Abstract
Horizontal gene transfer often leads to phenotypic changes within recipient organisms independent of any immediate evolutionary benefits. While secondary phenotypic effects of horizontal transfer (i.e., changes in growth rates) have been demonstrated and studied across a variety of systems using relatively small plasmids and phage, little is known about the magnitude or number of such costs after the transfer of larger regions. Here we describe numerous phenotypic changes that occur after a large-scale horizontal transfer event (∼1 Mb megaplasmid) within Pseudomonas stutzeri including sensitization to various stresses as well as changes in bacterial behavior. These results highlight the power of horizontal transfer to shift pleiotropic relationships and cellular networks within bacterial genomes. They also provide an important context for how secondary effects of transfer can bias evolutionary trajectories and interactions between species. Lastly, these results and system provide a foundation to investigate evolutionary consequences in real time as newly acquired regions are ameliorated and integrated into new genomic contexts.
Highlights
Horizontal Gene Transfer (HGT), the movement of genetic material between individuals without reproduction, is a major evolutionary force within microbial communities and impacts genome dynamics across all life [1,2]
In a parallel manuscript [18], we demonstrate that acquisition of this megaplasmid lowers fitness of Pseudomonas stutzeri by,20% and here we report on multiple additional phenotypes affected by large-scale HGT
For horizontally transferred regions to be maintained within a population, they must either provide a large enough benefit or be transmitted at high enough rates across individuals to avoid loss due to selection or genetic drift [26,27]. That such benefits may be the primary target of strong selective pressures within a given environment, as with antibiotic resistance, doesn’t preclude the existence of neutral secondary phenotypic changes or HGTassociated costs which are deleterious in other environments [6]
Summary
Horizontal Gene Transfer (HGT), the movement of genetic material between individuals without reproduction, is a major evolutionary force within microbial communities and impacts genome dynamics across all life [1,2]. Numerous studies have demonstrated the existence of such costs by documenting changes to fitness, growth rate, or other phenotypes after the transfer of relatively small genomic regions. Recently acquired genes are typically expressed at inefficient levels leading to limitations in resources such as ribonucleotides, amino acids, or ATP [7,8]. Acquired regions may disrupt flux through cellular systems, leading to the buildup of toxic intermediates [12,13]. While such costs have been directly observed in laboratory experiments, retrospective studies across genomes add an additional layer of complexity as there exists an inverse correlation between gene retention after HGT and number of protein-protein interactions affected [14]. In most cases the precise molecular mechanisms underlying observed costs of HGT have not been identified, both the magnitude and molecular basis for costs could be greatly affected by both the size and gene content of the acquired region
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