Abstract
ABSTRACTPlasmids play an important role in bacterial evolution by transferring niche-adaptive functional genes between lineages, thus driving genomic diversification. Bacterial genomes commonly contain multiple, coexisting plasmid replicons, which could fuel adaptation by increasing the range of gene functions available to selection and allowing their recombination. However, plasmid coexistence is difficult to explain because the acquisition of plasmids typically incurs high fitness costs for the host cell. Here, we show that plasmid coexistence was stably maintained without positive selection for plasmid-borne gene functions and was associated with compensatory evolution to reduce fitness costs. In contrast, with positive selection, plasmid coexistence was unstable despite compensatory evolution. Positive selection discriminated between differential fitness benefits of functionally redundant plasmid replicons, retaining only the more beneficial plasmid. These data suggest that while the efficiency of negative selection against plasmid fitness costs declines over time due to compensatory evolution, positive selection to maximize plasmid-derived fitness benefits remains efficient. Our findings help to explain the forces structuring bacterial genomes: coexistence of multiple plasmids in a genome is likely to require either rare positive selection in nature or nonredundancy of accessory gene functions among the coexisting plasmids.
Highlights
IMPORTANCE Bacterial genomes often contain multiple coexisting plasmids that provide important functions like antibiotic resistance
Whereas Hgr remained at high frequency in the two-plasmid treatment, Hgr declined in the single-plasmid treatments and significantly so in the pQBR103-only treatment [Dunnett’s T3 test for pairwise comparisons of plasmid treatments without Hg(II) selection: for pQBR103 versus both, P = 0.0044; for pQBR57 versus both, P = 0.4038; for pQBR103 versus pQBR57 only, P = 0.3157)
In the single-plasmid treatments, whereas plasmid-encoded Hgr predominated in populations propagated without positive selection, we observed the invasion of plasmid-free cells carrying a chromosomal Tn5042 in some replicates with positive selection (Fig. 1; Fig. S1) (2/6 replicates of the pQBR57-only treatment; 1/6 replicates of the pQBR103-only treatment)
Summary
IMPORTANCE Bacterial genomes often contain multiple coexisting plasmids that provide important functions like antibiotic resistance. SBW25(pQBR57) outcompetes SBW25(pQBR103) in the absence of mercury, this competitive hierarchy is reversed in mercury-containing environments [25] This suggests that while pQBR57 imposes a lower fitness cost, it provides a lesser fitness benefit in the presence of mercury, relative to pQBR103 in singly infected SBW25 cells. Both plasmids are maintained individually in bacterial populations, and while this appears in each case to be linked to compensatory evolution [19, 27], unlike pQBR103, pQBR57 is capable of a high rate of conjugative transfer, which contributes to its survival and spread, in the absence of mercury [28, 29]. Chromosomal compensatory mutations that occur either in gacA-gacS, encoding a two-component global regulatory system, or in PFLU4242, encoding a hypothetical protein with two domains of unknown function, reduce the cost of these and other pQBR plasmids individually [18, 19]
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