Plasmid persistence: costs, benefits, and the plasmid paradox

Abstract

22Plasmids are extrachromosomal DNA elements that can be found throughout bacteria, as well as 23 in other domains of life. Nonetheless, the evolutionary processes underlying the persistence of 24 plasmids are incompletely understood. Bacterial plasmids may encode genes for traits which are 25 sometimes beneficial to their hosts, such as antimicrobial resistance, virulence, heavy metal 26 tolerance, and the catabolism of unique nutrient sources. In the absence of selection for these 27 traits, however, plasmids generally impose a fitness cost on their hosts. As such, plasmid 28 persistence presents a conundrum: models predict that costly plasmids will be lost over time, or 29 that beneficial plasmid genes will be integrated into the host genome. However, laboratory and Benefits of Plasmid Carriage 55The range of possible explanations for continued plasmid persistence has two extremes. 56At one end, plasmids exist entirely as selfish entities, only concerned in their continued survival 57 (Bergstrom et al. 2000;Slater et al. 2008). At the other, plasmids can confer some unconditional 58 benefit on their bacterial hosts. For the most part, neither extreme is likely to hold true -many transferred on their own (Bergstrom et al. 2000). Thus, we expect that most plasmids must be 63 beneficial to their hosts -at least some of the time -to be maintained in populations. 64Plasmid-encoded benefits are typically related to survival in novel environments and 65 conditions, with many plasmids encoding genes for antibiotic resistance, virulence, tolerance to 66 heavy metals, or for the metabolism of unique carbon sources, as well as nitrogen fixation, plant 67 gall formation, and root nodulation (Masterson et al. 1982; Eberhard 1989;Nies 1999; Beceiro et 68 al. 2013;Ramirez et al. 2014; Pal et al. 2015). Not only can plasmid-encoded genes provide a 69 potential benefit to their host, they may influence both the environment and neighbouring cells, 70for example through production of helpful enzymes or nutrients, or through production of 71 harmful chemicals . Plasmids can thus be a source of genes that help the host 72 adapt to novel environments (Eberhard 1989). 73Resistance to antibiotics is one of the better studied benefits conferred by plasmids, and 74 one that is increasingly relevant in clinical settings. Plasmids carry resistance genes to most 75 major classes of antibiotics, with genes for protection against aminoglycosides, beta-lactams, and 76 tetracyclines most commonly found (Bennett 2008; Pal et al. 2015 Deleterious Effects of Plasmid Carriage 91While under particular conditions many plasmid-borne traits confer a benefit to their 92 hosts, the wider fitness effects of plasmids are not always clear. For example, a plasmid may be 93 beneficial when its bacterial host is exposed to a novel stressor, but detrimental once the stressor 94 is removed (Vogwill and MacLean 2015). Under these conditions, it is expected that bacterial 95 strains lacking the costly plasmid outcompete the plasmid-bearing strai...

A large self-transmissible plasmid from Nigeria confers resistance to multiple antibacterials without a carrying cost

“…However, research has shown that, once evolved, multidrug resistance plasmids can be maintained in the absence of selection (67). There is a dearth of fitness defects reported for resistance plasmids in the literature and the reasons why some of them are evolutionarily successful are not well understood (58,68). This study demonstrates that the aac(6')-Ib-cr gene of strain M63c is carried on a large multidrug resistance plasmid pMB2, which also bears a number of genetic loci that support its evolutionary success irrespective of antibiotic selection.…”

Duplication and diversification of a unique chromosomal virulence island hosting the subtilase cytotoxin in Escherichia coli ST58

“…Whilst these genes encoding these factors are not novel, the appearance of large aggregations of these virulence genes suggests high acquisition rates within this chromosome. The potential fitness costs associated with carrying these large islands may have resulted in the lack of plasmid content [61], although this is strictly conjecture.…”

Experimental Evolution of the Megaplasmid pMPPla107 in Pseudomonas stutzeri Enables Identification of Genes Contributing to Sensitivity to an Inhibitory Agent

“…In previous evolutionary studies focusing on plasmids, the burden of plasmid acquisition resulted in compensatory mutations present on host chromosomes (15,16,26,27). To identify where the resistance mutations occurred, we analyzed the genomes of six laboratory passage strains of P. stutzeri after 500 generations under conditions that selected for maintenance of megaplasmid pMPPla107.…”