Multiple Phenotypic Changes Associated with Large-Scale Horizontal Gene Transfer

Dougherty, Kevin; Smith, Brian A.; Moore, Autumn; Maitland, Shannon; Fanger, Chris; Murillo, Rachel; Baltrus, David A.

doi:10.1371/journal.pone.0102170

Cited by 32 publications

(47 citation statements)

References 61 publications

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“…Plasmids can promote bacterial survival in the presence of antibiotics, but, as we have seen, they can also impose a fitness cost when they enter a new bacterial host. The past few years have witnessed growing interest in the fitness effects of plasmids (21)(22)(23)(24)(25)(26)(27)(28)115), and some of the general principles underlying these effects are now beginning to be identified. However, we still are a long way from understanding the specific molecular basis of these costs or being able to predict plasmid fitness effects in a bacterial host.…”

Section: Challenges In the Fieldmentioning

confidence: 99%

Fitness Costs of Plasmids: a Limit to Plasmid Transmission

2017

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Plasmids mediate the horizontal transmission of genetic information between bacteria, facilitating their adaptation to multiple environmental conditions. An especially important example of the ability of plasmids to catalyze bacterial adaptation and evolution is their instrumental role in the global spread of antibiotic resistance, which constitutes a major threat to public health. Plasmids provide bacteria with new adaptive tools, but they also entail a metabolic burden that, in the absence of selection for plasmid-encoded traits, reduces the competitiveness of the plasmid-carrying clone. Although this fitness reduction can be alleviated over time through compensatory evolution, the initial cost associated with plasmid carriage is the main constraint on the vertical and horizontal replication of these genetic elements. The fitness effects of plasmids therefore have a crucial influence on their ability to associate with new bacterial hosts and consequently on the evolution of plasmid-mediated antibiotic resistance. However, the molecular mechanisms underlying plasmid fitness cost remain poorly understood. Here, we analyze the literature in the field and examine the potential fitness effects produced by plasmids throughout their life cycle in the host bacterium. We also explore the various mechanisms evolved by plasmids and bacteria to minimize the cost entailed by these mobile genetic elements. Finally, we discuss potential future research directions in the field.

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Section: Challenges In the Fieldmentioning

confidence: 99%

Fitness Costs of Plasmids: a Limit to Plasmid Transmission

2017

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“…Modes of ameliorative evolution include changes in genes whose products interact with the new adaptation (138-140) and in some cases changes in the transferred genes themselves (137). Moreover, the incompatibilities brought by a transferred adaptation can yield a cascade of evolutionary changes (141).…”

Section: The Genetic Basis Of Early Diversificationmentioning

confidence: 99%

Transmission in the Origins of Bacterial Diversity, From Ecotypes to Phyla

Cohan

2017

Microbiol Spectr

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Any two lineages, no matter how distant they are now, began their divergence as one population splitting into two lineages that could coexist indefinitely. The rate of origin of higher-level taxa is therefore the product of the rate of speciation times the probability that two new species coexist long enough to reach a particular level of divergence. Here I have explored these two parameters of disparification in bacteria. Owing to low recombination rates, sexual isolation is not a necessary milestone of bacterial speciation. Rather, irreversible and indefinite divergence begins with ecological diversification, that is, transmission of a bacterial lineage to a new ecological niche, possibly to a new microhabitat but at least to new resources. Several algorithms use sequence data from a taxon of focus to identify phylogenetic groups likely to bear the dynamic properties of species. Identifying these newly divergent lineages allows us to characterize the genetic bases of speciation, as well as the ecological dimensions upon which new species diverge. Speciation appears to be least frequent when a given lineage has few new resources it can adopt, as exemplified by photoautotrophs, C1 heterotrophs, and obligately intracellular pathogens; speciation is likely most rapid for generalist heterotrophs. The genetic basis of ecological divergence may determine whether ecological divergence is irreversible and whether lineages will diverge indefinitely into the future. Long-term coexistence is most likely when newly divergent lineages utilize at least some resources not shared with the other and when the resources themselves will coexist into the remote future.

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“…Why, then, was mucoidy favoured in the presence of plasmids? A possible explanation is that acquisition of large plasmids, such as pQBR103, can have major effects on the bacterial phenotype, beyond those of the accessory gene cargo itself, through largescale remodelling of bacterial gene regulatory networks (Dougherty et al 2014). We have previously shown that acquisition of the pQBR103 plasmid causes~17% of SBW25 chromosomal genes to be upregulated, including a large proportion of the alginate biosynthesis pathway (seven positive regulators, three negative regulators and the biosynthesis locus PFLU5986; Harrison et al 2015a).…”

Section: )mentioning

confidence: 99%

Conflicting selection alters the trajectory of molecular evolution in a tripartite bacteria–plasmid–phage interaction

et al. 2017

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Bacteria engage in a complex network of ecological interactions, which includes mobile genetic elements (MGEs) such as phages and plasmids. These elements play a key role in microbial communities as vectors of horizontal gene transfer but can also be important sources of selection for their bacterial hosts. In natural communities, bacteria are likely to encounter multiple MGEs simultaneously and conflicting selection among MGEs could alter the bacterial evolutionary response to each MGE. Here, we test the effect of interactions with multiple MGEs on bacterial molecular evolution in the tripartite interaction between the bacterium, Pseudomonas fluorescens, the lytic bacteriophage, SBW25φ2, and conjugative plasmid, pQBR103, using genome sequencing of experimentally evolved bacteria. We show that individually, both plasmids and phages impose selection leading to bacterial evolutionary responses that are distinct from bacterial populations evolving without MGEs, but that together, plasmids and phages impose conflicting selection on bacteria, constraining the evolutionary responses observed in pairwise interactions. Our findings highlight the likely difficulties of predicting evolutionary responses to multiple selective pressures from the observed evolutionary responses to each selective pressure alone. Understanding evolution in complex microbial communities comprising many species and MGEs will require that we go beyond studies of pairwise interactions.

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Multiple Phenotypic Changes Associated with Large-Scale Horizontal Gene Transfer

Cited by 32 publications

References 61 publications

Fitness Costs of Plasmids: a Limit to Plasmid Transmission

Fitness Costs of Plasmids: a Limit to Plasmid Transmission

Transmission in the Origins of Bacterial Diversity, From Ecotypes to Phyla

Conflicting selection alters the trajectory of molecular evolution in a tripartite bacteria–plasmid–phage interaction

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