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Prokaryotic Sex: Eukaryote-Like Qualities of Recombination in An Dispatch R601 Prokaryotic Sex: Eukaryote-like match, the ends may be cut to a random extent by exonucleases, Qualities of Recombination in an and then the newly revealed ends are tested, and so on. This would increase Archaean Lineage the probability that eventually a reduced donor segment would sufficiently match a sequence from the Genetic exchange within one Archaean lineage is a bit like sex in recipient. We suggest this process eukaryotes — cells fuse and huge segments of DNA are recombined — with would be particularly successful in consequences for the spread of adaptations across species. organisms that recombine through cell fusion, as the donor segments start out Frederick M. Cohan* (which may be harmful to the recipient) exceptionally long. This hypothesis and Stephanie Aracena [3]. We therefore hypothesize that predicts that more-closely-related in Haloferax and other cell-fusion organisms may recombine after Two decades ago, Moshe Mevarech systems, niche-transcending a smaller number of cuts; so and colleagues discovered an adaptations may not transfer as easily more-distant crosses would yield extraordinary mode of recombination as in the Bacteria. On the other hand, shorter recombinant segments, in an Archaean taxon — cells of the huge size of recombined a pattern observed in Bacillus Haloferax can recombine through cell segments may foster the transfer transformation [3]. fusion [1]. After two cells fuse, their of extremely complex adaptations The authors suggest that horizontal genomes can recombine, and then the that could not otherwise be transferred genetic transfer would be particularly fused cell can resolve into two cells, [4], including possibly the ancient easy between species where cell fusion each with a single chromosome. The transfer of aerobic metabolism occurs. While recombination between authors noted that fusion-based from Bacteria into Archaean already-fused cells seems almost recombination holds some methanogens [5]. unhindered by the sequence resemblance to mating in the Naor et al. also challenged our divergence between Haloferax eukaryotes. understanding of barriers to genetic species, it is possible that resistance to As reported in this issue of Current exchange between divergent species, cell fusion may increase with greater Biology, Mevarech and colleagues [2] finding surprisingly little sexual phylogenetic distances. It will be from Tel Aviv University and the isolation between two Haloferax interesting to find out the phylogenetic University of Connecticut have recently species (Figure 1). The 14% sequence distance over which cells can readily investigated the population genetics divergence between these species fuse, and also how widespread cell of fusion-based recombination in would have predicted a 1,000-fold fusion is over the Archaea. So far we Haloferax, and have challenged views reduction in recombination rate in know that Haloferax failed to on the evolutionary effects of genetic Bacteria [6], but recombination in this recombine with two related genera exchange in prokaryotes. Naor et al. [2] system was reduced by only a factor through cell fusion [10] and that first challenged the widely accepted of about 40. fusion-based recombination can occur view that recombination in prokaryotes Why is Haloferax recombination in the distantly related Archaean involves transfer of short DNA so much less sensitive to sequence Sulfolobus [11]. segments. In principle, cell fusion could divergence? The authors noted that the Finally, the authors challenge the enable recombination of enormous borders of recombination frequently conclusion from bacterial studies that segments of DNA, possibly up to the coincided at one end with chromosome recombination is rare in prokaryotic 50:50 mix of genes seen in eukaryotic locations of very high inter-species systems. Their experiments in sex. Naor et al. found that w17% of the identity, including rRNA and tRNA laboratory culture yielded genome is transferred in Haloferax genes. This is consistent with Bacterial recombination rates around 1024, fusion; at 475 kilobases, these recombination, which requires a nearly which are high compared to other segments are much larger than perfect match between donor and prokaryotic systems [12]. However, it is generally seen in bacterial recipient sequences at one [7] or both important to keep in mind that the rate recombination [3]. [8] ends of the donor segment, while of recombination in nature is not easily The huge size of recombined the sequence divergence between simulated in the laboratory. This is segments in Haloferax could negatively ends is of no consequence [9]. Thus, because recombination rates depend and positively impact the course of interspecies recombination in on the rate at which cells encounter one adaptive evolution. Haloferax loses Haloferax was augmented by another (limited by densities and one advantage seen in Bacteria for segments ending at the nearly identical sharing of microhabitats), as well as the transferring short segments across tRNA and rRNA genes. likelihood of cells being in populations. In Bacteria, transfers The enormous sizes of transferred a physiological state conducive to of short segments allow a recipient segments in Haloferax may explain why recombination, parameters that are to acquire a niche-transcending recombination junctions so frequently generally unknown in nature. adaptation (which is beneficial in occurred at regions of unusually high In contrast, sequence analyses of different niches and genetic identity. We hypothesize an iterative organisms sampled from nature can backgrounds, e.g., resistance to an process whereby the original two yield a ‘retrospective’ recombination antibiotic) without also acquiring donor-segment ends are tested against rate, averaged over time and habitats, niche-specifying genes from the donor the recipient genome; if they fail to while avoiding the biases of Current Biology Vol 22 No 15 R602 AB References Intraspecies Interspecies 1. Rosenshine, I., Tchelet, R., and Mevarech, M. (1989). The mechanism of DNA transfer in the mating system of an archaebacterium. Science 245, 1387–1389. 2. Naor, A., Lapierre, P., Mevarech, M., Papke, R.T., and Gophna, U. (2012). Low species barriers in halophilic Archaea and the formation of recombinant hybrids. Curr. Biol. 22, 1444–1448. Fusion: 0.02% Fusion: 0.004% 3. Zawadzki, P., and Cohan, F.M. (1995). The size and continuity of DNA segments integrated in Bacillus transformation. Genetics 141, 1231–1243. 4. Cohan, F.M. (2010). Synthetic biology: now that we’re creators, what should we create? Curr. Biol. 20, R675–R677. 5. Kennedy, S.P., Ng, W.V., Salzberg, S.L., Hood, L., and DasSarma, S. (2001). Understanding the Recombination: 62% Recombination: 8% adaptation of Halobacterium species NRC-1 to its extreme environment through computational analysis of its genome sequence. Genome Res. 11, 1641–1650. 6. Fraser, C., Hanage, W.P., and Spratt, B.G. (2007). Recombination and the nature of bacterial speciation. Science 315, 476–480. 7. Shen, P., and Huang, H.V. (1986). Homologous recombination in Escherichia coli: dependence Current Biology on substrate length and homology. Genetics 112, 441–457. 8. Majewski, J., and Cohan, F.M. (1999). DNA sequence similarity requirements for Figure 1. Cell fusion and recombination in Haloferax. interspecific recombination in Bacillus. Genetic exchange can occur in Haloferax through cell fusion followed by recombination, within Genetics 153, 1525–1533. (A) and between (B) species. Both cell fusion and recombination are reduced between species 9. Majewski, J. (2001). Sexual isolation in bacteria. (by 5-fold and 8-fold, respectively), yielding an overall 40-fold reduction in genetic exchange. FEMS Microbiol. Lett. 199, 161–169. 10. Tchelet, R., and Mevarech, M. (1994). This is much less sexual isolation than would be expected for bacterial species that are equally Interspecies genetic transfer in halophilic divergent (expected 1000-fold reduction). These results suggest that genetic transfer may be Archaebacteria. System. Appl. Microbiol. 16, easier among archaean than among bacterial species. However, it is not yet known over what 578–581. phylogenetic distances archaean cells can easily fuse. 11. Schleper, C., Holz, I., Janekovic, D., Murphy, J., and Zillig, W. (1995). A multicopy plasmid of the extremely thermophilic archaeon Sulfolobus effects its transfer to recipients by mating. J. Bacteriol. 177, 4417–4426. experimental studies. Naor et al. [2] sequence at one gene locus spread 12. Vos, M., and Didelot, X. (2009). A comparison of noted that while a retrospective across an entire phylotype, while homologous recombination rates in bacteria and archaea. Isme J. 3, 199–208. phylogenetic analysis in the closely elsewhere on the chromosome the 13. Papke, R.T., Zhaxybayeva, O., Feil, E.J., related Halorubrum did not indicate phylotype was much more diverse. Sommerfeld, K., Muise, D., and Doolittle, W.F. (2007). Searching for species in haloarchaea. exceptionally high recombination rates They suggest this implies frequent Proc. Natl. Acad. Sci. USA 104, 14092–14097. in nature [12,13], frequent recombination, as have others 14. Maynard Smith, J., Smith, N., O’Rourke, M., and recombination was indicated by observing similar patterns [16–18]. Spratt, B.G. (1993). How clonal are bacteria? Proc. Natl. Acad. Sci. USA 90, 4384–4388. near-zero levels of linkage However, periodic selection can purge 15. Cohan, F.M. (1994). The effects of rare but disequilibrium (i.e., little association
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