Within-host competition selects for plasmidencoded toxin-antitoxin systems

Proceedings of the Royal Society B: Biological Sciences

Volumn 277, Issue 1697, 2010, Pages 3149-3155

  Cooper, Tim F ^a   Paixão, Tiago ^a   Heinemann, Jack A ^b,c  

^a University of Houston   (United States)

^b UNIVERSITY OF CANTERBURY   (New Zealand)

^c Genk Centre for Biosafety   (Norway)

Author keywords

Plasmid; Toxin antitoxin system; Within host competition

Indexed keywords

BACTERIUM; BIOACCUMULATION; BIOMONITORING; CELL ORGANELLE; CHROMOSOME; COMPETITION (ECOLOGY); GROWTH RATE; INHIBITION; NUMERICAL MODEL; PLASMID; SENSITIVITY ANALYSIS; TOXIN;

BACTERIA (MICROORGANISMS);

EID: 77956905629     PISSN: 09628452     EISSN: 14712970     Source Type: Journal    
DOI: 10.1098/rspb.2010.0831     Document Type: Conference Paper

References (34)

1. Alexeyev, M. F. & Shokolenko, I. N. 1995 Mini-Tn10 trans-poson derivatives for insertion mutagenesis and gene delivery into the chromosome of Gram-negative bacteria. Gene 160, 59-62. (doi:10.1016/0378-1119(95)00141-R)
2. Bergstrom, C. T., Lipsitch, M. & Levin, B. 2000 Natural selection, infectious transfer and the existence conditions for bacterial plasmids. Genetics 155, 1505-1519.
3. Brendler, T., Reaves, L. & Austin, S. 2004 Interplay between plasmid partition and postsegregational killing systems. J. Bacteriol. 186, 2504-2507. (doi:10.1128/JB.186.8. 2504-2507.2004)
4. Bull, J. J. & Molineaux, I. J. 1992 Molecular genetics of adaptation in an experimental model of cooperation. Evolution. 46, 882-895. (doi:10.2307/2409743)
5. Cooper, T. F. & Heinemann, J. A. 2000 Post-segregational killing does not increase plasmid stability but acts to mediate the exclusion of competing plasmids. Proc. Natl Acad. Sci. USA 97, 12 643-12 648. (doi:10.1073/pnas. 220077897)
6. Cooper, T. F. & Heinemann, J. A. 2005 Selection for plasmid post-segregational killing depends on multiple infection: evidence for the selection of more virulent parasites through parasite-level competition. Proc. R. Soc. B 272, 403-410. (doi:10.1098/rspb.2004.2921) (Pubitemid 41411103)
7. De Bast, M. S., Mine, N. & Van Melderen, L. 2008 Chromosomal toxin-antitoxin systems may act as antiaddiction modules. J. Bacteriol. 190, 4603-4609.
8. Eberhard, W. G. 1989 Why do bacterial plasmids carry some genes and not others? Plasmid 21, 164-174.
9. Engelberg-Kulka, H., Reches, M., Nrasimahn, S., Schoulaker-Schwarz, R., Klemes, Y., Aizenman, E. & Glaser, G. 1998 rexB of bacteriophage lambda is an anti-cell death gene. Proc. Natl Acad. Sci. USA 95, 15 481-15 486. (doi:10.1073/pnas.95.26.15481) (Pubitemid 29018724)
10. Frost, L. S., Leplae, R., Summers, A. O. & Toussaint, A. 2005 Mobile genetic elements: the agents of open source evolution. Nat. Rev. Microbiol. 3, 722-732. (doi:10.1038/nrmicro1235) (Pubitemid 41195088)
11. Gerdes, K., Rasmussen, P. B. & Molin, S. 1986 Unique type of plasmid maintenance function: postsegregational killing of plasmid-free cells. Proc. Natl Acad. Sci. USA 83, 3116-3120. (doi:10.1073/pnas.83.10.3116)
12. Gerdes, K., Christensen, S. K. & Lobner-Olesen, A. 2005 Prokaryotic toxin-antitoxin stress response loci. Nat. Rev. Genet. 3, 371-382. (doi:10.1038/nrmicro1147) (Pubitemid 40590380)
13. Guglielmini, J., Szpirer, C. & Milinkovitch, M. C. 2008 Automated discovery and phylogenetic analysis of new toxin-antitoxin systems. BMC Microbiol. 8, 104. (doi:10.1186/1471-2180-8-104) (Pubitemid 351952124)
14. Handa, N., Nakayama, Y., Sadykov, M. & Kobayashi, I. 2001 Experimental genome evolution: large-scale genome rearrangements associated with resistance to replacement of a chromosomal restriction-modification gene complex. Mol. Microbiol. 40, 932-940. (doi:10. 1046/j.1365-2958.2001.02436.x)
15. Hayes, F. 2003 Toxins-antitoxins: plasmid maintenance, programmed cell death, and cell cycle arrest. Science 301, 1496-1499. (doi:10.1126/science. 1088157) (Pubitemid 37128533)
16. Heinemann, J. A. 1998 Looking sideways at the evolution of replicons. In horizontal gene transfer (eds C. Kado & M. Syvanen), pp. 11-24. London, UK: Thomson Publishing.
17. Heinemann, J. A., Scott, H. E. & Williams, M. 1996 Doing the conjugative two-step: evidence of recipient autonomy in retrotransfer. Genetics 143, 1425-1435.
18. Jensen, R. B., Grohmann, E., Schwab, H., Diaz-Orejas, R. & Gerdes, K. 1995 Comparison of ccd of F, parDE of RP4, and parD of R1 using a novel conditional replication control system of plasmid R1. Mol. Microbiol. 17, 211-220. (doi:10.1111/j.1365-2958.1995.mmi-17020211.x)
19. Kleckner, N., Bender, J. & Gottesman, S. 1991 Uses of transposons with emphasis on Tn10. Methods Enzymol. 204, 139-180. (doi:10.1016/0076-6879(91) 04009-D)
20. Kusano, K., Naito, T., Handa, N. & Kobayashi, I. 1995 Restriction-modification systems as genomic parasites in competition for specific sequences. Proc. Natl Acad. Sci. USA 92, 11 095-11 099. (doi:10.1073/pnas.92.24. 11095)
21. Magnuson, R. D. 2007 Hypothetical functions of toxin-antitoxin systems. J. Bacteriol. 189, 6089-6092. (doi:10. 1128/JB.00958-07)
22. Mochizuki, A., Yahara, K., Kobayashi, I. & Iwasa, Y. 2006 Genetic addiction: selfish gene's strategy for symbiosis in the genome. Genetics 172, 1309-1323. (doi:10.1534/ genetics.105.042895)
23. Molineux, I. J. & Spence, J. L. 1984 Virus-plasmid interactions: mutants of bacteriophage T3 that abortively infect plasmid F-containing (F\+) strains of Escherichia coli. Proc. Natl Acad. Sci. USA 81, 1465-1469. (doi:10. 1073/pnas.81.5.1465)
24. Mongold, J. A. 1998 Theoretical implications for the evolution of postsegregational killing by bacterial plasmids. Am. Nat. 139, 677-689. (doi:10.1086/285352)
25. Naito, T., Kusano, K. & Kobayashi, I. 1995 Selfish behavior of restriction-modification systems. Science 267, 897-899. (doi:10.1126/science. 7846533)
26. Nakamura, Y., Itoh, T., Matsuda, H. & Gojobori, T. 2004 Biased biological function and lateral gene transfer in pro-karyotic genomes. Nat. Genet. 36, 760-766. (doi:10. 1038/ng1381)
27. Nordstrom, K. & Austin, S. J. 1989 Mechanisms that contribute to the stable segregation of plasmids. Annu. Rev. Genet. 23, 37-69. (doi:10.1146/annurev.ge.23.120189.000345)
28. Pandey, D. P. & Gerdes, K. 2005 Toxin-antitoxin quality control loci are highly abundant in free-living but lost from host-associated prokaryotes. Nucleic Acids Res. 33, 966-976. (doi:10.1093/nar/gki201) (Pubitemid 41430517)
29. Pecota, D. C. & Wood, T. K. 1996 Exclusion of T4 phage by the hok/sok killer locus from plasmid R1. J. Bacteriol. 178, 2044-2050.
30. Sadykov, M., Asami, Y., Niki, H., Handa, N., Itaya, M., Tanokura, M. & Kobayashi, I. 2003 Multiplication of a restriction-modification complex. Mol. Microbiol. 48, 417-427. (doi:10.1046/j.1365-2958.2003.03464.x) (Pubitemid 36819078)
31. Simonsen, L., Gordon, D. M., Stewart, F. M. & Levin, B. R. 1990 Estimating the rate of plasmid transfer: an end point method. J. Gen. Microbiol. 136, 2319-2325.
32. Takahashi, N., Naito, Y., Handa, N. & Kobayashi, I. 2002 A DNA methyltransferase can protect the genome from postdisturbance attack by a restriction-modification complex. J. Bacteriol. 184, 6100-6108. (doi:10.1128/JB.184. 22.6100-6108.2002)
33. Travisano, M., Vasi, F. & Lenski, R. E. 1995 Long-term experimental evolution in Escherichia coli. III. Variation among replicate populations in correlated responses to novel environments. Evolution 49, 189-200. (doi:10. 2307/2410304)
34. Turner, P. E. & Chao, L. 1998 Sex and the evolution of intrahost competition in RNA virus f6. Genetics 150, 523-532.