Natural Selection, Infectious Transfer and the Existence Conditions for Bacterial Plasmids

Corresponding author: Carl T. Bergstrom, Department of Biology, Emory University, 1510 Clifton Rd., Atlanta, GA 30322., cbergst{at}emory.edu (E-mail)

Communicating editor: A. G. CLARK

Despite the near-ubiquity of plasmids in bacterial populations and the profound contribution of infectious gene transfer to the adaptation and evolution of bacteria, the mechanisms responsible for the maintenance of plasmids in bacterial populations are poorly understood. In this article, we address the question of how plasmids manage to persist over evolutionary time. Empirical studies suggest that plasmids are not infectiously transmitted at a rate high enough to be maintained as genetic parasites. In PART I, we present a general mathematical proof that if this is the case, then plasmids will not be able to persist indefinitely solely by carrying genes that are beneficial or sometimes beneficial to their host bacteria. Instead, such genes should, in the long run, be incorporated into the bacterial chromosome. If the mobility of host-adaptive genes imposes a cost, that mobility will eventually be lost. In PART II, we illustrate a pair of mechanisms by which plasmids can be maintained indefinitely even when their rates of transmission are too low for them to be genetic parasites. First, plasmids may persist because they can transfer locally adapted genes to newly arriving strains bearing evolutionary innovations, and thereby preserve the local adaptations in the face of background selective sweeps. Second, plasmids may persist because of their ability to shuttle intermittently favored genes back and forth between various (noncompeting) bacterial strains, ecotypes, or even species.

This article has been cited by other articles:

				F. R. Slater, K. D. Bruce, R. J. Ellis, A. K. Lilley, and S. L. Turner Heterogeneous Selection in a Spatially Structured Environment Affects Fitness Tradeoffs of Plasmid Carriage in Pseudomonads Appl. Envir. Microbiol., May 15, 2008; 74(10): 3189 - 3197. [Abstract] [Full Text] [PDF]

				L. De Gelder, J. J. Williams, J. M. Ponciano, M. Sota, and E. M. Top Adaptive Plasmid Evolution Results in Host-Range Expansion of a Broad-Host-Range Plasmid Genetics, April 1, 2008; 178(4): 2179 - 2190. [Abstract] [Full Text] [PDF]

				L. N. Lili, N. F. Britton, and E. J. Feil The Persistence of Parasitic Plasmids Genetics, September 1, 2007; 177(1): 399 - 405. [Abstract] [Full Text] [PDF]

				S. M. Krone, R. Lu, R. Fox, H. Suzuki, and E. M. Top Modelling the spatial dynamics of plasmid transfer and persistence Microbiology, August 1, 2007; 153(8): 2803 - 2816. [Abstract] [Full Text] [PDF]

				J. M. Ponciano, L. De Gelder, E. M. Top, and P. Joyce The Population Biology of Bacterial Plasmids: A Hidden Markov Model Approach Genetics, June 1, 2007; 176(2): 957 - 968. [Abstract] [Full Text] [PDF]

				M. Sota, M. Tsuda, H. Yano, H. Suzuki, L. J. Forney, and E. M. Top Region-Specific Insertion of Transposons in Combination with Selection for High Plasmid Transferability and Stability Accounts for the Structural Similarity of IncP-1 Plasmids J. Bacteriol., April 15, 2007; 189(8): 3091 - 3098. [Abstract] [Full Text] [PDF]

				M. I. Bahl, L. H. Hansen, T. R. Licht, and S. J. Sorensen Conjugative Transfer Facilitates Stable Maintenance of IncP-1 Plasmid pKJK5 in Escherichia coli Cells Colonizing the Gastrointestinal Tract of the Germfree Rat Appl. Envir. Microbiol., January 1, 2007; 73(1): 341 - 343. [Abstract] [Full Text] [PDF]

				A. Srivastava, H. Casey, N. Johnson, O. Levy, and R. Malley Recombinant Bactericidal/Permeability-Increasing Protein rBPI21 Protects against Pneumococcal Disease Infect. Immun., January 1, 2007; 75(1): 342 - 349. [Abstract] [Full Text] [PDF]

				K. Kamachi, M. Sota, Y. Tamai, N. Nagata, T. Konda, T. Inoue, E. M. Top, and Y. Arakawa Plasmid pBP136 from Bordetella pertussis represents an ancestral form of IncP-1beta plasmids without accessory mobile elements Microbiology, December 1, 2006; 152(12): 3477 - 3484. [Abstract] [Full Text] [PDF]

				J. A. Draghi and P. E. Turner DNA secretion and gene-level selection in bacteria. Microbiology, September 1, 2006; 152(Pt 9): 2683 - 2688. [Abstract] [Full Text] [PDF]

				G. F. Webb, E. M. C. D'Agata, P. Magal, and S. Ruan A model of antibiotic-resistant bacterial epidemics in hospitals PNAS, September 13, 2005; 102(37): 13343 - 13348. [Abstract] [Full Text] [PDF]

				Y. Zhao, Z. Ma, and G. W. Sundin Comparative Genomic Analysis of the pPT23A Plasmid Family of Pseudomonas syringae J. Bacteriol., March 15, 2005; 187(6): 2113 - 2126. [Abstract] [Full Text] [PDF]

				M. M. Tanaka, N. A. Rosenberg, and P. M. Small The Control of Copy Number of IS6110 in Mycobacterium tuberculosis Mol. Biol. Evol., December 1, 2004; 21(12): 2195 - 2201. [Abstract] [Full Text] [PDF]

				H. Heuer, R. Szczepanowski, S. Schneiker, A. Puhler, E. M. Top, and A. Schluter The complete sequences of plasmids pB2 and pB3 provide evidence for a recent ancestor of the IncP-1{beta} group without any accessory genes Microbiology, November 1, 2004; 150(11): 3591 - 3599. [Abstract] [Full Text] [PDF]

				L. De Gelder, J. M. Ponciano, Z. Abdo, P. Joyce, L. J. Forney, and E. M. Top Combining Mathematical Models and Statistical Methods to Understand and Predict the Dynamics of Antibiotic-Sensitive Mutants in a Population of Resistant Bacteria During Experimental Evolution Genetics, November 1, 2004; 168(3): 1131 - 1144. [Abstract] [Full Text] [PDF]

				P. E. Turner Phenotypic Plasticity in Bacterial Plasmids Genetics, May 1, 2004; 167(1): 9 - 20. [Abstract] [Full Text] [PDF]

				L. Molbak, A. Tett, D. W. Ussery, K. Wall, S. Turner, M. Bailey, and D. Field The Plasmid Genome Database Microbiology, November 1, 2003; 149(11): 3043 - 3045. [Full Text] [PDF]

				C. G. Kurland, B. Canback, and O. G. Berg Horizontal gene transfer: A critical view PNAS, August 19, 2003; 100(17): 9658 - 9662. [Abstract] [Full Text] [PDF]

				M. M. Tanaka, C. T. Bergstrom, and B. R. Levin The Evolution of Mutator Genes in Bacterial Populations: The Roles of Environmental Change and Timing Genetics, July 1, 2003; 164(3): 843 - 854. [Abstract] [Full Text] [PDF]

				F. Dionisio, I. Matic, M. Radman, O. R. Rodrigues, and F. Taddei Plasmids Spread Very Fast in Heterogeneous Bacterial Communities Genetics, December 1, 2002; 162(4): 1525 - 1532. [Abstract] [Full Text] [PDF]

				O. G. Berg and C. G. Kurland Evolution of Microbial Genomes: Sequence Acquisition and Loss Mol. Biol. Evol., December 1, 2002; 19(12): 2265 - 2276. [Abstract] [Full Text] [PDF]

				J. Paulsson Multileveled Selection on Plasmid Replication Genetics, August 1, 2002; 161(4): 1373 - 1384. [Abstract] [Full Text] [PDF]

				J. Pannucci, R. T. Okinaka, R. Sabin, and C. R. Kuske Bacillus anthracis pXO1 Plasmid Sequence Conservation among Closely Related Bacterial Species J. Bacteriol., January 1, 2002; 184(1): 134 - 141. [Abstract] [Full Text] [PDF]