From Trading Genes to Crafting New Tricks: How Horizontal Gene Transfer Potentiates the Emergence of Novel Functions

Horizontal gene transfer (HGT), the set of processes by which genetic information is transferred between individuals, has shaped life’s evolution. It is particularly frequent in microbial organisms, where it has driven numerous remarkable adaptations to extreme conditions, anti-microbial agents, or biotic interactions. Its role in spreading novel functions is now documented by countless examples of dramatic phenotypic changes. It is however less clear how frequently HGT favours functional innovations, i.e. the emergence of novel biochemical, physiological or ecological functions. Here, I will argue that very high rates of gene acquisition by HGT favour functional innovation by providing a constant flow of genes encoding a large diversity of processes. Part of this genetic information is under little, if any, purifying selection, paving the way for evolutionary tinkering that may ultimately result in their co-option for novel functions. Such processes have been described for the evolution of regulatory networks, metabolic pathways, antibiotic resistance, and co-option of complex machineries. Mobile genetic elements provide a lot of the material for functional co-options and then spread them across microbial communities. They have the key role of preventing that functional innovations remain private to the lineages where they emerge. Consequently, when microbial communities encounter new challenges or opportunities, they function as a collective of agents that innovate to address them.