Downloaded from www.microbiologyresearch.org by IP: 54.70.40.11 On: Thu, 04 Apr 2019 00:07:40 Microbiology (1999), 145, 3321–3329 Printed in Great Britain REVIEW ARTICLE Retrotransfer or gene capture : a feature of conjugative plasmids, with ecological and evolutionary significance Cedric Szpirer, 1 Eva Top, 2 Martine Couturier 1 and Max Mergeay 1,3,4 Author for correspondence : Max Mergeay. Tel : 32 14 333440. Fax: 32 14 320313. e-mail : mmergeaysckcen.be 1 Laboratoire de Ge  ne  tique des Prokaryotes, Universite  Libre de Bruxelles, IBMM, B-6041-Gosselies, Belgium 2 Laboratory for Microbial Ecology and Technology, University of Gent, B-9000 Gent, Belgium 3 Environmental Technology, Flemish Institute for Technological Research, VITO, B-2400 Mol, Belgium 4 Laboratory of Microbiology, Radioactive Waste & Clean-up Division, Center of Studies for Nuclear Energy, SCK/CEN, B-2400 Mol, Belgium Keywords : Retrotransfer, horizontal gene transfer, chromosomal gene capture, broad- host-range plasmids, bacterial evolution Overview and general definition The traditional view on bacterial conjugative gene exchange is a gene flow from the plasmid-containing donor strain into the plasmid-free recipient strain. When mobilization of non-conjugative plasmids is described, it is either a biparental mating with a donor containing both conjugative and a non-conjugative but mobilizable (Mob + ) plasmids, and a plasmid-free recipient, or a triparental mating with a donor, containing the Mob + plasmid, a helper strain harbouring a conjugative helper plasmid, and again a plasmid-free recipient strain. In these scenarios, mobilization was always considered as a gene flow from the original donor to the recipient strain. However, the first report of gene flow at high frequencies in two directions was published by Mergeay et al. in 1987. By means of an IncP conjugative plasmid, chromo- somal genes were not only mobilized from the original donor of the IncP plasmid towards the plasmid-free recipient, but also from the original recipient back into the donor. The terms ‘ retrotransfer ’, ‘ shuttle transfer ’, plasmid-mediated ‘ gene capture ’ or even a kind of bacterial ‘ hermaphroditism ’, were used to describe a conjugational biparental event that led to the inheritance (capture) by the original host of a con- jugative plasmid, of genetic traits (either chromosomal markers or plasmids) from the mating partner, free of conjugative plasmids. The frequency of this retro- transfer can be very high, being in some cases of the same order of magnitude as the frequencies observed for the transfer of genetic traits promoted in the canonical donor–recipient direction (Mergeay et al., 1987). Although the phenomenon was first observed and analysed in most detail for broad-host-range (BHR) IncP1 plasmids (Mergeay et al., 1987), it was also reported for other plasmids such as some IncN (pULG14) and IncM plasmids (R69.2) (Thiry et al., 1984 ; Mergeay et al., 1985), the IncF plasmid pDE-FL54 and the IncW plasmid pSa322 (Heinemann & Ankenbauer, 1993a), and for the catabolic IncP9 plasmid pWW0 (Ramos- Gonzalez et al., 1994). This capture of new genetic traits could thus be of great significance for the evolution of microbial communities, especially where stress is selec- ting rare events, yielding individual populations with new combinations of genes, which may allow better survival or more rapid growth. Capture of chromosomal markers The capture of chromosomal markers was first observed during conjugation mediated by derivatives of IncP plasmids carrying a transposable element (Mergeay et al., 1984, 1987) such as R68.45 and RP4::Mu3A (also called pULB113 ; Van Gijsegem & Toussaint, 1982). The matings involved a donor with multiple markers spread over the chromosome and a recipient carrying one marker. In homologous matings between two Erwinia chrysanthemi partners (Schoonejans & Toussaint, 1983) or two Pseudomonas fluorescens 6.2 partners (Lejeune et al., 1983 ; Mergeay et al., 1984), transconjugants were selected for having inherited one marker from each mating partner (Fig. 1). Surprisingly, the transcon- jugants that carried all the unselected markers of the donor of the conjugative plasmid were often more frequent than those with only one or a few of the unselected donor markers. In other words, a class of recombinants that seemed to have received the whole donor chromosome, and hence expected to be the least 0002-3533  1999 SGM 3321