Eugene Yurtsev

Oscillatory dynamics in a bacterial cross-protection mutualism

Significance Enzymatic deactivation of antibiotics is a cooperative behavior that can allow resistant cells to protect sensitive cells from antibiotics. The prevalence of this mechanism of antibiotic resistance in clinical isolates and in soil bacteria makes it important both clinically and ecologically. Here, we demonstrate experimentally that two populations of resistant bacteria can form a cross-protection mutualism in a two-drug environment, allowing the coculture to survive high antibiotic concentrations at which neither of the two strains can survive alone. Moreover, we find that daily growth-dilution cycles result in large oscillations in the relative abundances of the two strains, thus demonstrating that mutualisms can display striking dynamical behavior. Cooperation between microbes can enable microbial communities to survive in harsh environments. Enzymatic deactivation of antibiotics, a common mechanism of antibiotic resistance in bacteria, is a cooperative behavior that can allow resistant cells to protect sensitive cells from antibiotics. Understanding how bacterial populations survive antibiotic exposure is important both clinically and ecologically, yet the implications of cooperative antibiotic deactivation on the population and evolutionary dynamics remain poorly understood, particularly in the presence of more than one antibiotic. Here, we show that two Escherichia coli strains can form an effective cross-protection mutualism, protecting each other in the presence of two antibiotics (ampicillin and chloramphenicol) so that the coculture can survive in antibiotic concentrations that inhibit growth of either strain alone. Moreover, we find that daily dilutions of the coculture lead to large oscillations in the relative abundance of the two strains, with the ratio of abundances varying by nearly four orders of magnitude over the course of the 3-day period of the oscillation. At modest antibiotic concentrations, the mutualistic behavior enables long-term survival of the oscillating populations; however, at higher antibiotic concentrations, the oscillations destabilize the population, eventually leading to collapse. The two strains form a successful cross-protection mutualism without a period of coevolution, suggesting that similar mutualisms may arise during antibiotic treatment and in natural environments such as the soil.

Range expansions transition from pulled to pushed waves as growth becomes more cooperative in an experimental microbial population

Significance Species undergo range shifts in response to changing climate or following an introduction to a new environment. Invasions often incur significant economic cost and threaten biodiversity. Ecological theory predicts two distinct types of expansion waves, pulled and pushed, depending on the degree of cooperativity in the population. Although pulled and pushed invasions differ dramatically in how population-level properties such as the expansion rate depend on the organism-level properties such as rates of growth and dispersal, these theoretical predictions have not been tested empirically. Here, we use a microbial model system to perform these tests and demonstrate that pulled and pushed waves can be distinguished based on their dynamics. Range expansions are becoming more frequent due to environmental changes and rare long-distance dispersal, often facilitated by anthropogenic activities. Simple models in theoretical ecology explain many emergent properties of range expansions, such as a constant expansion velocity, in terms of organism-level properties such as growth and dispersal rates. Testing these quantitative predictions in natural populations is difficult because of large environmental variability. Here, we used a controlled microbial model system to study range expansions of populations with and without intraspecific cooperativity. For noncooperative growth, the expansion dynamics were dominated by population growth at the low-density front, which pulled the expansion forward. We found these expansions to be in close quantitative agreement with the classical theory of pulled waves by Fisher [Fisher RA (1937) Ann Eugen 7(4):355–369] and Skellam [Skellam JG (1951) Biometrika 38(1-2):196–218], suitably adapted to our experimental system. However, as cooperativity increased, the expansions transitioned to being pushed, that is, controlled by growth and dispersal in the bulk as well as in the front. Given the prevalence of cooperative growth in nature, understanding the effects of cooperativity is essential to managing invading species and understanding their evolution.

Correction: Resource Availability Modulates the Cooperative and Competitive Nature of a Microbial Cross-Feeding Mutualism

[This corrects the article DOI: 10.1371/journal.pbio.1002540.].