Academic journal article Genetics

The Maintenance of Sex in Bacteria Is Ensured by Its Potential to Reload Genes

Academic journal article Genetics

The Maintenance of Sex in Bacteria Is Ensured by Its Potential to Reload Genes

Article excerpt

ABSTRACT

Why sex is maintained in nature is a fundamental question in biology. Natural genetic transformation (NGT) is a sexual process by which bacteria actively take up exogenous DNA and use it to replace homologous chromosomal sequences. As it has been demonstrated, the role of NGT in repairing deleterious mutations under constant selection is insufficient for its survival, and the lack of other viable explanations have left no alternative except that DNA uptake provides nucleotides for food. Here we develop a novel simulation approach for the long-term dynamics of genome organization (involving the loss and acquisition of genes) in a bacterial species consisting of a large number of spatially distinct populations subject to independently fluctuating ecological conditions. Our results show that in the presence of weak interpopulation migration NGT is able to subsist as a mechanism to reload locally lost, intermittently selected genes from the collective gene pool of the species through DNA uptake from migrants. Reloading genes and combining them with those in locally adapted genomes allow individual cells to readapt faster to environmental changes. The machinery of transformation survives under a wide range of model parameters readily encompassing real-world biological conditions. These findings imply that the primary role of NGT is not to serve the cell with food, but to provide homologous sequences for restoring genes that have disappeared from or become degraded in the local population.

(ProQuest Information and Learning: ... denotes formulae omitted.)

SEXUAL reproduction is a process that brings genomes, or portions of genomes, from different individuals into a common cell, producing a new combination of genes: in eukaryotes, this occurs as a result of fertilization and meiotic recombination; in bacteria, it happens as a result of the acquisition of exogenous DNA. The ubiquity of genetic transfer in bacteria is reflected in the dynamic structure of their genomes, which are constantly being shaped by two opposing forces: selection for shorter length (favoring DNA loss through deletion) and selection for gene function (driving genome loading by the acquisition of exogenous DNA) (VELLAI et al. 1999; MIRA et al. 2001). The balance of these forces results in most bacteria having highly economized genomes with only a small fraction (~10%) of noncoding sequences (VELLAI et al. 1998; MIRA et al. 2001). DNA transfer into the bacterial cell can occur in three ways: (i) transduction by viruses, (ii) conjugation by plasmids, and (iii) natural genetic transformation (NGT) by developing competence, a regulated physiological state in which the bacterial cell is able to take up DNA fragments released by another cell (AVERY et al. 1944; SOLOMON and GROSSMAN 1996). The genetic elements responsible for transduction and conjugation primarily survive as parasites and are located on viral and plasmid DNA. The genes required for competence are, however, located on the bacterial chromosome, placing NGT under the direct control of the cell. While all three mechanisms play a role in rare gene transfer events between bacteria of different species, termed horizontal gene transfer, NGT is the most significant source of active and frequent genetic transfer within a species (for a comparative review of the three processes see THOMAS and NIELSEN 2005). In bacteria capable of NGT, alleles typically change more frequently by recombination (e.g., 5- to 10-fold in Streptococcus pneumoniae and Neisseria meningitidis) than by mutation (LEVIN and BERGSTROM 2000; FEIL et al. 2001; FEIL 2004; THOMAS and NIELSEN 2005). It is this combination of high-throughput genetic mixing among members of the same species and direct cellular control that is responsible for NGT often being referred to as the bacterial analog of meiotic sex in eukaryotes (MAYNARD SMITH et al. 1991; MAYNARD SMITH 1993).

The persistence of NGT raises the same question as the prevalence of meiotic sex (BERNSTEIN et al. …

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