSION REGULATION; GENETICS; GROWTH, DEVELOPMENT AND AGING; MICROBIOLOGY; MOUTH; MUTATION; PATHOGENICITY; REPRODUCTIVE FITNESS;

ANIMALS; BACTERIAL PROTEINS; BIOFILMS; DNA BARCODING, TAXONOMIC; GENE DELETION; GENE EXPRESSION REGULATION, BACTERIAL; GENETIC FITNESS; GENOME, BACTERIAL; GENOMICS; HYDROGEN-ION CONCENTRATION; MOUTH; MUTATION; OXIDATIVE STRESS; RATS; STREPTOCOCCUS MUTANS;

EID: 84946488769     PISSN: 20411006     EISSN: 20411014     Source Type: Journal    
DOI: 10.1111/omi.12107     Document Type: Article

References (56)

1. Aas, J.A., Griffen, A.L., Dardis, S.R., et al. (2008) Bacteria of dental caries in primary and permanent teeth in children and young adults. J Clin Microbiol 46: 1407-1417.
2. Ahn, S.J., Lemos, J.A. and Burne, R.A. (2005) Role of HtrA in growth and competence of Streptococcus mutans UA159. J Bacteriol 187: 3028-3038.
3. Ajdic, D., McShan, W.M., McLaughlin, R.E., et al. (2002) Genome sequence of Streptococcus mutans UA159, a cariogenic dental pathogen. Proc Natl Acad Sci USA 99: 14434-14439.
4. Aoki, H., Shiroza, T., Hayakawa, M., Sato, S. and Kuramitsu, H.K. (1986) Cloning of a Streptococcus mutans glucosyltransferase gene coding for insoluble glucan synthesis. Infect Immun 53: 587-594.
5. Becker, M.R., Paster, B.J., Leys, E.J., et al. (2002) Molecular analysis of bacterial species associated with childhood caries. J Clin Microbiol 40: 1001-1009.
6. Belli, W.A. and Marquis, R.E. (1991) Adaptation of Streptococcus mutans and Enterococcus hirae to acid stress in continuous culture. Appl Environ Microbiol 57: 1134-1138.
7. Bose, J.L., Fey, P.D. and Bayles, K.W. (2013) Genetic tools to enhance the study of gene function and regulation in Staphylococcus aureus. Appl Environ Microbiol 79: 2218-2224.
8. Bowen, W.H. and Koo, H. (2011) Biology of Streptococcus mutans-derived glucosyltransferases: role in extracellular matrix formation of cariogenic biofilms. Caries Res 45: 69-86.
9. Buckley, A.A., Faustoferri, R.C. and Quivey, R.G. Jr (2014) β-phosphoglucomutase contributes to aciduricity in Streptococcus mutans. Microbiology 160: 818-827.
10. Cornejo, O.E., Lefebure, T., Bitar, P.D., et al. (2013) Evolutionary and population genomics of the cavity causing bacteria Streptococcus mutans. Mol Biol Evol 30: 881-893.
11. Costalonga, M. and Herzberg, M.C. (2014) The oral microbiome and the immunobiology of periodontal disease and caries. Immunol Lett 162: 22-38.
12. Derr, A.M., Faustoferri, R.C., Betzenhauser, M.J., Gonzalez, K., Marquis, R.E. and Quivey, R.G. Jr (2012) Mutation of the NADH oxidase gene (nox) reveals an overlap of the oxygen- and acid-mediated stress responses in Streptococcus mutans. Appl Environ Microbiol 78: 1215-1227.
13. Faustoferri, R.C., Hubbard, C.J., Santiago, B., Buckley, A.A., Seifert, T.B. and Quivey, R.G. (2015) Regulation of fatty acid biosynthesis by the global regulator CcpA and the local regulator FabT in Streptococcus mutans. Mol Oral Microbiol 30: 128-146.
14. Fey, P.D., Endres, J.L., Yajjala, V.K., et al. (2013) A genetic resource for rapid and comprehensive phenotype screening of nonessential Staphylococcus aureus genes. MBio 4: e00537-e00512.
15. Fozo, E.M. and Quivey, R.G. Jr (2004a) The fabM gene product of Streptococcus mutans is responsible for the synthesis of monounsaturated fatty acids and is necessary for survival at low pH. J Bacteriol 186: 4152-4158.
16. Fozo, E.M. and Quivey, R.G. Jr (2004b) Shifts in the membrane fatty acid profile of Streptococcus mutans enhance survival in acidic environments. Appl Environ Microbiol 70: 929-936.
17. Fozo, E.M., Kajfasz, J.K. and Quivey, R.G. Jr (2004) Low pH-induced membrane fatty acid alterations in oral bacteria. FEMS Microbiol Lett 238: 291-295.
18. Fozo, E.M., Scott-Anne, K., Koo, H. and Quivey, R.G. Jr (2007) Role of unsaturated fatty acid biosynthesis in virulence of Streptococcus mutans. Infect Immun 75: 1537-1539.
19. Gagarinova, A., Babu, M., Greenblatt, J. and Emili, A. (2012) Mapping bacterial functional networks and pathways in Escherichia coli using synthetic genetic arrays. J Vis Exp 69: e4056, doi:10.3791/4056.
20. Ge, X., Kitten, T., Chen, Z., Lee, S.P., Munro, C.L. and Xu, P. (2008) Identification of Streptococcus sanguinis genes required for biofilm formation and examination of their role in endocarditis virulence. Infect Immun 76: 2551-2559.
21. Giaever, G., Chu, A.M., Ni, L., et al. (2002) Functional profiling of the Saccharomyces cerevisiae genome. Nature 418: 387-391.
22. Gross, E.L., Beall, C.J., Kutsch, S.R., Firestone, N.D., Leys, E.J. and Griffen, A.L. (2012) Beyond Streptococcus mutans: dental caries onset linked to multiple species by 16S rRNA community analysis. PLoS ONE 7: e47722.
23. Hughes, T.R., Marton, M.J., Jones, A.R., et al. (2000) Functional discovery via a compendium of expression profiles. Cell 102: 109-126.
24. Kajfasz, J.K., Rivera-Ramos, I., Abranches, J., et al. (2010) Two Spx proteins modulate stress tolerance, survival, and virulence in Streptococcus mutans. J Bacteriol 192: 2546-2556.
25. Kanasi, E., Dewhirst, F.E., Chalmers, N.I., et al. (2010) Clonal analysis of the microbiota of severe early childhood caries. Caries Res 44: 485-497.
26. Klein, B.A., Tenorio, E.L., Lazinski, D.W., Camilli, A., Duncan, M.J. and Hu, L.T. (2012) Identification of essential genes of the periodontal pathogen Porphyromonas gingivalis. BMC Genom 13: 578.
27. Korte, H.L., Fels, S.R., Christensen, G.A., et al. (2014) Genetic basis for nitrate resistance in Desulfovibrio strains. Front Microbiol 5: 153.
28. Kuzmin, E., Sharifpoor, S., Baryshnikova, A., et al. (2014) Synthetic genetic array analysis for global mapping of genetic networks in yeast. Methods Mol Biol 1205: 143-168.
29. Lau, P.C., Sung, C.K., Lee, J.H., Morrison, D.A. and Cvitkovitch, D.G. (2002) PCR ligation mutagenesis in transformable streptococci: application and efficiency. J Microbiol Methods 49: 193-205.
30. Lemme, A., Sztajer, H. and Wagner-Dobler, I. (2010) Characterization of mleR, a positive regulator of malolactic fermentation and part of the acid tolerance response in Streptococcus mutans. BMC Microbiol 10: 58.
31. Lemos, J.A., Quivey, R.G. Jr, Koo, H. and Abranches, J. (2013) Streptococcus mutans: a new Gram-positive paradigm? Microbiology 159: 436-445.
32. Li, Y.H., Tang, N., Aspiras, M.B., et al. (2002) A quorum-sensing signaling system essential for genetic competence in Streptococcus mutans is involved in biofilm formation. J Bacteriol 184: 2699-2708.
33. Liu, B., Faller, L.L., Klitgord, N., et al. (2012) Deep sequencing of the oral microbiome reveals signatures of periodontal disease. PLoS ONE 7: e37919.
34. Lopez, A., Parsons, A.B., Nislow, C., Giaever, G. and Boone, C. (2008) Chemical-genetic approaches for exploring the mode of action of natural products. Prog Drug Res 66: 237, 239-271.
35. MacGilvray, M.E., Lapek, J.D. Jr, Friedman, A.E. and Quivey, R.G. Jr (2012) Cardiolipin biosynthesis in Streptococcus mutans is regulated in response to external pH. Microbiology 158: 2133-2143.
36. Marquis, R.E. (1995) Oxygen metabolism, oxidative stress and acid-base physiology of dental plaque biofilms. J Ind Microbiol 15: 198-207.
37. Muller-Herbst, S., Wustner, S., Muhlig, A., et al. (2014) Identification of genes essential for anaerobic growth of Listeria monocytogenes. Microbiology 160: 752-765.
38. Murchison, H.H., Barrett, J.F., Cardineau, G.A. and Curtiss, R. 3rd (1986) Transformation of Streptococcus mutans with chromosomal and shuttle plasmid (pYA629) DNAs. Infect Immun 54: 273-282.
39. Nichols, R.J., Sen, S., Choo, Y.J., et al. (2011) Phenotypic landscape of a bacterial cell. Cell 144: 143-156.
40. Nyvad, B., Crielaard, W., Mira, A., Takahashi, N. and Beighton, D. (2013) Dental caries from a molecular microbiological perspective. Caries Res 47: 89-102.
41. Perry, D. and Kuramitsu, H.K. (1981) Genetic transformation of Streptococcus mutans. Infect Immun 32: 1295-1297.
42. Pierce, S.E., Davis, R.W., Nislow, C. and Giaever, G. (2007) Genome-wide analysis of barcoded Saccharomyces cerevisiae gene-deletion mutants in pooled cultures. Nat Protoc 2: 2958-2974.
43. Quivey, R.G. Jr, Faustoferri, R.C., Belli, W.A. and Flores, J.S. (1991) Polymerase chain reaction amplification, cloning, sequence determination and homologies of streptococcal ATPase-encoding DNAs. Gene 97: 63-68.
44. Quivey, R.G. Jr, Faustoferri, R.C., Clancy, K.A. and Marquis, R.E. (1995) Acid adaptation in Streptococcus mutans UA159 alleviates sensitization to environmental stress due to RecA deficiency. FEMS Microbiol Lett 126: 257-261.
45. Rooney, J.P., Patil, A., Zappala, M.R., Conklin, D.S., Cunningham, R.P. and Begley, T.J. (2008) A molecular bar-coded DNA repair resource for pooled toxicogenomic screens. DNA Repair (Amst) 7: 1855-1868.
46. Rozen, S. and Skaletsky, H. (2000) Primer3 on the WWW for general users and for biologist programmers. Methods Mol Biol 132: 365-386.
47. Santiago, B., MacGilvray, M., Faustoferri, R.C. and Quivey, R.G. Jr (2012) The branched-chain amino acid aminotransferase encoded by ilvE is involved in acid tolerance in Streptococcus mutans. J Bacteriol 194: 2010-2019.
48. Santiago, B., Marek, M., Faustoferri, R.C. and Quivey, R.G. Jr (2013) The Streptococcus mutans aminotransferase encoded by ilvE is regulated by CodY and CcpA. J Bacteriol 195: 3552-3562.
49. Sheng, J. and Marquis, R.E. (2007) Malolactic fermentation by Streptococcus mutans. FEMS Microbiol Lett 272: 196-201.
50. Sheng, J., Baldeck, J.D., Nguyen, P.T., Quivey, R.G. Jr and Marquis, R.E. (2010) Alkali production associated with malolactic fermentation by oral streptococci and protection against acid, oxidative, or starvation damage. Can J Microbiol 56: 539-547.
51. Smith, A.M., Heisler, L.E., St Onge, R.P., et al. (2010) Highly-multiplexed barcode sequencing: an efficient method for parallel analysis of pooled samples. Nucleic Acids Res 38: e142.
52. Takahashi, N. and Nyvad, B. (2008) Caries ecology revisited: microbial dynamics and the caries process. Caries Res 42: 409-418.
53. Takahashi, N. and Nyvad, B. (2011) The role of bacteria in the caries process: ecological perspectives. J Dent Res 90: 294-303.
54. Valentino, M.D., Foulston, L., Sadaka, A., et al. (2014) Genes contributing to Staphylococcus aureus fitness in abscess- and infection-related ecologies. MBio 5: e01729-01714.
55. Wang, L., Wang, X., Arkin, A.P. and Samoilov, M.S. (2013) Inference of gene regulatory networks from genome-wide knockout fitness data. Bioinformatics 29: 338-346.
56. Xu, D., Jiang, B., Ketela, T., et al. (2007) Genome-wide fitness test and mechanism-of-action studies of inhibitory compounds in Candida albicans. PLoS Pathog 3: e92.