Specialized adaptation of a lactic acid bacterium to the milk environment: The comparative genomics of Streptococcus thermophilus LMD-9

Microbial Cell Factories

Volumn 10, Issue SUPPL. 1, 2011, Pages

  Goh, Yong J ^a   Goin, Caitlin ^b   O'Flaherty, Sarah ^a   Altermann, Eric ^c,d   Hutkins, Robert ^e  

^a NORTH CAROLINA STATE UNIVERSITY   (United States)

^b UNIVERSITY OF NEBRASKA   (United States)

^c AGRESEARCH GRASSLANDS   (New Zealand)

^d MASSEY UNIVERSITY   (New Zealand)

^e UNIVERSITY OF NEBRASKA LINCOLN   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

AMINO ACID; BACTERIAL DNA; BACTERIAL PROTEIN; BINDING PROTEIN; CARRIER PROTEIN; HISTIDINE; MUCUS BINDING PROTEIN; PEPTIDE TRANSPORTER; PROTEIN CRISPR1; PROTEINASE; TRANSCRIPTOME; UNCLASSIFIED DRUG; YOGHURT; LACTIC ACID;

AMINO ACID METABOLISM; AMINO ACID TRANSPORT; ARTICLE; BACTERIAL CHROMOSOME; BACTERIAL GENE; BACTERIAL GENOME; BACTERIAL GROWTH; BACTERIAL STRAIN; BACTERIAL VIRULENCE; BACTERIOPHAGE; BACTERIUM CULTURE; CARBOHYDRATE METABOLISM; COMPARATIVE GENE MAPPING; COMPARATIVE GENOME ANALYSIS; CONTROLLED STUDY; DNA REPLICATION; EVOLUTIONARY ADAPTATION; GENOME ANALYSIS; LACTIC ACID BACTERIUM; LACTOBACILLUS DELBRUECKII; MICROENVIRONMENT; MILK; MOLECULAR EVOLUTION; NONHUMAN; OPEN READING FRAME; ORTHOLOGY; PLASMID; PROTEIN EXPRESSION; PSEUDOGENE; STREPTOCOCCUS THERMOPHILUS; UPREGULATION; ANIMAL; BIOLOGY; CATTLE; DAIRY PRODUCT; GENETICS; GENOMICS; HUMAN; METABOLISM; MICROBIOLOGY;

BACTERIA (MICROORGANISMS); LACTOBACILLUS DELBRUECKII; STREPTOCOCCUS THERMOPHILUS; STREPTOCOCCUS THERMOPHILUS LMD-9;

ANIMALS; CATTLE; COMPUTATIONAL BIOLOGY; DAIRY PRODUCTS; GENOMICS; HUMANS; LACTIC ACID; MILK; STREPTOCOCCUS THERMOPHILUS;

EID: 80052190507     PISSN: None     EISSN: 14752859     Source Type: Journal    
DOI: 10.1186/1475-2859-10-S1-S22     Document Type: Article

References (75)

1. Orla-Jensen S. The lactic acid bacteria. 1919, Copenhagen: A. F. Host and Son.
2. Euzeby JP. List of Bacterial Names with Standing in Nomenclature: a folder available on the Internet. Int J Syst Bacteriol 1997, 47:590-592. 10.1099/00207713-47-2-590, 9103655.
3. Ott A, Hugi A, Baumgartner M, Chaintreau A. Sensory investigation of yogurt flavor perception: mutual influence of volatiles and acidity. J Agric Food Chem 2000, 48:441-450. 10.1021/jf990432x, 10691654.
4. de Vrese M, Stegelmann A, Richter B, Fenselau S, Laue C, Schrezenmeir J. Probiotics--compensation for lactase insufficiency. Am J Clin Nutr 2001, 73:421S-429S.
5. Garcia-Albiach R, Jose M, de Felipe P, Angulo S, Morosini MI, Bravo D, Baquero F, del Campo R. Molecular analysis of yogurt containing Lactobacillus delbrueckii subsp. bulgaricus and Streptococcus thermophilus in human intestinal microbiota. Am J Clin Nutr 2008, 87:91-96.
6. Meyer AL, Elmadfa I, Herbacek I, Micksche M. Probiotic, as well as conventional yogurt, can enhance the stimulated production of proinflammatory cytokines. J Hum Nutr Diet 2007, 20:590-598. 10.1111/j.1365-277X.2007.00807.x, 18001380.
7. Rodriguez C, Medici M, Rodriguez AV, Mozzi F, Font de Valdez G. Prevention of chronic gastritis by fermented milks made with exopolysaccharide-producing Streptococcus thermophilus strains. J Dairy Sci 2009, 92:2423-2434. 10.3168/jds.2008-1724, 19447974.
8. Zhu Y, Xiao L, Shen D, Hao Y. Competition between yogurt probiotics and periodontal pathogens in vitro. Acta Odontol Scand 2010, 68:261-268. 10.3109/00016357.2010.492235, 20491536.
9. Bolotin A, Quinquis B, Renault P, Sorokin A, Ehrlich SD, Kulakauskas S, Lapidus A, Goltsman E, Mazur M, Pusch GD, et al. Complete sequence and comparative genome analysis of the dairy bacterium Streptococcus thermophilus. Nat Biotechnol 2004, 22:1554-1558. 10.1038/nbt1034, 15543133.
10. Makarova K, Slesarev A, Wolf Y, Sorokin A, Mirkin B, Koonin E, Pavlov A, Pavlova N, Karamychev V, Polouchine N, et al. Comparative genomics of the lactic acid bacteria. Proc Natl Acad Sci U S A 2006, 103:15611-15616. 10.1073/pnas.0607117103, 1622870, 17030793.
11. Fontaine L, Boutry C, de Frahan MH, Delplace B, Fremaux C, Horvath P, Boyaval P, Hols P. A novel pheromone quorum-sensing system controls the development of natural competence in Streptococcus thermophilus and Streptococcus salivarius. J Bacteriol 2010, 192:1444-1454. 10.1128/JB.01251-09, 2820839, 20023010.
12. Fontaine L, Boutry C, Guedon E, Guillot A, Ibrahim M, Grossiord B, Hols P. Quorum-sensing regulation of the production of Blp bacteriocins in Streptococcus thermophilus. J Bacteriol 2007, 189:7195-7205. 10.1128/JB.00966-07, 2168441, 17693498.
13. Fontaine L, Hols P. The inhibitory spectrum of thermophilin 9 from Streptococcus thermophilus LMD-9 depends on the production of multiple peptides and the activity of BlpG(St), a thiol-disulfide oxidase. Appl Environ Microbiol 2008, 74:1102-1110. 10.1128/AEM.02030-07, 2258595, 18156339.
14. Gardan R, Besset C, Guillot A, Gitton C, Monnet V. The oligopeptide transport system is essential for the development of natural competence in Streptococcus thermophilus strain LMD-9. J Bacteriol 2009, 191:4647-4655. 10.1128/JB.00257-09, 2704715, 19447907.
15. Ibrahim M, Guillot A, Wessner F, Algaron F, Besset C, Courtin P, Gardan R, Monnet V. Control of the transcription of a short gene encoding a cyclic peptide in Streptococcus thermophilus: a new quorum-sensing system?. J Bacteriol 2007, 189:8844-8854. 10.1128/JB.01057-07, 2168622, 17921293.
16. Hols P, Hancy F, Fontaine L, Grossiord B, Prozzi D, Leblond-Bourget N, Decaris B, Bolotin A, Delorme C, Dusko Ehrlich S, et al. New insights in the molecular biology and physiology of Streptococcus thermophilus revealed by comparative genomics. FEMS Microbiol Rev 2005, 29:435-463.
17. Barrangou R, Fremaux C, Deveau H, Richards M, Boyaval P, Moineau S, Romero DA, Horvath P. CRISPR provides acquired resistance against viruses in prokaryotes. Science 2007, 315:1709-1712. 10.1126/science.1138140, 17379808.
18. Horvath P, Romero DA, Coute-Monvoisin AC, Richards M, Deveau H, Moineau S, Boyaval P, Fremaux C, Barrangou R. Diversity, activity, and evolution of CRISPR loci in Streptococcus thermophilus. J Bacteriol 2008, 190:1401-1412. 10.1128/JB.01415-07, 2238196, 18065539.
19. Sherman JM. The streptococci. Bacteriol Rev 1937, 1:3-97. 440821, 16350049.
20. Rasmussen TB, Danielson M, Valina O, Johansen E, Pederson MB. The Streptococcus thermophilus core genome - a comparative genome hybridization study of 47 strains. Appl Environ Microbiol 2008, 74:4703-4710. 10.1128/AEM.00132-08, 2519362, 18539806.
21. Altermann E, Klaenhammer TR. GAMOLA: a new local solution for sequence annotation and analyzing draft and finished prokaryotic genomes. Omics 2003, 7:161-169. 10.1089/153623103322246557, 14506845.
22. Rutherford K, Parkhill J, Crook J, Horsnell T, Rice P, Rajandream MA, Barrell B. Artemis: sequence visualization and annotation. Bioinformatics 2000, 16:944-945. 10.1093/bioinformatics/16.10.944, 11120685.
23. Delcher AL, Bratke KA, Powers EC, Salzberg SL. Identifying bacterial genes and endosymbiont DNA with Glimmer. Bioinformatics 2007, 23:673-679. 10.1093/bioinformatics/btm009, 2387122, 17237039.
24. Altschul SF, Madden TL, Schaffer AA, Zhang J, Zhang Z, Miller W, Lipman DJ. Gapped BLAST and PSI-BLAST: a new generation of protein database search programs. Nucleic Acids Res 1997, 25:3389-3402. 10.1093/nar/25.17.3389, 146917, 9254694.
25. Tatusov RL, Fedorova ND, Jackson JD, Jacobs AR, Kiryutin B, Koonin EV, Krylov DM, Mazumder R, Mekhedov SL, Nikolskaya AN, et al. The COG database: an updated version includes eukaryotes. BMC Bioinformatics 2003, 4:41. 10.1186/1471-2105-4-41, 222959, 12969510.
26. Eddy SR. A new generation of homology search tools based on probabilistic inference. Genome Inform 2009, 23:205-211.
27. Bateman A, Birney E, Cerruti L, Durbin R, Etwiller L, Eddy SR, Griffiths-Jones S, Howe KL, Marshall M, Sonnhammer EL. The Pfam protein families database. Nucleic Acids Res 2002, 30:276-280. 10.1093/nar/30.1.276, 99071, 11752314.
28. Krogh A, Larsson B, von Heijne G, Sonnhammer EL. Predicting transmembrane protein topology with a hidden Markov model: application to complete genomes. J Mol Biol 2001, 305:567-580. 10.1006/jmbi.2000.4315, 11152613.
29. Bendtsen JD, Nielsen H, von Heijne G, Brunak S. Improved prediction of signal peptides: SignalP 3.0. J Mol Biol 2004, 340:783-795. 10.1016/j.jmb.2004.05.028, 15223320.
30. Bendtsen JD, Nielsen H, Widdick D, Palmer T, Brunak S. Prediction of twin-arginine signal peptides. BMC Bioinformatics 2005, 6:167. 10.1186/1471-2105-6-167, 1182353, 15992409.
31. Kerkhoven R, van Enckevort FH, Boekhorst J, Molenaar D, Siezen RJ. Visualization for genomics: the Microbial Genome Viewer. Bioinformatics 2004, 20:1812-1814. 10.1093/bioinformatics/bth159, 14988111.
32. Yang J, Wang J, Yao ZJ, Jin Q, Shen Y, Chen R. GenomeComp: a visualization tool for microbial genome comparison. J Microbiol Methods 2003, 54:423-426. 10.1016/S0167-7012(03)00094-0, 12842490.
33. Altermann E, Klaenhammer TR. PathwayVoyager: pathway mapping using the Kyoto Encyclopedia of Genes and Genomes (KEGG) database. BMC Genomics 2005, 6:60. 10.1186/1471-2164-6-60, 1112592, 15869710.
34. Sneath PH, Sokal RR. Numerical taxonomy. Nature 1962, 193:855-860. 10.1038/193855a0, 13914561.
35. Tamura K, Dudley J, Nei M, Kumar S. MEGA4: Molecular Evolutionary Genetics Analysis (MEGA) software version 4.0. Mol Biol Evol 2007, 24:1596-1599. 10.1093/molbev/msm092, 17488738.
36. Carver TJ, Rutherford KM, Berriman M, Rajandream MA, Barrell BG, Parkhill J. ACT: the Artemis Comparison Tool. Bioinformatics 2005, 21:3422-3423. 10.1093/bioinformatics/bti553, 15976072.
37. Monnet C, Ulve V, Sarthou AS, Irlinger F. Extraction of RNA from cheese without prior separation of microbial cells. Appl Environ Microbiol 2008, 74:5724-5730. 10.1128/AEM.00716-08, 2547026, 18658279.
38. Liu M, Siezen RJ, Nauta A. In silico prediction of horizontal gene transfer events in Lactobacillus bulgaricus and Streptococcus thermophilus reveals protocooperation in yogurt manufacturing. Appl Environ Microbiol 2009, 75:4120-4129. 10.1128/AEM.02898-08, 2698337, 19395564.
39. Delorme C, Bartholini C, Bolotine A, Ehrlich SD, Renault P. Emergence of a cell wall protease in the Streptococcus thermophilus population. Appl Environ Microbiol 2010, 76:451-460. 10.1128/AEM.01018-09, 2805209, 19915034.
40. Fernandez A, Thibessard A, Borges F, Gintz B, Decaris B, Leblond-Bourget N. Characterization of oxidative stress-resistant mutants of Streptococcus thermophilus CNRZ368. Arch Microbiol 2004, 182:364-372. 10.1007/s00203-004-0712-2, 15378231.
41. Kawamura Y, Hou XG, Sultana F, Miura H, Ezaki T. Determination of 16S rRNA sequences of Streptococcus mitis and Streptococcus gordonii and phylogenetic relationships among members of the genus Streptococcus. Int J Syst Bacteriol 1995, 45:406-408. 10.1099/00207713-45-2-406, 7537076.
42. Tettelin H, Nelson KE, Paulsen IT, Eisen JA, Read TD, Peterson S, Heidelberg J, DeBoy RT, Haft DH, Dodson RJ, et al. Complete genome sequence of a virulent isolate of Streptococcus pneumoniae. Science 2001, 293:498-506. 10.1126/science.1061217, 11463916.
43. Ding F, Tang P, Hsu MH, Cui P, Hu S, Yu J, Chiu CH. Genome evolution driven by host adaptations results in a more virulent and antimicrobial-resistant Streptococcus pneumoniae serotype 14. BMC Genomics 2009, 10:158. 10.1186/1471-2164-10-158, 2678160, 19361343.
44. Smoot JC, Barbian KD, Van Gompel JJ, Smoot LM, Chaussee MS, Sylva GL, Sturdevant DE, Ricklefs SM, Porcella SF, Parkins LD, et al. Genome sequence and comparative microarray analysis of serotype M18 group A Streptococcus strains associated with acute rheumatic fever outbreaks. Proc Natl Acad Sci U S A 2002, 99:4668-4673. 10.1073/pnas.062526099, 123705, 11917108.
45. Nakagawa I, Kurokawa K, Yamashita A, Nakata M, Tomiyasu Y, Okahashi N, Kawabata S, Yamazaki K, Shiba T, Yasunaga T, et al. Genome sequence of an M3 strain of Streptococcus pyogenes reveals a large-scale genomic rearrangement in invasive strains and new insights into phage evolution. Genome Res 2003, 13:1042-1055. 10.1101/gr.1096703, 403657, 12799345.
46. Beres SB, Sylva GL, Sturdevant DE, Granville CN, Liu M, Ricklefs SM, Whitney AR, Parkins LD, Hoe NP, Adams GJ, et al. Genome-wide molecular dissection of serotype M3 group A Streptococcus strains causing two epidemics of invasive infections. Proc Natl Acad Sci U S A 2004, 101:11833-11838. 10.1073/pnas.0404163101, 511060, 15282372.
47. Holden MT, Scott A, Cherevach I, Chillingworth T, Churcher C, Cronin A, Dowd L, Feltwell T, Hamlin N, Holroyd S, et al. Complete genome of acute rheumatic fever-associated serotype M5 Streptococcus pyogenes strain Manfredo. J Bacteriol 2007, 189:1473-1477. 10.1128/JB.01227-06, 1797351, 17012393.
48. McShan WM, Ferretti JJ, Karasawa T, Suvorov AN, Lin S, Qin B, Jia H, Kenton S, Najar F, Wu H, et al. Genome sequence of a nephritogenic and highly transformable M49 strain of Streptococcus pyogenes. J Bacteriol 2008, 190:7773-7785. 10.1128/JB.00672-08, 2583620, 18820018.
49. Arioli S, Monnet C, Guglielmetti S, Parini C, De Noni I, Hogenboom J, Halami PM, Mora D. Aspartate biosynthesis is essential for the growth of Streptococcus thermophilus in milk, and aspartate availability modulates the level of urease activity. Appl Environ Microbiol 2007, 73:5789-5796. 10.1128/AEM.00533-07, 2074928, 17660309.
50. Ajdic D, McShan WM, McLaughlin RE, Savic G, Chang J, Carson MB, Primeaux C, Tian R, Kenton S, Jia H, et al. Genome sequence of Streptococcus mutans UA159, a cariogenic dental pathogen. Proc Natl Acad Sci U S A 2002, 99:14434-14439. 10.1073/pnas.172501299, 137901, 12397186.
51. Xu P, Alves JM, Kitten T, Brown A, Chen Z, Ozaki LS, Manque P, Ge X, Serrano MG, Puiu D, et al. Genome of the opportunistic pathogen Streptococcus sanguinis. J Bacteriol 2007, 189:3166-3175. 10.1128/JB.01808-06, 1855836, 17277061.
52. van de Guchte M, Penaud S, Grimaldi C, Barbe V, Bryson K, Nicolas P, Robert C, Oztas S, Mangenot S, Couloux A, et al. The complete genome sequence of Lactobacillus bulgaricus reveals extensive and ongoing reductive evolution. Proc Natl Acad Sci U S A 2006, 103:9274-9279. 10.1073/pnas.0603024103, 1482600, 16754859.
53. Kuhn A. From the Sec complex to the membrane insertase YidC. Biol Chem 2009, 390:701-706. 10.1515/BC.2009.059, 19361278.
54. Abe A. [Bacterial secretion systems: their function and contribution to disease process]. Kansenshogaku Zasshi 2009, 83:94-100.
55. Bourgoin F, Pluvinet A, Gintz B, Decaris B, Guedon G. Are horizontal transfers involved in the evolution of the Streptococcus thermophilus exopolysaccharide synthesis loci?. Gene 1999, 233:151-161. 10.1016/S0378-1119(99)00144-4, 10375631.
56. Broadbent JR, McMahon DJ, Welker DL, Oberg CJ, Moineau S. Biochemistry, genetics, and applications of exopolysaccharide production in Streptococcus thermophilus: a review. J Dairy Sci 2003, 86:407-423. 10.3168/jds.S0022-0302(03)73619-4, 12647947.
57. Makino S, Ikegami S, Kano H, Sashihara T, Sugano H, Horiuchi H, Saito T, Oda M. Immunomodulatory effects of polysaccharides produced by Lactobacillus delbrueckii ssp. bulgaricus OLL1073R-1. J Dairy Sci 2006, 89:2873-2881. 10.3168/jds.S0022-0302(06)72560-7, 16840603.
58. van den Bogaard PT, Hols P, Kuipers OP, Kleerebezem M, de Vos WM. Sugar utilisation and conservation of the gal-lac gene cluster in Streptococcus thermophilus. Syst Appl Microbiol 2004, 27:10-17. 10.1078/0723-2020-00258, 15053316.
59. Vaillancourt K, Moineau S, Frenette M, Lessard C, Vadeboncoeur C. Galactose and lactose genes from the galactose-positive bacterium Streptococcus salivarius and the phylogenetically related galactose-negative bacterium Streptococcus thermophilus: organization, sequence, transcription, and activity of the gal gene products. J Bacteriol 2002, 184:785-793. 10.1128/JB.184.3.785-793.2002, 139519, 11790749.
60. Brooker JD, McCarthy JM. Gene knockout of the intracellular amylase gene by homologous recombination in Streptococcus bovis. Curr Microbiol 1997, 35:133-138. 10.1007/s002849900226, 9236293.
61. Satoh E, Uchimura T, Kudo T, Komagata K. Purification, characterization, and nucleotide sequence of an intracellular maltotriose-producing alpha-amylase from Streptococcus bovis 148. Appl Environ Microbiol 1997, 63:4941-4944. 168820, 9406414.
62. Simpson CL, Russell RR. Intracellular alpha-amylase of Streptococcus mutans. J Bacteriol 1998, 180:4711-4717. 107487, 9721315.
63. Bonifait L, de la Cruz Dominguez-Punaro M, Vaillancourt K, Bart C, Slater J, Frenette M, Gottschalk M, Grenier D. The cell envelope subtilisin-like proteinase is a virulence determinant for Streptococcus suis. BMC Microbiol 10:42.
64. Courtin P, Monnet V, Rul F. Cell-wall proteinases PrtS and PrtB have a different role in Streptococcus thermophilus/Lactobacillus bulgaricus mixed cultures in milk. Microbiology 2002, 148:3413-3421.
65. Geis A, El Demerdash HA, Heller KJ. Sequence analysis and characterization of plasmids from Streptococcus thermophilus. Plasmid 2003, 50:53-69. 10.1016/S0147-619X(03)00029-5, 12826058.
66. Solow BT, Somkuti GA. Comparison of low-molecular-weight heat stress proteins encoded on plasmids in different strains of Streptococcus thermophilus. Curr Microbiol 2000, 41:177-181. 10.1007/s002840010114, 10915203.
67. Wouters JA, Sanders JW, Kok J, de Vos WM, Kuipers OP, Abee T. Clustered organization and transcriptional analysis of a family of five csp genes of Lactococcus lactis MG1363. Microbiology 1998, 144:2885-2893. 10.1099/00221287-144-10-2885, 9802030.
68. Yamaguchi M, Terao Y, Ogawa T, Takahashi T, Hamada S, Kawabata S. Role of Streptococcus sanguinis sortase A in bacterial colonization. Microbes Infect 2006, 8:2791-2796. 10.1016/j.micinf.2006.08.010, 17045503.
69. Leigh JA, Egan SA, Ward PN, Field TR, Coffey TJ. Sortase anchored proteins of Streptococcus uberis play major roles in the pathogenesis of bovine mastitis in dairy cattle. Vet Res 2010, 41:63. 10.1051/vetres/2010036, 2898060, 20519112.
70. Ventura M, O'Flaherty S, Claesson MJ, Turroni F, Klaenhammer TR, van Sinderen D, O'Toole PW. Genome-scale analyses of health-promoting bacteria: probiogenomics. Nat Rev Microbiol 2009, 7:61-71. 10.1038/nrmicro2047, 19029955.
71. Li W, Liu L, Chen H, Zhou R. Identification of Streptococcus suis genes preferentially expressed under iron starvation by selective capture of transcribed sequences. FEMS Microbiol Lett 2009, 292:123-133. 10.1111/j.1574-6968.2008.01476.x, 19191874.
72. Osaki M, Takamatsu D, Shimoji Y, Sekizaki T. Characterization of Streptococcus suis genes encoding proteins homologous to sortase of gram-positive bacteria. J Bacteriol 2002, 184:971-982. 10.1128/jb.184.4.971-982.2002, 134807, 11807057.
73. Pederson MB, Iverson SL, Sorenson KI, Johansen E. The long and winding road from the research laboratory to industrial applications of lactic acid bacteria. FEMS Microbiol Rev 2005, 29:611-624. 10.1016/j.fmrre.2005.04.001, 15935510.
74. Mills S, Griffin C, Coffey A, Mijer WC, Hafkamp B, Ross RP. CRISPR analysis of bacteriphage-insensitive mutants (BIMs) of industrial Streptococcus thermophilus - implications for starter design. J Appl Microbiol 2010, 108:945-955. 10.1111/j.1365-2672.2009.04486.x, 19709335.
75. Herve-Jimenez L, Guillouard I, Guedon E, Boudebbouze S, Hols P, Monnet V, Maguin E, Rul F. Postgenomic analysis of Streptococcus thermophilus cocultivated in milk with Lactobacillus delbrueckii subsp. bulgaricus: involvement of nitrogen, purine, and iron metabolism. Appl Environ Microbiol 2009, 75:2062-2073. 10.1128/AEM.01984-08, 2663229, 19114510.