Abstract
ABSTRACTEvolution by natural selection under complex and dynamic environmental conditions occurs through intricate and often counterintuitive trajectories affecting many genes and metabolic solutions. To study short- and long-term evolution of bacteria in vivo, we used the natural model system of cystic fibrosis (CF) infection. In this work, we investigated how and through which trajectories evolution of Pseudomonas aeruginosa occurs when migrating from the environment to the airways of CF patients, and specifically, we determined reduction of growth rate and metabolic specialization as signatures of adaptive evolution. We show that central metabolic pathways of three distinct Pseudomonas aeruginosa lineages coevolving within the same environment become restructured at the cost of versatility during long-term colonization. Cell physiology changes from naive to adapted phenotypes resulted in (i) alteration of growth potential that particularly converged to a slow-growth phenotype, (ii) alteration of nutritional requirements due to auxotrophy, (iii) tailored preference for carbon source assimilation from CF sputum, (iv) reduced arginine and pyruvate fermentation processes, and (v) increased oxygen requirements. Interestingly, although convergence was evidenced at the phenotypic level of metabolic specialization, comparative genomics disclosed diverse mutational patterns underlying the different evolutionary trajectories. Therefore, distinct combinations of genetic and regulatory changes converge to common metabolic adaptive trajectories leading to within-host metabolic specialization. This study gives new insight into bacterial metabolic evolution during long-term colonization of a new environmental niche.
Highlights
Evolution by natural selection under complex and dynamic environmental conditions occurs through intricate and often counterintuitive trajectories affecting many genes and metabolic solutions
Since we found very few mutations that could explain the observed changes (Fig. 4E and 5A), the metabolic specialization of the adapted DK01 and late DK53 isolates might depend on the tailored activity of the carbon catabolite repression (CCR) system, which during evolution narrows the preference and hierarchy of assimilation to the nutritional resource present in the cystic fibrosis (CF) sputum, or on regulatory network changes that modify the expression and activity of metabolic pathways and enzymes
We present a high-resolution metabolic footprinting of clinical isolates of the opportunistic pathogen P. aeruginosa over 8 years of adaptive evolution in a complex dynamic niche, which we correlated with the genome sequences and mutational patterns from a prior genomic study [19]
Summary
Evolution by natural selection under complex and dynamic environmental conditions occurs through intricate and often counterintuitive trajectories affecting many genes and metabolic solutions. We investigated how and through which trajectories evolution of Pseudomonas aeruginosa occurs when migrating from the environment to the airways of CF patients, and we determined reduction of growth rate and metabolic specialization as signatures of adaptive evolution. Bacterial survival and replication during colonization of a new environment depend on sensing and responding to available nutrients and on activation of specific metabolic pathways which maximize growth efficiency [1]. It has been hypothesized that long-term adaptation drives alterations of the metabolic repertoire to maximize growth at the cost of versatility In many microorganisms such as Escherichia coli and Mycobacterium tuberculosis, reduced growth rates have previously been described to confer selective advantages under adverse environmental conditions and to facilitate tolerance to stresses such as the immune system and antibiotics [18]
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