Comparative Biology of Two Natural Variants of the IncQ-2 Family Plasmids, pRAS3.1 and pRAS3.2

Loftie-Eaton, Wesley; Rawlings, Douglas E.

doi:10.1128/jb.00864-09

Cited by 13 publications

(15 citation statements)

References 40 publications

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“…These results are in agreement with a predicted theoretical loss frequency (based on random segregation) of 1 in 1.6 ϫ 10 4 generations for a plasmid with a copy number of 15 plasmids per chromosome, and even less for plasmids with a higher copy number (25). The high level of TA system-independent stability may be a result of the relatively high PCN of pRAS3 plasmids relative to other IncQ family plasmids which have been reported to have a PCN varying from 10 to 16 (17). The reason for the high PCN of the pRAS3 plasmids is not known.…”

Section: Discussionsupporting

confidence: 67%

“…If the additional 6-bp repeat altered the mobilization frequency, this could affect the horizontal spread of one of the variants and thereby provide a selective advantage. However, when mobilized by the RP4 conjugative system, the mobilization frequency of plasmids with either four or five 6-bp repeats and identical iteron numbers was found to be similar (17). Therefore, a change in mobilization frequency is unlikely to have provided selective pressure for acquisition of an altered number of 6-bp repeats.…”

Section: Discussionmentioning

confidence: 97%

“…The reciprocal experiment with pRAS3.1.35 and pRAS3.1Km gave largely similar results with the 4-iteron plasmid (pRAS3.1Km) displacing the 3-iteron plasmid (pRAS3.1.35) in 87% Ϯ 10% of host cells and with 12% Ϯ 8% of the host cells retaining both plasmids. The displacement of a 3-iteron plasmid by a 4-iteron plasmid occurred in spite of the observation that when the iteron number of pRAS3.1 was increased from 3 to 4, its PCN decreased from ϳ59 to ϳ41 (17). The displacement of a plasmid containing three 22-bp iterons with a higher PCN by a plasmid with an identical structure but with a lower PCN was unexpected.…”

Section: Construction Of Plasmids With Increased Numbers Of Iteronsmentioning

confidence: 87%

“…As shown in this study, this plasmid with four 22-bp iterons would be expected to displace the intermediate plasmid with three 22-bp iterons, even though it had a higher PCN. Should an increase in the number of iterons have occurred first with a corresponding reduction in PCN (such a plasmid, pRAS3.1.44, was constructed, and the PCN was found to be ϳ23) (17), the plasmid with a lower PCN and with four iterons would still have displaced the three-iteron plasmid as shown in Table 3. However, since this lower-copynumber plasmid is perfectly stable, it seems less likely for there to have been evolutionary pressure for this plasmid to have gained an additional 6-bp repeat, thereby increasing its PCN but placing an increased metabolic load on the host.…”

Section: Discussionmentioning

confidence: 99%

“…Plasmids pRAS3.1 and pRA3.2 are almost identical IncQ plasmids that were isolated from the fish pathogen Aeromonas salmonicida (pRAS3.2) or atypical A. salmonicida (pRAS3.1 and pRAS3.2) in Norway (12). The mobilization and replication genes of pRAS3 plasmids are similar in order and sequence to the mobilization and replication genes of both pTF-FC2 (7) and pTC-F14 (9), with greater sequence identity to pTF-FC2 than to pTC-F14 (17). Together these plasmids constitute the only known members of the IncQ-2 subgroup of IncQ plasmids.…”

mentioning

confidence: 98%

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Evolutionary Competitiveness of Two Natural Variants of the IncQ-Like Plasmids, pRAS3.1 and pRAS3.2

Loftie-Eaton

Rawlings

2010

J Bacteriol

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Plasmids pRAS3.1 and pRAS3.2 are natural variants of the IncQ-2 plasmid family, that except for two differences, have identical plasmid backbones. Plasmid pRAS3.1 has four 22-bp iterons in its oriV region, while pRAS3.2 has only three 6-bp repeats and pRAS3.1 has five 6-bp repeats in the promoter region of the mobB-mobA/repB genes and pRAS3.2 has only four. In previous work, we showed that the overall effect of these differences was that when the plasmid was in an Escherichia coli host, the copy numbers of pRAS3.1 and pRAS3.2 were approximately 41 and 30, respectively. As pRAS3.1 and pRAS3.2 are likely to have arisen from the same ancestor, we addressed the question of whether one of the variants had an evolutionary advantage over the other. By constructing a set of identical plasmids with the number of 22-bp iterons varying from three to seven, it was found that plasmids with four or five iterons displaced plasmids with three iterons even though they had lower copy numbers. Furthermore, the metabolic load that the plasmids placed on E. coli host cells compared with plasmid-free cells increased with copy number from 10.9% at a copy number of 59 to 2.6% at a copy number of 15. Plasmid pRAS3.1 with four 22-bp iterons was able to displace pRAS3.2 with three iterons when both were coresident in the same host. However, the lower-copy-number pRAS3.2 placed 2.8% less of a metabolic burden on an E. coli host population, and therefore, pRAS3.2 has a competitive advantage over pRAS3.1 at the population level, as pRAS3.2-containing cells would be expected to outgrow pRAS3.1-containing cells.Plasmids of the IncQ family are characterized by their relatively small size (ϳ6 to 15 kb), their ability to replicate in a very wide range of bacterial host cells, and by being readily mobilizable by certain self-transmissible plasmids, in particular the broad-host-range IncP plasmids such as RP4 or RK2 (22). IncQ family plasmids have been subdivided into the IncQ-1 and IncQ-2 groups depending on whether their mobilization genes are of the three-gene IncQ type or the five-gene IncP type. Both subgroups of IncQ family plasmids have similar replicons that consist of three genes that encode a helicase (repA), a primase (repB), a DNA-binding initiator protein (repC), and an oriV region. The oriV region typically contains three complete, identical 22-bp iterons (or 20-bp iterons with 2-bp spacers) that serve as the binding site for RepC proteins (18,22). Although some IncQ family plasmids may possess more than three copies of the iterons, the additional iterons are either partial copies, have sequence variations, or lack the spacer regions (22). It has been shown that even a single-basepair replacement in a single iteron could result in a nonfunctional iteron-containing region and the inability of the IncQ-1 plasmid RSF1010 to replicate (19). Furthermore, in IncQ plasmids, the iterons have been shown to serve as the primary incompatibility determinants with cloned iterons on their own being able to displace the plasmid from which they were ...

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Section: Discussionsupporting

confidence: 67%

Section: Discussionmentioning

confidence: 97%

Section: Construction Of Plasmids With Increased Numbers Of Iteronsmentioning

confidence: 87%

Section: Discussionmentioning

confidence: 99%

mentioning

confidence: 98%

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