Accessory DNAs in the bacterial gene pool: playground for coevolution.

Chemostat studies of bacteria that harbour the prokaryotic transposable elements Tn5 and Tn10 and the temperate phages lambda, Mu, P1 and P2 have shown that these accessory DNA elements confer a selective advantage on their hosts. We propose that similar selective effects provided the initial impetus for the evolution of nascent accessory DNA elements in primitive bacterial populations. In subsequent evolution the elements acquired or perfected the 'selfish' characteristics of over-replication and horizontal transmission. Such selfish traits led to the dissemination of accessory DNAs among commensal strains, species and genera, genetically interconnecting them to create a 'commonwealth' of species that potentially share a common gene pool. The involvement of accessory DNAs in genetic exchange provides selection at the population level for refinement and diversification of the elements and for regulation of their replication, transposition and transfer among cells. The diversity of intracellular environments encountered by the elements imposes constraints on their evolution while at the same time altering the selection pressures operating on conventional chromosomal genes. This process of coevolution of accessory DNAs with the genomes of their diverse hosts has led to a unique population structure and mechanism of genetic exchange among bacteria, which constitutes the most effective adaptive strategy yet devised by selection.

[1]  Y. Doi.  Studies on the Oxidizing Power of Roots of Crop Plants : 1.The Difference with Species of Crop Plants and Wild Grasses , 1952 .

[2]  Jody W. Deming,et al.  Growth of ‘black smoker’ bacteria at temperatures of at least 250 °C , 1983, Nature.

[3]  D. Reanney,et al.  Extrachromosomal Genetic Elements and the Adaptive Evolution of Bacteria , 1980 .

[4]  J. Hatchett,et al.  Genetics of the Ability of the Hessian Fly, Mayetiola destructor, to Survive on Wheats Having Different Genes for Resistance , 1970 .

[5]  H. Mooney,et al.  Endomycorrhizal Role for Interspecific Transfer of Phosphorus in a Community of Annual Plants , 1982, Science.

[6]  D. Ellwood,et al.  Survival of R-factor carrying Escherichia coli in mixed cultures in the chemostat , 1977 .

[7]  M. Havas,et al.  The Smoking Hills: natural acidification of an aquatic ecosystem , 1983, Nature.

[8]  J. L. Young,et al.  Soil Lime Level (pH) and VA‐Mycorrhiza Effects on Growth Responses of Sweetgum Seedlings , 1983 .

[9]  W. Doolittle,et al.  Selfish genes, the phenotype paradigm and genome evolution , 1980, Nature.

[10]  D. Dykhuizen,et al.  The influences of a lambda prophage on the growth rate of Escherichia coli. , 1978, Microbios.

[11]  A. Campbell.  Evolutionary significance of accessory DNA elements in bacteria. , 1981, Annual review of microbiology.

[12]  A. Campbell.  Some general questions about movable elements and their implications. , 1981, Cold Spring Harbor symposia on quantitative biology.

[13]  M. Syvanen,et al.  Regulation of Tn5 by the right-repeat proteins: Control at the level of the transposition reaction? , 1982, Cell.

[14]  L. Lin,et al.  Increased reproductive fitness of Escherichia coli lambda lysogens , 1977, Journal of virology.

[15]  J. Rochaix,et al.  Transposition of R factor genes to bacteriophage lambda. , 1975, Proceedings of the National Academy of Sciences of the United States of America.

[16]  R. Kudrna,et al.  λ Lysogens of E. coli reproduce more rapidly than non-lysogens , 1975, Nature.

[17]  F. Crick,et al.  Selfish DNA: the ultimate parasite , 1980, Nature.

[18]  S. Silver,et al.  Microbial transformations of metals. , 1978, Annual review of microbiology.

[19]  W. Reznikoff,et al.  Control of Tn5 transposition in Escherichia coli is mediated by protein from the right repeat , 1982, Cell.

[20]  J. Welch,et al.  Tandem gene amplification mediates copper resistance in yeast. , 1982, Proceedings of the National Academy of Sciences of the United States of America.

[21]  D. Hartl,et al.  Evolution of transposons: natural selection for Tn5 in Escherichia coli K12. , 1983, Genetics.

[22]  G. Lebek,et al.  Generation time-prolonging R plasmids: correlation between increases in the generation time of Escherichia coli caused by R plasmids and their molecular size. , 1980, Plasmid.

[23]  N. Datta,et al.  Conjugative plasmids in bacteria of the ‘pre-antibiotic’ era , 1983, Nature.

[24]  L. Lin,et al.  Reproductive fitness of P1, P2, and Mu lysogens of Escherichia coli , 1977, Journal of virology.

[25]  B. Hirschel,et al.  Inverted repeats of Tn5 are transposable elements. , 1982, Proceedings of the National Academy of Sciences of the United States of America.

[26]  L. Chao,et al.  COMPETITION BETWEEN HIGH AND LOW MUTATING STRAINS OF ESCHERICHIA COLI , 1983, Evolution; international journal of organic evolution.

[27]  E. Novitski,et al.  Meiotic Drive as an Evolutionary Force , 1957, The American Naturalist.

[28]  C. J. Marchant,et al.  Evolution in Spartina (Gramineae): II. Chromosomes, basic relationships and the problem of S. ×townsendii agg. , 1968 .