Abstract
Evolutionary innovations that enable organisms to colonize new ecological niches are rare compared to gradual evolutionary changes in existing traits. We discovered that key mutations in the gltA gene, which encodes citrate synthase (CS), occurred both before and after Escherichia coli gained the ability to grow aerobically on citrate (Cit(+) phenotype) during the Lenski long-term evolution experiment. The first gltA mutation, which increases CS activity by disrupting NADH-inhibition of this enzyme, is beneficial for growth on the acetate and contributed to preserving the rudimentary Cit(+) trait from extinction when it first evolved. However, after Cit(+) was refined by further mutations, this potentiating gltA mutation became deleterious to fitness. A second wave of beneficial gltA mutations then evolved that reduced CS activity to below the ancestral level. Thus, dynamic reorganization of central metabolism made colonizing this new nutrient niche contingent on both co-opting and overcoming a history of prior adaptation.
Highlights
Evolutionary descent with modification has produced organisms with complex metabolic and gene regulatory networks
We have established that mutations in the gltA gene encoding citrate synthase (CS) were critical for both potentiating the evolution of aerobic citrate utilization in the Lenski long-term evolution experiment (LTEE) and for the subsequent refinement of this new metabolic capability
A key insight from our studies was the importance of fitness components in the LTEE related to utilizing both glucose, the sole carbon source added to the growth medium, and acetate, a transient overflow byproduct of E. coli growth on glucose (Figure 8)
Summary
Evolutionary descent with modification has produced organisms with complex metabolic and gene regulatory networks. When a microbial population encounters a new environment, mutants encoding more effective variants of these networks that improve nutrient utilization or reveal latent metabolic capabilities may evolve (Ryall et al, 2012). While there are many degrees of freedom that evolution can potentially access in altering cellular networks, only those mutational pathways that do not include deleterious intermediate steps are likely to be realized in most populations (Bridgham et al, 2006, 2009; Weinreich et al, 2006). Laboratory studies have characterized mutational pathways that enable microorganisms to access new enzyme activities when there is strong selection for a new trait (Hall, 2003; Nasvall et al, 2012). Combinations of metabolic and regulatory mutations that enable microorganisms to evolve toward optimal growth rates under defined conditions have
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