Academic journal article Genetics

The Persistence of Parasitic Plasmids

Academic journal article Genetics

The Persistence of Parasitic Plasmids

Article excerpt

ABSTRACT

The conditions under which plasmids are predicted to persist remain controversial. Here, we reevaluate the ordinary differential equations used previously to model plasmid persistence and conclude that the parameter space required for maintenance is far less stringent than has been supposed. Strikingly, our model demonstrates that purely parasitic plasmids may persist, even in the absence of heterogeneity in the host population, and that this persistence is expressed by oscillations or damped oscillations between the plasmid-bearing and the plasmid-free class.

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A key concept from the genomics era is the partition of the bacterial genome into "core" and "acces-sory" elements. The former includes all those genes responsible for essential housekeeping functions of the cell and defines the "essence" of a given taxonomic unit by excluding any genes not present in all strains. The presence of accessory elements, in contrast, is highly variable between strains and although the functions of these genes tend to be less clear they are generally thought to be responsible for microadaptations at the subspecies level. Although primarily conceptual, this partition can also be physical, with core genes being confined to the bacterial chromosome while accessory genes are found on semiautonomous replicons such as plasmids or (as in the case of the Burkholderia, Rhizo-bium, or Vibrio genera) secondary chromosomes that are likely to have evolved frommegaplasmids. Given certain environmental conditions, plasmids can provide many different types of selective advantage, including antibiotic resistance, resistance to pollutants or UV, and biofilm formation (Chigo 2001; Dionisio 2005).

Plasmids thus make a major contribution to the accessory gene pool, but they are also considered to impose a fitness cost related to plasmid carriage and the time and resources required to replicate extra DNA. The precise magnitude and consistency of the fitness cost imposed by plasmids are currently a matter of debate. Dionisio et al. (2005) have recently suggested that this cost ameliorates over evolutionary time and that initially costly plasmidsmay eventually confer a selective advantage. More recently the model of Gelder et al. (2004) suggested that the fitness cost may change somewhat erratically over time due to stochastic plasmid and chromosomal mutations. Dionisio (2005) has discussed a different kind of fitness cost, where the synthesis of sex pili leaves the cell vulnerable to male-specific phages. Dionisio proposes that heterogeneity in the expression of sex pili can facilitate the maintenance of plasmid (and phage) within the bacterial population.

In addition to conferring a potential fitness cost, plas-mids may be lost stochastically during bacterial reproduction by failing to segregate into one of the daughter cells during binary fission. Ponciano et al. (2006) note that in some strains this stochastic segregation loss may be an important effect even in plasmids of low cost. A high copy number of plasmids per cell can dramatically reduce the risk of stochastic plasmid loss; for example, pBR322 has a copy number of ~21, meaning that in theory only 1 cell in 1 million would lose all plasmids by stochastic loss (Sorensen et al. 2005). However, a tradeoff exists as an increase in copy number imposes an increased cost to the cell (Paulsson 2002). Larger plas-mids tend to have a lower copy number, but these often contain genetic systems (e.g., the stable partitioning, or par, gene) that act to reduce the probability of daughter cells not receiving a plasmid. The limited evidence available from in situ studies suggests that local adaptation to a microniche will also lead to increased plasmid-host stability (Sorensen et al. 2005).

Despite these caveats, a combination of fitness cost and stochastic loss should, over time, act to remove plasmids from the bacterial population. …

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