Distributive Conjugal Transfer in Mycobacteria Generates Progeny with Meiotic-Like Genome-Wide Mosaicism, Allowing Mapping of a Mating Identity Locus

PLoS Biology

Volumn 11, Issue 7, 2013, Pages

  Gray, Todd A ^a,b   Krywy, Janet A ^b   Harold, Jessica ^a   Palumbo, Michael J ^a   Derbyshire, Keith M ^a,b  

^a WADSWORTH CENTER   (United States)

^b STATE UNIVERSITY OF NEW YORK   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

NUCLEOTIDE;

ARTICLE; BACTERIAL GENOME; BACTERIAL STRAIN; BACTERIUM CONJUGATION; DNA TRANSFER; GENE LOCUS; GENE SEQUENCE; GENETIC ASSOCIATION; GENETIC VARIABILITY; HORIZONTAL GENE TRANSFER; INTROGRESSION; MATING SYSTEM; MEIOSIS; MICROBIAL DIVERSITY; MITOTIC RECOMBINATION; MOSAICISM; MYCOBACTERIUM; MYCOBACTERIUM CANETTII; MYCOBACTERIUM SMEGMATIS; MYCOBACTERIUM TUBERCULOSIS; NONHUMAN; NUCLEOTIDE SEQUENCE; PROGENY; SEQUENCE ALIGNMENT; SINGLE NUCLEOTIDE POLYMORPHISM;

CONJUGATION, GENETIC; GENE TRANSFER, HORIZONTAL; GENES, BACTERIAL; MOSAICISM; MYCOBACTERIUM; MYCOBACTERIUM TUBERCULOSIS;

EID: 84880938874     PISSN: 15449173     EISSN: 15457885     Source Type: Journal    
DOI: 10.1371/journal.pbio.1001602     Document Type: Article

References (47)

1. Buchanan-Wollaston V, Passiatore JE, Cannon F, (1987) The mob and oriT mobilization functions of a bacterial plasmid promote its transfer to plants. Nature 328: 172-175.
2. Frost LS, Leplae R, Summers AO, Toussaint A, (2005) Mobile genetic elements: the agents of open source evolution. Nature reviews Microbiology 3: 722-732.
3. Heinemann JA, Sprague GF Jr, (1989) Bacterial conjugative plasmids mobilize DNA transfer between bacteria and yeast. Nature 340: 205-209.
4. Thomas CM, Nielsen KM, (2005) Mechanisms of, and barriers to, horizontal gene transfer between bacteria. Nature Reviews Microbiology 3: 711-721.
5. Alvarez-Martinez CE, Christie PJ, (2009) Biological diversity of prokaryotic type IV secretion systems. Microbiol Mol Biol Rev 73: 775-808.
6. de la Cruz F, Frost LS, Meyer RJ, Zechner EL, (2010) Conjugative DNA metabolism in Gram-negative bacteria. FEMS Microbiol Rev 34: 18-40.
7. Wollman EL, Jacob F, Hayes W, (1956) Conjugation and genetic recombination in Escherichia coli K-12. Cold Spring Harb Symp Quant Biol 21: 141-162.
8. Parsons LM, Jankowski CS, Derbyshire KM, (1998) Conjugal transfer of chromosomal DNA in Mycobacterium smegmatis. Mol Microbiol 28: 571-582.
9. Firth N, Ippen-Ihler K, Skurray RA (1996) Structure and function of the F factor and mechanism of conjugation. In; Escherichia coli and Salmonella Cellular and Molecular Biology, 2nd ed., Neidhardt FC, Curtiss III R, Ingraham JL, Lin ECC, Low KB, et al., editors. Washington, DC: ASM Press.
10. Lloyd RG, Low KB (1996) Homologous Recombination. In: Escherichia coli and Salmonella Cellular and Molecular Biology, 2nd ed., Neidhardt FC, Curtiss III R, Ingraham JL, Lin ECC, Low KB, et al., editors. Washington, D.C.: ASM Press.
11. Wang J, Karnati PK, Takacs CM, Kowalski JC, Derbyshire KM, (2005) Chromosomal DNA transfer in Mycobacterium smegmatis is mechanistically different from classical Hfr chromosomal DNA transfer. Mol Microbiol 58: 280-288.
12. Wollman EL, Jacob F, (1955) [Mechanism of the transfer of genetic material during recombination in Escherichia coli K12]. Comptes rendus hebdomadaires des seances de l'Academie des sciences 240: 2449-2451.
13. Wollman EL, Jacob F, Hayes W, (1956) Conjugation and genetic recombination in Escherichia coli K-12. Cold Spring Harbor symposia on quantitative biology 21: 141-162.
14. Coros A, Callahan B, Battaglioli E, Derbyshire KM, (2008) The specialized secretory apparatus ESX-1 is essential for DNA transfer in Mycobacterium smegmatis. Mol Microbiol 69: 794-808.
15. Flint JL, Kowalski JC, Karnati PK, Derbyshire KM, (2004) The RD1 virulence locus of Mycobacterium tuberculosis regulates DNA transfer in Mycobacterium smegmatis. Proc Natl Acad Sci U S A 101: 12598-12603.
16. Smith GR, (1991) Conjugational recombination in E. coli: myths and mechanisms. Cell 64: 19-27.
17. Wang J, Parsons LM, Derbyshire KM, (2003) Unconventional conjugal DNA transfer in mycobacteria. Nat Genet 34: 80-84.
18. Mizuguchi Y, Suga K, Tokunaga T, (1976) Multiple mating types of Mycobacterium smegmatis. Japanese Journal of Microbiology 20: 435-443.
19. de la Cruz F, Frost LS, Meyer RJ, Zechner EL, (2010) Conjugative DNA metabolism in Gram-negative bacteria. FEMS Microbiology Reviews 34: 18-40.
20. Abdallah AM, Gey van Pittius NC, Champion PA, Cox J, Luirink J, et al. (2007) Type VII secretion-mycobacteria show the way. Nature Reviews Microbiology 5: 883-891.
21. DiGiuseppe Champion PA, Cox JS, (2007) Protein secretion systems in Mycobacteria. Cellular Microbiology 9: 1376-1384.
22. Guinn KM, Hickey MJ, Mathur SK, Zakel KL, Grotzke JE, et al. (2004) Individual RD1-region genes are required for export of ESAT-6/CFP-10 and for virulence of Mycobacterium tuberculosis. Molecular Microbiology 51: 359-370.
23. Hsu T, Hingley-Wilson SM, Chen B, Chen M, Dai AZ, et al. (2003) The primary mechanism of attenuation of bacillus Calmette-Guerin is a loss of secreted lytic function required for invasion of lung interstitial tissue. Proceedings of the National Academy of Sciences of the United States of America 100: 12420-12425.
24. Lewis KN, Liao R, Guinn KM, Hickey MJ, Smith S, et al. (2003) Deletion of RD1 from Mycobacterium tuberculosis mimics bacille Calmette-Guerin attenuation. The Journal of Infectious Diseases 187: 117-123.
25. Llosa M, Gomis-Ruth FX, Coll M, de la Cruz Fd F, (2002) Bacterial conjugation: a two-step mechanism for DNA transport. Molecular Microbiology 45: 1-8.
26. Gupta R, Barkan D, Redelman-Sidi G, Shuman S, Glickman MS, (2011) Mycobacteria exploit three genetically distinct DNA double-strand break repair pathways. Mol Microbiol 79: 316-330.
27. Warner DF, Mizrahi V, (2011) Making ends meet in mycobacteria. Mol Microbiol 79: 283-287.
28. Narra HP, Ochman H, (2006) Of what use is sex to bacteria? Current Biology: CB 16: R705-R710.
29. Croucher NJ, Harris SR, Barquist L, Parkhill J, Bentley SD, (2012) A high-resolution view of genome-wide pneumococcal transformation. PLoS Pathog 8: e1002745 doi:10.1371/journal.ppat.1002745.
30. Golubchik T, Brueggemann AB, Street T, Gertz RE, Spencer CCA, et al. (2012) Pneumococcal genome sequencing tracks a vaccine escape variant formed through a multi-fragment recombination event. Nature Genetics 44: 352-355.
31. Kulick S, Moccia C, Didelot X, Falush D, Kraft C, et al. (2008) Mosaic DNA imports with interspersions of recipient sequence after natural transformation of Helicobacter pylori. PLoS One 3: e3797 doi:10.1371/journal.pone.0003797.
32. Mell JC, Shumilina S, Hall IM, Redfield RJ, (2011) Transformation of natural genetic variation into Haemophilus influenzae genomes. PLoS Pathog 7: e1002151 doi:10.1371/journal.ppat.1002151.
33. Sreevatsan S, Pan X, Stockbauer KE, Connell ND, Kreiswirth BN, et al. (1997) Restricted structural gene polymorphism in the Mycobacterium tuberculosis complex indicates evolutionarily recent global dissemination. Proceedings of the National Academy of Sciences of the United States of America 94: 9869-9874.
34. Gutierrez MC, Brisse S, Brosch R, Fabre M, Omais B, et al. (2005) Ancient origin and gene mosaicism of the progenitor of Mycobacterium tuberculosis. PLoS Pathog 1: e5 doi:10.1371/journal.ppat.0010005.
35. Supply P, Marceau M, Mangenot S, Roche D, Rouanet C, et al. (2013) Genomic analysis of smooth tubercle bacilli provides insights into ancestry and pathoadaptation of Mycobacterium tuberculosis. Nat Genet 45: 172-179.
36. Gordon SV, Bottai D, Simeone R, Stinear TP, Brosch R, (2009) Pathogenicity in the tubercle bacillus: molecular and evolutionary determinants. BioEssays: News and Reviews in Molecular, Cellular and Developmental Biology 31: 378-388.
37. Smith NH, Hewinson RG, Kremer K, Brosch R, Gordon SV, (2009) Myths and misconceptions: the origin and evolution of Mycobacterium tuberculosis. Nature Reviews Microbiology 7: 537-544.
38. Sassetti CM, Boyd DH, Rubin EJ, (2001) Comprehensive identification of conditionally essential genes in mycobacteria. Proceedings of the National Academy of Sciences of the United States of America 98: 12712-12717.
39. Zhang YJ, Ioerger TR, Huttenhower C, Long JE, Sassetti CM, et al. (2012) Global assessment of genomic regions required for growth in Mycobacterium tuberculosis. PLoS Pathog 8: e1002946 doi: 10.1371/journal.ppat.1002946.
40. Nguyen KT, Piastro K, Gray TA, Derbyshire KM, (2010) Mycobacterial biofilms facilitate horizontal DNA transfer between strains of Mycobacterium smegmatis. J Bacteriol 192: 5134-5142.
41. Snapper SB, Melton RE, Mustafa S, Kieser T, Jacobs WR Jr, (1990) Isolation and characterization of efficient plasmid transformation mutants of Mycobacterium smegmatis. Molecular Microbiology 4: 1911-1919.
42. Pavelka MS Jr, Jacobs WR Jr, (1996) Biosynthesis of diaminopimelate, the precursor of lysine and a component of peptidoglycan, is an essential function of Mycobacterium smegmatis. Journal of Bacteriology 178: 6496-6507.
43. Robinson JT, Thorvaldsdottir H, Winckler W, Guttman M, Lander ES, et al. (2011) Integrative genomics viewer. Nature Biotechnology 29: 24-26.
44. Krzywinski M, Schein J, Birol I, Connors J, Gascoyne R, et al. (2009) Circos: an information aesthetic for comparative genomics. Genome Research 19: 1639-1645.
45. Darling AE, Mau B, Blattner FR, Perna NT, (2004) GRIL: genome rearrangement and inversion locator. Bioinformatics 20: 122-124.
46. Darling AE, Mau B, Perna NT, (2010) progressiveMauve: multiple genome alignment with gene gain, loss and rearrangement. PLoS One 5: e11147 doi:10.1371/journal.pone.0011147.
47. Wirth SE, Krywy JA, Aldridge BB, Fortune SM, Fernandez-Suarez M, et al. (2012) Polar assembly and scaffolding proteins of the virulence-associated ESX-1 secretory apparatus in mycobacteria. Mol Microbiol 83: 654-664.