Bacteria gone native vs. bacteria gone awry?: plasmidic transfer and bacterial evolution.

Despite the importance, abundance, and diversity of bacteria, we are just beginning to understand their evolutionary biology. Sex, understood as genetic exchange, is one of the keystone issues in bacterial evolution. Most bacteria reproduce by binary fission, and genetic exchange is independent of reproduction (1). If there is little or no genetic exchange among clones, each strain evolves as an independent lineage, and standard population genetics concepts, such as allelic frequencies and changes of these frequencies in populations, are not applicable (2). On the other hand, if recombination is common among related bacterial lineages (i.e., within bacterial species), we may analyze bacterial populations like most other organisms using standard population genetics methods (2). Recently, Maynard-Smith et al. (3), using detailed analyses based on multilocus linkage disequilibrium, have shown that there is a wide range of bacterial sexualities, ranging from lineages with little or no recombination (like Salmonella) to others that are almost panmictic (like Neisseria gonorrhoeae), and some with intermediate (and more complicated) sexualities: localized recombination among closely related strains (Rhizobium meliloti) or apparently very clonal populations, due to few very successful strains, have a structure called ‘‘epidemic’’ (e.g., Neisseria meningitidis) (3). These analyses are mainly based on multilocus enzyme electrophoresis data from chromosomal genes. But bacteria have a fascinating complication; they usually present accessory genes, in the form of smaller chromosomes, known as plasmids (4, 5). Plasmids usually encode specific functions, such as conjugation, antibiotic resistance, sugar utilization, colicin activity, and nitrogen fixation (5–8). Some plasmids are small and cryptic (i.e, without any known function, if any), whereas others are large and more complex (5, 9). Plasmidic genes are not only dynamic, due to rearrangements and duplications within and among them (9, 10), they are also capable of moving among strains, among related bacterial species, or even among different genera (9, 11–15). This process is called ‘‘horizontal’’ or ‘‘lateral’’ transfer of plasmids (14). The mobility of plasmidic genes is relevant for the evolutionary ecology of bacteria, since they may confer instantaneous adaptation in changing environments, or they may be costly to the bacteria carrying them (16). If plasmids are only inherited in a ‘‘vertical’’ fashion (from ancestor to their descendants by binary fission), then there should be a close linkage between chromosome and plasmid, and they would evolve together as one evolutionary unit. But if plasmids are very mobile, they would have evolutionary and populational dynamics of their own, and they may behave in a selfish way, similar to pathogens. In this case, they would be found in different chromosomal backgrounds, and their numbers would depend on the advantages they confer to the host, their cost, and their rate of transmission (17). In this issue of the Proceedings, Wernegreen et al. (5) give us some insight on the dynamics and patterns of plasmid evolution by analyzing Rhizobium associated to four sympatric species of wild clover (Trifolium) growing together in two natural populations from nondisturbed meadows of the Sierra Nevada, in California. To interpret their results from a qualitative perspective, followingMaynard-Smith et al. (3) ideas on the genetic structure of bacteria, we propose the following plasmidychromosome evolutionary patterns (Fig. 1) (considering that the true phylogenies of both chromosome and plasmid are know):