Abstract
Integrative and conjugative elements (ICEs) comprise ubiquitous large mobile regions in prokaryotic chromosomes that transmit vertically to daughter cells and transfer horizontally to distantly related lineages. Their evolutionary success originates in maximized combined ICE-host fitness trade-offs, but how the ICE impacts on the host metabolism and physiology is poorly understood. Here we investigate global changes in the host genetic network and physiology of Pseudomonas putida with or without an integrated ICEclc, a model ICE widely distributed in proteobacterial genomes. Genome-wide gene expression differences were analyzed by RNA-seq using exponentially growing or stationary phase-restimulated cultures on 3-chlorobenzoate, an aromatic compound metabolizable thanks to specific ICEclc-located genes. We found that the presence of ICEclc imposes a variety of changes in global pathways such as cell cycle and amino acid metabolism, which were more numerous in stationary-restimulated than exponential phase cells. Unexpectedly, ICEclc stimulates cellular motility and leads to more rapid growth on 3-chlorobenzoate than cells carrying only the integrated clc genes. ICEclc also concomitantly activates the P. putida Pspu28-prophage, but this in itself did not provoke measurable fitness effects. ICEclc thus interferes in a number of cellular pathways, inducing both direct benefits as well as indirect costs in P. putida.
Highlights
Horizontal gene transfer (HGT) is a major driving force for microbial evolution and adaptation, since transmission of genes from a donor bacterium can rapidly confer additional cellular functions and phenotypes to a naive recipient[1,2]
The presence of ICEclc improves P. putida fitness on the carbon substrate 3CBA, which is exclusively metabolizable thanks to the Integrative and conjugative elements (ICEs), but impairs fitness on other carbon substrates
A previous study using micro-array analysis showed very few differences in host gene expression and less than 1% fitness costs of ICEclc on P. aeruginosa PAO1 growing on succinate as a non-selective neutral carbon source[30]
Summary
Horizontal gene transfer (HGT) is a major driving force for microbial evolution and adaptation, since transmission of genes from a donor bacterium can rapidly confer additional cellular functions and phenotypes to a naive recipient[1,2]. Mobile DNA vectors that promote HGT include, for example, plasmids, integrative and conjugative elements (ICEs) or bacteriophages[11]. While acquisition of such auxiliary genes and their relevant phenotypes can be beneficial for hosts to adapt in particular ecological niches, it is generally assumed that the DNA acquisition imposes various types of fitness costs on the cells. Since ICEclc horizontal transmission from PAO1 as donor was very low compared to P. knackmussii (one per 105 donor cells), and since that particular study could not address the impact of the ICE during growth on 3CBA, it may not have captured all relevant ICE-induced effects
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