Genomic analysis of fast expanding bacteria reveals new molecular adaptive mechanisms

Bacterial populations have been shown to accumulate deleterious mutations during spatial expansions that overall decrease their fitness and ability to grow. However, it is unclear if and how they can respond to selection in face of this mutation load. We examine here if artificial selection can counteract the negative effects of range expansions. We investigated the molecular evolution of 20 lines (SEL) selected for fast expansions and compared them to 20 lines without artificial selection (CONTROL). We find that all 20 SEL lines have been able to increase their expansion speed relative to the ancestral line, unlike CONTROL lines, showing that enough beneficial mutations are produced during spatial expansions to counteract the negative effect of expansion load. Importantly, SEL and CONTROL lines have similar numbers of mutations indicating that they evolved for the same number of generations and that increased fitness is not due to a purging of deleterious mutations. We find that loss of function (LOF) mutations are better at explaining the increased expansion speed of SEL lines than non-synonymous mutations or a combination of the two. Interestingly, most LOF mutations are found in simple sequence repeats located in genes involved in gene regulation and gene expression. We postulate that such potentially reversible mutations could play a major role in the rapid adaptation of bacteria to changing environmental conditions by shutting down expensive genes and adjusting gene expression.Author SummaryWe investigated if strong artificial selection for fast expansion can counteract the negative effects of range expansion which had been shown to lead to an accumulation of deleterious mutations. This experiments showed that i) an increase in expansion speed could occur if bacteria were selected from the largest protruding sectors, and ii) that artificially selected bacterial lines accumulated about the same number of mutations than simply expanding line suggesting that the observed increased fitness is not due to increased purifying selection where deleterious mutations would have been removed in fast growing lines. We find that loss of function (LOF) mutations are best explaining the observed increased expansion speed in selected lines. These mutations, which are known to play an important role in adaptive processes in bacterial populations, frequently consist in small insertion-deletions in simple sequence repeats, and are thus relatively easily reversible. They could thus act as switches that can reversibly shut down genes. Our results therefore suggest that shutting down expensive genes and adjusting gene expression are important for adaptive processes during range expansion.