Costs and Benefits of High Mutation Rates: Adaptive Evolution of Bacteria in the Mouse Gut

Giraud, Antoine; Matić, Ivan; Tenaillon, Olivier; Clara, Antonio; Radman, Miroslav; Fons, Michel; Taddéi, François

doi:10.1126/science.1056421

Cited by 450 publications

(471 citation statements)

References 21 publications

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“…Our work extends the possibilities offered by null mutations by generating context-dependent ecological interactions that can stabilise genetic diversity within evolving bacterial populations (Friesen et al, 2004). The larger target size available for this type of mutations combined with the fitness advantage auxotrophs gain in the presence of the required metabolite offers a plausible adaptive argument to account for the rapid evolution of metabolic auxotrophies (Giraud et al, 2001) as well as of cross-feeding interactions within bacterial communities (Harcombe, 2010;Poltak and Cooper, 2011). Our observation that synergistic growth benefits were prevalent in a broad range of different cross-feeding Figure 5 Competition of cross-feeding consortia against wild type.…”

Section: Distribution Of Obligate Cross-feeding Interactionsmentioning

confidence: 74%

Fitness and stability of obligate cross-feeding interactions that emerge upon gene loss in bacteria

et al. 2013

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Cross-feeding interactions, in which bacterial cells exchange costly metabolites to the benefit of both interacting partners, are very common in the microbial world. However, it generally remains unclear what maintains this type of interaction in the presence of non-cooperating types. We investigate this problem using synthetic cross-feeding interactions: by simply deleting two metabolic genes from the genome of Escherichia coli, we generated genotypes that require amino acids to grow and release other amino acids into the environment. Surprisingly, in a vast majority of cases, cocultures of two cross-feeding strains showed an increased Darwinian fitness (that is, rate of growth) relative to prototrophic wild type cells-even in direct competition. This unexpected growth advantage was due to a division of metabolic labour: the fitness cost of overproducing amino acids was less than the benefit of not having to produce others when they were provided by their partner. Moreover, frequency-dependent selection maintained cross-feeding consortia and limited exploitation by non-cooperating competitors. Together, our synthetic study approach reveals ecological principles that can help explain the widespread occurrence of obligate metabolic cross-feeding interactions in nature.

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Section: Distribution Of Obligate Cross-feeding Interactionsmentioning

confidence: 74%

Fitness and stability of obligate cross-feeding interactions that emerge upon gene loss in bacteria

et al. 2013

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“…During long-term adaptation or passage through selective bottlenecks, mutators can arise from a population and outgrow the wild-type strain (15-17). The advantage conferred by mutator genes is indirect because they increase fitness by introducing mutations at other loci that offer selectable growth benefits (14,15).Experiments involving the competition of bacteria with differing mutation rates have generally used only one or a few mutators, have not included antimutators, and have typically entailed pairwise competition. Although mutators often outcompete wild-type strains in serial transfer experiments, theoretical models predict that, as mutation rates increase, a threshold is crossed where hypermutability becomes more deleterious than beneficial (18,19).…”

mentioning

confidence: 99%

Optimization of DNA polymerase mutation rates during bacterial evolution

Loh

Salk

Loeb

2009

Proc. Natl. Acad. Sci. U.S.A.

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Mutation rate is an important determinant of evolvability. The optimal mutation rate for different organisms during evolution has been modeled in silico and tested in vivo, predominantly through pairwise comparisons. To characterize the fitness landscape across a broad range of mutation rates, we generated a panel of 66 DNA polymerase I mutants in Escherichia coli with comparable growth properties, yet with differing DNA replication fidelities, spanning 10 3 -fold higher and lower than that of wild type. These strains were competed for 350 generations in six replicate cultures in two different environments. A narrow range of mutation rates, 10-to 47-fold greater than that of wild type, predominated after serial passage. Mutants exhibiting higher mutation rates were not detected, nor were wild-type or antimutator strains. Winning clones exhibited shorter doubling times, greater maximum culture densities, and a growth advantages in pairwise competition relative to their precompetition ancestors, indicating the acquisition of adaptive phenotypes. To investigate the basis for mutator selection, we undertook a large series of pairwise competitions between mutator and wildtype strains under conditions where, in most cases, one strain completely overtook the culture within 18 days. Mutators were the most frequent winners but wild-type strains were also observed winning, suggesting that the competitive advantage of mutators is due to a greater probability of developing selectably advantageous mutations rather than from an initial growth advantage conferred by the polymerase variant itself. Our results indicate that under conditions where organism fitness is not yet maximized for a particular environment, competitive adaptation may be facilitated by enhanced mutagenesis.adaptation | competition | fidelity | mutator M utation rates in organisms reflect the need for accuracy to maintain critical genetic information and the requirement for flexibility to adapt to environmental changes. In eukaryotic and prokaryotic cells, spontaneous mutations occur infrequently-less than once per billion bases copied (1). A departure from this norm can be detrimental to an individual and to a population as a whole. Increased mutation rates in viruses (2, 3) and bacteria (4, 5) can lead to decreased fitness and ultimately to extinction (6). Elevated mutation frequencies are associated with human pathologies such as cancer and premature aging (7,8). Large increases in accuracy, on the other hand, can be energetically costly (9) and also lead to decreased fitness.Although low mutation rates benefit populations in stable environments, higher mutation rates favor adaptation. Evolution has derived mechanisms for transient changes in mutation rates to circumvent the narrow restriction imposed by the high fidelity required for long-term survival. Mutagenesis is induced by bacteria during times of stress (10), and the mammalian immune system relies on targeted hypermutation to respond to new pathogens (11). In experiments where populations of bacte...

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“…There is genomic evidence from bacteria residing inside eukaryotic cells (endocellular symbionts) that increased mutation rates can indeed drive faster evolution (Itoh et al, 2002). Organisms with mutator phenotypes (exhibiting elevated mutation rates) are known in nature, and though advantageous in the short term when colonizing or adapting to a new environment, they are generally maladaptive due to the accumulation of deleterious mutations (e.g., Giraud et al, 2001). The concept of adaptively variable mutation rates and the ability to evolve, or ''evolvability,'' of organisms was reviewed by Radman et al (1999) and Pigliucci (2008).…”

Section: Biological Effects Of Ionizing Radiationmentioning

confidence: 99%

Ionizing Radiation and Life

2011

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Ionizing radiation is a ubiquitous feature of the Cosmos, from exogenous cosmic rays (CR) to the intrinsic mineral radioactivity of a habitable world, and its influences on the emergence and persistence of life are wideranging and profound. Much attention has already been focused on the deleterious effects of ionizing radiation on organisms and the complex molecules of life, but ionizing radiation also performs many crucial functions in the generation of habitable planetary environments and the origins of life. This review surveys the role of CR and mineral radioactivity in star formation, generation of biogenic elements, and the synthesis of organic molecules and driving of prebiotic chemistry. Another major theme is the multiple layers of shielding of planetary surfaces from the flux of cosmic radiation and the various effects on a biosphere of violent but rare astrophysical events such as supernovae and gamma-ray bursts. The influences of CR can also be duplicitous, such as limiting the survival of surface life on Mars while potentially supporting a subsurface biosphere in the ocean of Europa. This review highlights the common thread that ionizing radiation forms between the disparate component disciplines of astrobiology.

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Costs and Benefits of High Mutation Rates: Adaptive Evolution of Bacteria in the Mouse Gut

Cited by 450 publications

References 21 publications

Fitness and stability of obligate cross-feeding interactions that emerge upon gene loss in bacteria

Fitness and stability of obligate cross-feeding interactions that emerge upon gene loss in bacteria

Optimization of DNA polymerase mutation rates during bacterial evolution

Ionizing Radiation and Life

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