Dynamics of Adaptation During Three Years of Evolution Under Long-Term Stationary Phase

Many bacterial species that cannot sporulate, such as the model bacterium Escherichia coil, can nevertheless survive for years, following exhaustion of external resources, in a state termed long-term stationary phase (LISP). Here we describe the dynamics of E. coil adaptation during the first three years spent under LISP. We show that during this time, E. coil continuously adapts genetically through the accumulation of mutations. For nonmutator clones, the majority of mutations accumulated appear to be adaptive under LISP, reflected in an extremely convergent pattern of mutation accumulation. Despite the rapid and convergent manner in which populations adapt under LISP, they continue to harbor extensive genetic variation. The dynamics of evolution of mutation rates under LISP are particularly interesting. The emergence of mutators affects overall mutation accumulation rates as well as the mutational spectra and the ultimate spectrum of adaptive alleles acquired under LISP. With time, mutators can evolve even higher mutation rates through the acquisition of additional mutation rate-enhancing mutations. Different mutator and nonmutator clones within a single population and time point can display extreme variation in their mutation rates, resulting in differences in both the dynamics of adaptation and their associated deleterious burdens. Despite these differences, clones that vary greatly in their mutation rates tend to coexist within their populations for many years, under LISP.