ICEA of Mycoplasma agalactiae: A new family of self-transmissible integrative elements that confers conjugative properties to the recipient strain

Molecular Microbiology

Volumn 89, Issue 6, 2013, Pages 1226-1239

  Dordet Frisoni, Emilie ^a,b   Marenda, Marc Serge ^c   Sagné, Eveline ^a,b   Nouvel, Laurent Xavier ^a,b   Guérillot, Romain ^d,e,f   Glaser, Philippe ^d,e   Blanchard, Alain ^g,h   Tardy, Florence ^i,j   Sirand Pugnet, Pascal ^g,h   Baranowski, Eric ^a,b   Citti, Christine ^a,b  

^a IHAP   (France)

^b UNIVERSITÉ DE TOULOUSE   (France)

^c UNIVERSITY OF MELBOURNE   (Australia)

^d INSTITUT PASTEUR   (France)

^e CNRS   (France)

^f SORBONNE UNIVERSITÉ   (France)

^g Univ Bordeaux   (France)

^h UNIVERSITÉ DE BORDEAUX   (France)

ⁱ FRENCH AGENCY FOR FOOD   (France)

^j UNIVERSITÉ DE LYON   (France)

more..

Author keywords

[No Author keywords available]

Indexed keywords

BACTERIAL DNA; BACTERIAL PROTEIN; CDS14 PROTEIN; CDS22 PROTEIN; DEOXYRIBONUCLEASE; TRANSPOSASE; UNCLASSIFIED DRUG;

ARTICLE; BACTERIAL CHROMOSOME; BACTERIAL GENE; BACTERIAL GENOME; BACTERIAL STRAIN; BACTERIAL VIRULENCE; BACTERIUM CONJUGATION; CDS14 GENE; CELL VIABILITY; CONTROLLED STUDY; GENE DISRUPTION; GENE STRUCTURE; HORIZONTAL GENE TRANSFER; HOST RANGE; INTEGRATIVE CONJUGATIVE ELEMENT A; MICROBIAL ACTIVITY; MYCOPLASMA AGALACTIAE; NONHUMAN; PRIORITY JOURNAL;

MYCOPLASMA; MYCOPLASMA AGALACTIAE; MYCOPLASMATALES;

BACTERIAL PROTEINS; CONJUGATION, GENETIC; GENE TRANSFER, HORIZONTAL; INTERSPERSED REPETITIVE SEQUENCES; LIPOPROTEINS; MYCOPLASMA AGALACTIAE;

EID: 84884289276     PISSN: 0950382X     EISSN: 13652958     Source Type: Journal    
DOI: 10.1111/mmi.12341     Document Type: Article

References (47)

1. Algire, M.A., Lartigue, C., Thomas, D.W., Assad-Garcia, N., Glass, J.I., and Merryman, C. (2009) New selectable marker for manipulating the simple genomes of Mycoplasma species. Antimicrob Agents Chemother 53: 4429-4432.
2. Aminov, R.I. (2011) Horizontal gene exchange in environmental microbiota. Front Microbiol 2: 158.
3. Bai, X., Fazzolari, T., and Hogenhout, S.A. (2004) Identification and characterization of traE genes of Spiroplasma kunkelii. Gene 336: 81-91.
4. Baranowski, E., Guiral, S., Sagné, E., Skapski, A., and Citti, C. (2010) Critical role of dispensable genes in Mycoplasma agalactiae interaction with mammalian cells. Infect Immun 78: 1542-1551.
5. Barroso, G., and Labarère, J. (1988) Chromosomal gene transfer in Spiroplasma citri. Science 241: 959-961.
6. Breton, M., Tardy, F., Dordet-Frisoni, E., Sagne, E., Mick, V., Renaudin, J., etal. (2012) Distribution and diversity of mycoplasma plasmids: lessons from cryptic genetic elements. BMC Microbiol 12: 257.
7. Brochet, M., Da Cunha, V., Couvé, E., Rusniok, C., Trieu-Cuot, P., and Glaser, P. (2009) Atypical association of DDE transposition with conjugation specifies a new family of mobile elements. Mol Microbiol 71: 948-959.
8. Burrus, V., and Waldor, M.K. (2004) Shaping bacterial genomes with integrative and conjugative elements. Res Microbiol 155: 376-386.
9. Calcutt, M.J., Lewis, M.S., and Wise, K.S. (2002) 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 184: 6929-6941.
10. Carraro, N., Libante, V., Morel, C., Decaris, B., Charron-Bourgoin, F., Leblond, P., and Guédon, G. (2011) Differential regulation of two closely related integrative and conjugative elements from Streptococcus thermophilus. BMC Microbiol 11: 238.
11. Chopra-Dewasthaly, R., Marenda, M., Rosengarten, R., Jechlinger, W., and Citti, C. (2005) Construction of the first shuttle vectors for gene cloning and homologous recombination in Mycoplasma agalactiae. FEMS Microbiol Lett 253: 89-94.
12. Citti, C., and Blanchard, A. (2013) Mycoplasmas and their host: emerging and re-emerging minimal pathogens. Trends Microbiol 21: 196-203.
13. Curcio, M.J., and Derbyshire, K.M. (2003) The outs and ins of transposition: from mu to kangaroo. Nat Rev Mol Cell Biol 4: 865-877.
14. Daccord, A., Ceccarelli, D., and Burrus, V. (2010) Integrating conjugative elements of the SXT/R391 family trigger the excision and drive the mobilization of a new class of Vibrio genomic islands. Mol Microbiol 78: 576-588.
15. Davis, R.E., Dally, E.L., Jomantiene, R., Zhao, Y., Roe, B., Lin, S., and Shao, J. (2005) Cryptic plasmid pSKU146 from the wall-less plant pathogen Spiroplasma kunkelii encodes an adhesin and components of a type IV translocation-related conjugation system. Plasmid 53: 179-190.
16. Dubey, G.P., and Ben-Yehuda, S. (2011) Intercellular nanotubes mediate bacterial communication. Cell 144: 590-600.
17. Dybvig, K., Lao, P., Jordan, D.S., and Simmons, W.L. (2010) Fewer essential genes in mycoplasmas than previous studies suggest. FEMS Microbiol Lett 311: 51-55.
18. Frost, L.S., Leplae, R., Summers, A.O., and Toussaint, A. (2005) Mobile genetic elements: the agents of open source evolution. Nat Rev Microbiol 3: 722-732.
19. Gaillard, M., Pradervand, N., Minoia, M., Sentchilo, V., Johnson, D.R., and van der Meer, J.R. (2010) Transcriptome analysis of the mobile genome ICEclc in Pseudomonas knackmussii B13. BMC Microbiol 10: 153.
20. Ghigo, J.M. (2001) Natural conjugative plasmids induce bacterial biofilm development. Nature 412: 442-445.
21. Glass, J.I., Assad-Garcia, N., Alperovich, N., Yooseph, S., Lewis, M.R., Maruf, M., etal. (2006) Essential genes of a minimal bacterium. Proc Natl Acad Sci USA 103: 425-430.
22. Grohmann, E. (2010) Conjugative transfer of the integrative and conjugative element ICEBs1 from Bacillus subtilis likely initiates at the donor cell pole. J Bacteriol 192: 23-25.
23. Guglielmini, J., Quintais, L., Garcillán-Barcia, M.P., de la Cruz, F., and Rocha, E.P.C. (2011) The repertoire of ICE in prokaryotes underscores the unity, diversity, and ubiquity of conjugation. PLoS Genet 7: e1002222.
24. Guglielmini, J., Cruz, F., and Rocha, E.P.C. (2013) Evolution of conjugation and type IV secretion systems. Mol Biol Evol 30: 315-331.
25. Halary, S., Leigh, J.W., Cheaib, B., Lopez, P., and Bapteste, E. (2010) Network analyses structure genetic diversity in independent genetic worlds. Proc Natl Acad Sci USA 107: 127-132.
26. Halbedel, S., and Stülke, J. (2007) Tools for the genetic analysis of Mycoplasma. Int J Med Microbiol 297: 37-44.
27. Juhas, M., Eberl, L., and Glass, J.I. (2011) Essence of life: essential genes of minimal genomes. Trends Cell Biol 21: 562-568.
28. Kloesges, T., Popa, O., Martin, W., and Dagan, T. (2011) Networks of gene sharing among 329 proteobacterial genomes reveal differences in lateral gene transfer frequency at different phylogenetic depths. Mol Biol Evol 28: 1057-1074.
29. Llosa, M., Gomis-Rüth, F.X., Coll, M., and de la Cruz Fd, F. (2002) Bacterial conjugation: a two-step mechanism for DNA transport. Mol Microbiol 45: 1-8.
30. McAuliffe, L., Ellis, R.J., Miles, K., Ayling, R.D., and Nicholas, R.A.J. (2006) Biofilm formation by mycoplasma species and its role in environmental persistence and survival. Microbiology 152: 913-922.
31. Marenda, M., Barbe, V., Gourgues, G., Mangenot, S., Sagne, E., and Citti, C. (2006) A new integrative conjugative element occurs in Mycoplasma agalactiae as chromosomal and free circular forms. J Bacteriol 188: 4137-4141.
32. Nouvel, L.X., Sirand-Pugnet, P., Marenda, M.S., Sagné, E., Barbe, V., Mangenot, S., etal. (2010) Comparative genomic and proteomic analyses of two Mycoplasma agalactiae strains: clues to the macro- and micro-events that are shaping mycoplasma diversity. BMC Genomics 11: 86.
33. Nouvel, L.-X., Marenda, M.S., Glew, M.D., Sagné, E., Giammarinaro, P., Tardy, F., etal. (2012) Molecular typing of Mycoplasma agalactiae: tracing European-wide genetic diversity and an endemic clonal population. Comp Immunol Microbiol Infect Dis 35: 487-496.
34. Ozbek, E., Miller, S.A., Meulia, T., and Hogenhout, S.A. (2003) Infection and replication sites of Spiroplasma kunkelii (Class: Mollicutes) in midgut and Malpighian tubules of the leafhopper Dalbulus maidis. J Invertebr Pathol 82: 167-175.
35. Pinto, P.M., Carvalho, M.O., Alves-Junior, L., Brocchi, M., and Schrank, I.S. (2007) Molecular analysis of an integrative conjugative element, ICEH, present in the chromosome of different strains of Mycoplasma hyopneumoniae. Genet Mol Biol 30: 256-263.
36. Razin, S., and Hayflick, L. (2010) Highlights of mycoplasma research - an historical perspective. Biologicals 38: 183-190.
37. Razin, S., and Herrmann, R. (2002) Molecular Biology and Pathogenicity of Mycoplasmas. New York, NY: Kluwer Academic/Plenum publishers.
38. Roberts, A.P., and Mullany, P. (2009) A modular master on the move: the Tn916 family of mobile genetic elements. Trends Microbiol 17: 251-258.
39. Sirand-Pugnet, P., Lartigue, C., Marenda, M., Jacob, D., Barré, A., Barbe, V., etal. (2007) Being pathogenic, plastic, and sexual while living with a nearly minimal bacterial genome. PLoS Genet 3: e75.
40. Skapski, A., Hygonenq, M.-C., Sagné, E., Guiral, S., Citti, C., and Baranowski, E. (2011) Genome-scale analysis of Mycoplasma agalactiae loci involved in interaction with host cells. PLoS ONE 6: e25291.
41. Tardy, F., Baranowski, E., Nouvel, L.-X., Mick, V., Manso-Silvàn, L., Thiaucourt, F., etal. (2012) Emergence of atypical Mycoplasma agalactiae strains harboring a new prophage and associated with an alpine wild ungulate mortality episode. Appl Environ Microbiol 78: 4659-4668.
42. Teachman, A.M., French, C.T., Yu, H., Simmons, W.L., and Dybvig, K. (2002) Gene transfer in Mycoplasma pulmonis. J Bacteriol 184: 947-951.
43. Thiaucourt, F., Manso-Silvan, L., Salah, W., Barbe, V., Vacherie, B., Jacob, D., etal. (2011) Mycoplasma mycoides, from 'mycoides Small Colony' to 'capri'. A microevolutionary perspective. BMC Genomics 12: 114.
44. Wise, K.S., Calcutt, M.J., Foecking, M.F., Röske, K., Madupu, R., and Methé, B.A. (2011) Complete genome sequence of Mycoplasma bovis type strain PG45 (ATCC 25523). Infect Immun 79: 982-983.
45. Woese, C.R., Maniloff, J., and Zablen, L.B. (1980) Phylogenetic analysis of the mycoplasmas. Proc Natl Acad Sci USA 77: 494-498.
46. Wozniak, R.A.F., and Waldor, M.K. (2010) Integrative and conjugative elements: mosaic mobile genetic elements enabling dynamic lateral gene flow. Nat Rev Microbiol 8: 552-563.
47. Zimmerman, C.-U., and Herrmann, R. (2005) Synthesis of a small, cysteine-rich, 29 amino acids long peptide in Mycoplasma pneumoniae. FEMS Microbiol Lett 253: 315-321.