Abstract:It is difficult to understand plasmid maintenance in the absence of selection and theoretical models predict the conditions for plasmid persistence to be limited. Plasmid-associated fitness costs decrease bacterial competitivity, while imperfect partition allows the emergence of plasmid-free cells during cell division. Although plasmid conjugative transfer allows mobility into plasmid-free cells, the rate of such events is generally not high enough to ensure plasmid persistence. Experimental data suggest sever… Show more
“…One explanation for abundant plasmid coexistence in bacterial genomes is that the fitness costs of acquiring multiple plasmids could be less than additive. Positive epistasis between plasmid costs could permit the accumulation of multiple plasmids by reducing the cost for plasmid bearers of acquiring additional plasmids (4,16,17); however, positive epistatic interactions among plasmid costs are not universal (4). Moreover, as we show in this study, the methods by which positive epistasis has been previously estimated (i.e., competition of plasmid carriers against plasmid-free cells) (4) may not measure the actual cost of plasmid coinfection.…”
Plasmids 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.
IMPORTANCE Bacterial genomes often contain multiple coexisting plasmids that provide important functions like antibiotic resistance. Using lab experiments, we show that such plasmid coexistence within a genome is stable only in environments where the function they encode is useless but is unstable if the function is useful and beneficial for bacterial fitness. Where competing plasmids perform the same useful function, only the most beneficial plasmid is kept by the cell, a process that is similar to competitive exclusion in ecological communities. This process helps explain how bacterial genomes are structured: bacterial genomes expand in size by acquiring multiple plasmids when selection is relaxed but subsequently contract during periods of strong selection for the useful plasmid-encoded function.
“…One explanation for abundant plasmid coexistence in bacterial genomes is that the fitness costs of acquiring multiple plasmids could be less than additive. Positive epistasis between plasmid costs could permit the accumulation of multiple plasmids by reducing the cost for plasmid bearers of acquiring additional plasmids (4,16,17); however, positive epistatic interactions among plasmid costs are not universal (4). Moreover, as we show in this study, the methods by which positive epistasis has been previously estimated (i.e., competition of plasmid carriers against plasmid-free cells) (4) may not measure the actual cost of plasmid coinfection.…”
Plasmids 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.
IMPORTANCE Bacterial genomes often contain multiple coexisting plasmids that provide important functions like antibiotic resistance. Using lab experiments, we show that such plasmid coexistence within a genome is stable only in environments where the function they encode is useless but is unstable if the function is useful and beneficial for bacterial fitness. Where competing plasmids perform the same useful function, only the most beneficial plasmid is kept by the cell, a process that is similar to competitive exclusion in ecological communities. This process helps explain how bacterial genomes are structured: bacterial genomes expand in size by acquiring multiple plasmids when selection is relaxed but subsequently contract during periods of strong selection for the useful plasmid-encoded function.
“…One explanation for abundant plasmid coinfection is that the fitness costs of acquiring multiple plasmids could be less than additive. Positive epistasis between plasmid costs could permit the accumulation of multiple plasmids by reducing the cost for plasmid-bearers of acquiring additional plasmids [4,15,16], however, positive epistatic interactions among plasmid costs are not universal [4]. Moreover, as we will show in this study, the methods by which positive epistasis has been previously estimated (i.e., competition of plasmid-carriers against plasmid-free cells [4]) may not measure the actual cost of plasmid coinfection.…”
Plasmids 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 (i.e., plasmid coinfection), which could fuel adaptation by increasing the range of gene functions available to selection and allowing their recombination. However, plasmid coinfection is difficult to explain because the acquisition of plasmids typically incurs high fitness costs for the host cell. Here, we show that plasmid coinfection was stably maintained without positive selection for plasmid-encoded gene functions and was associated with compensatory evolution to reduce fitness costs. By contrast, with positive selection, plasmid coinfection 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 maximise 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 non-redundancy of accessory gene functions among coinfecting plasmids.
“…Plasmids, for example, typically engender a fitness cost in the host bacterium (749,931) however, these costs can be ameliorated (positive epistasis) or accentuated (negative epistasis) by the presence of additional MGEs (752,932). Epistatic interactions between MGEs can determine the fate of the MGE in bacterial populations, promoting low-fitness-cost associations and long-term maintenance, thus shaping the highways of AMR genes (752,933,934). Plasmid evolutionary success and the plasmid-mediated spread of AMR are to a significant degree the result of a intracellular plasmid competition with other plasmids, influencing the spread by lateral transfer, in particular, the stable plasmid inheritance (incompatibility) (935).…”
Section: Barriers Determined By the Interactions Between Mobile Genetic Elementsmentioning
Evolution is the hallmark of life. Descriptions of the evolution of microorganisms have provided a wealth of information, but knowledge regarding “what happened” has precluded a deeper understanding of “how” evolution has proceeded, as in the case of antimicrobial resistance.
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