Comparative genomic and proteomic analyses of two Mycoplasma agalactiae strains: Clues to the macro- and micro-events that are shaping mycoplasma diversity

BMC Genomics

Volumn 11, Issue 1, 2010, Pages

  Nouvel, Laurent X ^a,b   Sirand Pugnet, Pascal ^c,d   Marenda, Marc S ^a,b,f   Sagné, Eveline ^a,b   Barbe, Valérie ^e   Mangenot, Sophie ^e   Schenowitz, Chantal ^e   Jacob, Daniel ^c   Barré, Aurélien ^c   Claverol, Stéphane ^c   Blanchard, Alain ^c,d   Citti, Christine ^a,b  

^a CNRS   (France)

^b IHAP   (France)

^c UNIVERSITÉ DE BORDEAUX   (France)

^d CEMAGREF   (France)

^e CENTRE NATIONAL DE SÉQUENÇAGE   (France)

^f School of Veterinary Science   (Australia)

Author keywords

[No Author keywords available]

Indexed keywords

ARTICLE; BACTERIAL GENETICS; BACTERIAL STRAIN; COMPARATIVE STUDY; CONTROLLED STUDY; GENE DUPLICATION; GENETIC VARIABILITY; GENOMICS; MICROBIAL DIVERSITY; MYCOPLASMA AGALACTIAE; MYCOPLASMA BOVIS; MYCOPLASMA MYCOIDES; NONHUMAN; NUCLEOTIDE SEQUENCE; PROTEOMICS; SINGLE NUCLEOTIDE POLYMORPHISM; STRAIN DIFFERENCE; AMINO ACID SEQUENCE; BACTERIAL GENOME; COMPARATIVE GENOMIC HYBRIDIZATION; DNA SEQUENCE; GENE EXPRESSION REGULATION; GENE FLOW; GENE POOL; GENETICS; HORIZONTAL GENE TRANSFER; METHODOLOGY; MOLECULAR EVOLUTION; MOLECULAR GENETICS; MULTIGENE FAMILY;

BACTERIA (MICROORGANISMS); MYCOPLASMA; MYCOPLASMA AGALACTIAE; MYCOPLASMA BOVIS; MYCOPLASMA MYCOIDES SUBSP. MYCOIDES; MYCOPLASMATALES;

BACTERIAL DNA;

AMINO ACID SEQUENCE; BASE SEQUENCE; COMPARATIVE GENOMIC HYBRIDIZATION; DNA, BACTERIAL; EVOLUTION, MOLECULAR; GENE FLOW; GENE POOL; GENE TRANSFER, HORIZONTAL; GENOME, BACTERIAL; MOLECULAR SEQUENCE DATA; MULTIGENE FAMILY; MUTAGENESIS, INSERTIONAL; MYCOPLASMA AGALACTIAE; POLYMORPHISM, SINGLE NUCLEOTIDE; PROTEOMICS; SEQUENCE ANALYSIS, DNA;

EID: 77349083975     PISSN: None     EISSN: 14712164     Source Type: Journal    
DOI: 10.1186/1471-2164-11-86     Document Type: Article

References (63)

1. Dobrindt U, Hacker J. Whole genome plasticity in pathogenic bacteria. Curr Opin Microbiol 2001, 4(5):550-557. 10.1016/S1369-5274(00)00250-2, 11587932.
2. Medini D, Donati C, Tettelin H, Masignani V, Rappuoli R. The microbial pan-genome. Curr Opin Genet Dev 2005, 15(6):589-594. 10.1016/j.gde.2005.09.006, 16185861.
3. Tettelin H, Masignani V, Cieslewicz MJ, Donati C, Medini D, Ward NL, Angiuoli SV, Crabtree J, Jones AL, Durkin AS, et al. Genome analysis of multiple pathogenic isolates of Streptococcus agalactiae: implications for the microbial "pan-genome". Proc Natl Acad Sci USA 2005, 102(39):13950-13955. 10.1073/pnas.0506758102, 1216834,1216834, 16172379.
4. Fraser CMGocayne JD, White O, Adams MD, Clayton RA, Fleischmann RD, Bult CJ, Kerlavage AR, Sutton G, Kelley JM, et al. The minimal gene complement of Mycoplasma genitalium. Science 1995, 270(5235):397-403. 10.1126/science.270.5235.397, 7569993.
5. Ciccarelli FD, Doerks T, von Mering C, Creevey CJ, Snel B, Bork P. Toward automatic reconstruction of a highly resolved tree of life. Science 2006, 311(5765):1283-1287. 10.1126/science.1123061, 16513982.
6. Sirand-Pugnet P, Citti C, Barre A, Blanchard A. Evolution of mollicutes: down a bumpy road with twists and turns. Res Microbiol 2007, 158(10):754-766. 10.1016/j.resmic.2007.09.007, 18023150.
7. Dybvig K, Zuhua C, Lao P, Jordan DS, French CT, Tu AH, Loraine AE. Genome of Mycoplasma arthritidis. Infect Immun 2008, 76(9):4000-4008. 10.1128/IAI.00516-08, 2519406, 18573899.
8. Calderon-Copete SP, Wigger G, Wunderlin C, Schmidheini T, Frey J, Quail MA, Falquet L. The Mycoplasma conjunctivae genome sequencing, annotation and analysis. BMC Bioinformatics 2009, 10(Suppl6):S7. 10.1186/1471-2105-10-S6-S7, 2697654, 19534756.
9. Minion FC, Lefkowitz EJ, Madsen ML, Cleary BJ, Swartzell SM, Mahairas GG. The genome sequence of Mycoplasma hyopneumoniae strain 232, the agent of swine mycoplasmosis. J Bacteriol 2004, 186(21):7123-7133. 10.1128/JB.186.21.7123-7133.2004, 523201, 15489423.
10. Vasconcelos AT, Ferreira HB, Bizarro CV, Bonatto SL, Carvalho MO, Pinto PM, Almeida DF, Almeida LG, Almeida R, Alves-Filho L, et al. Swine and poultry pathogens: the complete genome sequences of two strains of Mycoplasma hyopneumoniae and a strain of Mycoplasma synoviae. J Bacteriol 2005, 187(16):5568-5577. 10.1128/JB.187.16.5568-5577.2005, 1196056, 16077101.
11. Rosengarten R, Citti C, Much P, Spergser J, Droesse M, Hewicker-Trautwein M. The changing image of mycoplasmas: from innocent bystanders to emerging and reemerging pathogens in human and animal diseases. Contrib Microbiol 2001, 8:166-185. full_text, 11764733.
12. Sirand-Pugnet P, Lartigue C, Marenda M, Jacob D, Barre A, Barbe V, Schenowitz C, Mangenot S, Couloux A, Segurens B, et al. Being pathogenic, plastic, and sexual while living with a nearly minimal bacterial genome. PLoS Genet 2007, 3(5):e75. 10.1371/journal.pgen.0030075, 1868952,1868952, 17511520.
13. Solsona M, Lambert M, Poumarat F. Genomic, protein homogeneity and antigenic variability of Mycoplasma agalactiae. Vet Microbiol 1996, 50(1-2):45-58. 10.1016/0378-1135(95)00200-6, 8810007.
14. Marenda MS, Sagne E, Poumarat F, Citti C. Suppression subtractive hybridization as a basis to assess Mycoplasma agalactiae and Mycoplasma bovis genomic diversity and species-specific sequences. Microbiology 2005, 151(Pt 2).
15. McAuliffe L, Churchward CP, Lawes JR, Loria G, Ayling RD, Nicholas RA. VNTR analysis reveals unexpected genetic diversity within Mycoplasma agalactiae, the main causative agent of contagious agalactia. BMC Microbiol 2008, 8(193). 2585094, 18992155.
16. Marenda M, Barbe V, Gourgues G, Mangenot S, Sagne E, Citti C. A new integrative conjugative element occurs in Mycoplasma agalactiae as chromosomal and free circular forms. J Bacteriol 2006, 188(11):4137-4141. 10.1128/JB.00114-06, 1482908, 16707706.
17. Nouvel LX, Marenda M, Sirand-Pugnet P, Sagne E, Glew M, Mangenot S, Barbe V, Barre A, Claverol S, Citti C. Occurrence, plasticity, and evolution of the vpma gene family, a genetic system devoted to high-frequency surface variation in Mycoplasma agalactiae. J Bacteriol 2009, 191(13):4111-4121. 10.1128/JB.00251-09, 2698505, 19376859.
18. Marenda MS, Vilei EM, Poumarat F, Frey J, Berthelot X. Validation of the suppressive subtractive hybridization method in Mycoplasma agalactiae species by the comparison of a field strain with the type strain PG2. Vet Res 2004, 35(2):199-212. 10.1051/vetres:2004006, 15099496.
19. Frey J. Mycoplasmas of Animals. Molecular biology and pathogenicity of Mycoplasmas 2002, 73-90. New York (USA): Kluwer Academic/Plenum Publishers, Razin S, Herrmann R.
20. Corrales JC, Esnal A, De la Fe C, Sanchez A, Assuncao P, Poveda JB, Contreras A. Contagious agalactia in small ruminants. Small Ruminant Res 2007, 68(1-2):154-166.
21. Tola S, Crobeddu S, Chessa G, Uzzau S, Idini G, Ibba B, Rocca S. Sequence, cloning, expression and characterisation of the 81-kDa surface membrane protein (P80) of Mycoplasma agalactiae. FEMS Microbiol Lett 2001, 202(1):45-50. 10.1111/j.1574-6968.2001.tb10778.x, 11506906.
22. Fleury B, Bergonier D, Berthelot X, Peterhans E, Frey J, Vilei EM. Characterization of P40, a cytadhesin of Mycoplasma agalactiae. Infect Immun 2002, 70(10):5612-5621. 10.1128/IAI.70.10.5612-5621.2002, 128363, 12228289.
23. Rosati S, Robino P, Fadda M, Pozzi S, Mannelli A, Pittau M. Expression and antigenic characterization of recombinant Mycoplasma agalactiae P48 major surface protein. Vet Microbiol 2000, 71(3-4):201-210. 10.1016/S0378-1135(99)00164-9, 10703704.
24. Fleury B, Bergonier D, Berthelot X, Schlatter Y, Frey J, Vilei EM. Characterization and analysis of a stable serotype-associated membrane protein (P30) of Mycoplasma agalactiae. J Clin Microbiol 2001, 39(8):2814-2822. 10.1128/JCM.39.8.2814-2822.2001, 88244, 11473997.
25. Glew MD, Papazisi L, Poumarat F, Bergonier D, Rosengarten R, Citti C. Characterization of a multigene family undergoing high-frequency DNA rearrangements and coding for abundant variable surface proteins in Mycoplasma agalactiae. Infect Immun 2000, 68(8):4539-4548. 10.1128/IAI.68.8.4539-4548.2000, 98368, 10899853.
26. Chopra-Dewasthaly R, Citti C, Glew MD, Zimmermann M, Rosengarten R, Jechlinger W. Phase-locked mutants of Mycoplasma agalactiae: defining the molecular switch of high-frequency Vpma antigenic variation. Mol Microbiol 2008, 67(6):1196-1210. 10.1111/j.1365-2958.2007.06103.x, 2268961, 18248580.
27. Demina IA, Serebryakova MV, Ladygina VG, Rogova MA, Zgoda VG, Korzhenevskyi DA, Govorun VM. Proteome of the bacterium Mycoplasma gallisepticum. Biochemistry (Mosc) 2009, 74(2):165-174. 10.1134/S0006297909020072, 19267672.
28. Calcutt MJ, Lewis MS, Wise KS. Molecular genetic analysis of ICEF, an integrative conjugal element that is present as a repetitive sequence in the chromosome of Mycoplasma fermentans PG18. J Bacteriol 2002, 184(24):6929-6941. 10.1128/JB.184.24.6929-6941.2002, 135467, 12446643.
29. Pilo P, Fleury B, Marenda M, Frey J, Vilei EM. Prevalence and distribution of the insertion element ISMag1 in Mycoplasma agalactiae. Vet Microbiol 2003, 92(1-2):37-48. 10.1016/S0378-1135(02)00311-5, 12488069.
30. Thomas A, Linden A, Mainil J, Bischof DF, Frey J, Vilei EM. Mycoplasma bovis shares insertion sequences with Mycoplasma agalactiae and Mycoplasma mycoides subsp. mycoides SC: Evolutionary and developmental aspects. FEMS Microbiol Lett 2005, 245(2):249-255. 10.1016/j.femsle.2005.03.013, 15837379.
31. Lysnyansky I, Calcutt MJ, Ben-Barak I, Ron Y, Levisohn S, Methe BA, Yogev D. Molecular characterization of newly identified IS3, IS4 and IS30 insertion sequence-like elements in Mycoplasma bovis and their possible roles in genome plasticity. 2009, 294(2):172-182.
32. Breton M, Sagne E, Duret S, Beven L, Citti C, Renaudin J. First report of a tetracycline-inducible gene expression system for mollicutes. Microbiology 2010, 156(1):198-205. 10.1099/mic.0.034074-0, 19797362.
33. Citti C, Browning GF, Rosengarten R. Phenotypic diversity and cell invasion in host subversion by pathogenic mycoplasmas. Mycoplasmas: Molecular biology, pathogenicity and strategies for control 2005, 439-484. Norfolk (United Kingdom): Horizon Bioscience, Blanchard A, Browning GF.
34. Schell MA, Karmirantzou M, Snel B, Vilanova D, Berger B, Pessi G, Zwahlen MC, Desiere F, Bork P, Delley M. The genome sequence of Bifidobacterium longum reflects its adaptation to the human gastrointestinal tract. Proc Natl Acad Sci USA 2002, 99(22):14422-14427. 10.1073/pnas.212527599, 137899, 12381787.
35. Chambaud I, Heilig R, Ferris S, Barbe V, Samson D, Galisson F, Moszer I, Dybvig K, Wroblewski H, Viari A, et al. The complete genome sequence of the murine respiratory pathogen Mycoplasma pulmonis. Nucleic Acids Res 2001, 29(10):2145-2153. 10.1093/nar/29.10.2145, 55444, 11353084.
36. Sitaraman R, Denison AM, Dybvig K. A unique bifunctional site-specific DNA recombinase from Mycoplasma pulmonis. Mol Microbiol 2002, 46(4):1033-1040. 10.1046/j.1365-2958.2002.03206.x, 12421309.
37. Lartigue C, Glass JI, Alperovich N, Pieper R, Parmar PP, Hutchison CA, Smith HO, Venter JC. Genome transplantation in bacteria: changing one species to another. Science 2007, 317(5838):632-638. 10.1126/science.1144622, 17600181.
38. Lartigue C, Vashee S, Algire MA, Chuang RY, Benders GA, Ma L, Noskov VN, Denisova EA, Gibson DG, Assad-Garcia N. Creating Bacterial Strains from Genomes That Have Been Cloned and Engineered in Yeast. Science 2009, 325(5948):1693-1696. 10.1126/science.1173759, 19696314.
39. Tettelin H, Riley D, Cattuto C, Medini D. Comparative genomics: the bacterial pan-genome. Curr Opin Microbiol 2008, 11(5):472-477. 10.1016/j.mib.2008.09.006, 19086349.
40. Whitworth DE. Genomes and knowledge - a questionable relationship?. Trends Microbiol 2008, 16(11):512-519. 10.1016/j.tim.2008.08.001, 18819801.
41. Churchward G. Back to the future: the new ICE age. Mol Microbiol 2008, 70(3):554-556. 10.1111/j.1365-2958.2008.06415.x, 18761693.
42. Teachman AM, French CT, Yu H, Simmons WL, Dybvig K. Gene transfer in Mycoplasma pulmonis. J Bacteriol 2002, 184(4):947-951. 10.1128/jb.184.4.947-951.2002, 134802, 11807054.
43. Mahillon J, Chandler M. Insertion sequences. Microbiol Mol Biol Rev 1998, 62(3):725-774. 98933, 9729608.
44. Thomas CM, Nielsen KM. Mechanisms of, and barriers to, horizontal gene transfer between bacteria. Nat Rev Microbiol 2005, 3(9):711-721. 10.1038/nrmicro1234, 16138099.
45. Heusipp G, Falker S, Schmidt MA. DNA adenine methylation and bacterial pathogenesis. Int J Med Microbiol 2007, 297(1):1-7. 10.1016/j.ijmm.2006.10.002, 17126598.
46. Hernday AD, Braaten BA, Low DA. The mechanism by which DNA adenine methylase and PapI activate the pap epigenetic switch. Mol Cell 2003, 12(4):947-957. 10.1016/S1097-2765(03)00383-6, 14580345.
47. Glew MD, Marenda M, Rosengarten R, Citti C. Surface diversity in Mycoplasma agalactiae is driven by site-specific DNA inversions within the vpma multigene locus. J Bacteriol 2002, 184(21):5987-5998. 10.1128/JB.184.21.5987-5998.2002, 135373, 12374833.
48. Lysnyansky I, Yogev D, Levisohn S. Molecular characterization of the Mycoplasma bovis p68 gene, encoding a basic membrane protein with homology to P48 of Mycoplasma agalactiae. FEMS Microbiol Lett 2008, 279(2):234-242. 10.1111/j.1574-6968.2007.01040.x, 18194339.
49. Lapierre P, Gogarten JP. Estimating the size of the bacterial pan-genome. Trends Genet 2009, 25(3):107-110. 10.1016/j.tig.2008.12.004, 19168257.
50. Aluotto BB, Wittler RG, Williams CO, Faber JE. Standardized bacteriologic techniques for the characterization of mycoplasma species. Int J Syst Bacteriol 1970, 20:35-58.
51. Tully JG. Culture medium formulation for primary isolation and maintenance of mollicutes. Molecular and Diagnostic Procedures in Mycoplasmology: Molecular Characterization 1995, 33-39. San Diego: Academic Press, Tully JG.
52. Sambrook J, Fritsch EF, Maniatis T. Molecular cloning: a laboratory manual. 1989, N.Y.: Cold Spring Harbor Laboratory Press, 2.
53. Chen WP, Kuo TT. A simple and rapid method for the preparation of gram-negative bacterial genomic DNA. Nucleic Acids Res 1993, 21(9):2260. 10.1093/nar/21.9.2260, 309503, 8502576.
54. Frangeul L, Glaser P, Rusniok C, Buchrieser C, Duchaud E, Dehoux P, Kunst F. CAAT-Box, Contigs-Assembly and Annotation Tool-Box for genome sequencing projects. Bioinformatics 2004, 20(5):790-797. 10.1093/bioinformatics/btg490, 14752000.
55. Lowe TM, Eddy SR. tRNAscan-SE: a program for improved detection of transfer RNA genes in genomic sequence. Nucleic Acids Res 1997, 25(5):955-964. 10.1093/nar/25.5.955, 146525, 9023104.
56. Laslett D, Canback B. ARAGORN, a program to detect tRNA genes and tmRNA genes in nucleotide sequences. Nucleic Acids Res 2004, 32(1):11-16. 10.1093/nar/gkh152, 373265, 14704338.
57. Tamura K, Dudley J, Nei M, Kumar S. MEGA4: Molecular Evolutionary Genetics Analysis (MEGA) software version 4.0. Mol Biol Evol 2007, 24(8):1596-1599. 10.1093/molbev/msm092, 17488738.
58. Barre A, de Daruvar A, Blanchard A. MolliGen, a database dedicated to the comparative genomics of Mollicutes. Nucleic Acids Res 2004, (32 Database):D307-310. 10.1093/nar/gkh114, 308848, 14681420.
59. Rutherford K, Parkhill J, Crook J, Horsnell T, Rice P, Rajandream MA, Barrell B. Artemis: sequence visualization and annotation. Bioinformatics 2000, 16(10):944-945. 10.1093/bioinformatics/16.10.944, 11120685.
60. Carver TJ, Rutherford KM, Berriman M, Rajandream MA, Barrell BG, Parkhill J. ACT: the Artemis Comparison Tool. Bioinformatics 2005, 21(16):3422-3423. 10.1093/bioinformatics/bti553, 15976072.
61. Frazer KA, Pachter L, Poliakov A, Rubin EM, Dubchak I. VISTA: computational tools for comparative genomics. Nucleic Acids Res 2004, (32 Web Server):W273-279. 10.1093/nar/gkh458, 441596, 15215394.
62. Bordier C. Phase separation of integral membrane proteins in Triton X-114 solution. J Biol Chem 1981, 256(4):1604-1607.
63. Carver T, Thomson N, Bleasby A, Berriman M, Parkhill J. DNAPlotter: circular and linear interactive genome visualization. Bioinformatics 2009, 25(1):119-120. 10.1093/bioinformatics/btn578, 2612626,2612626, 18990721.