Spatial dynamics of synthetic microbial mutualists and their parasites

Abstract

A major force contributing to the emergence of novelty in nature is the presence of cooperative interactions, where two or more components of a system act in synergy, sometimes leading to higher-order, emergent phenomena. Within molecular evolution, the so called hypercycle defines the simplest model of an autocatalytic cycle, providing major theoretical insights on the evolution of cooperation in the early biosphere. These closed cooperative loops have also inspired our understanding of how catalytic loops appear in ecological systems. In both cases, hypercycle and ecological cooperative loops, the role played by space seems to be crucial for their stability and resilience against parasites. However, it is difficult to test these ideas in natural ecosystems, where time and spatial scales introduce considerable limitations. Here, we use engineered bacteria as a model system to a variety of environmental scenarios identifying trends that transcend the specific model system, such an enhanced genetic diversity in environments requiring mutualistic interactions. Interestingly, we show that improved environments can slow down mutualistic range expansions as a result of genetic drift effects preceding local resource depletion. Moreover, we show that a parasitic strain is excluded from the population during range expansions (which acknowledges a classical prediction). Nevertheless, environmental deterioration can reshape population interactions, this same strain becoming part of a three-species mutualistic web in scenarios in which the two-strain mutualism becomes non functional. The evolutionary and ecological implications for the design of synthetic ecosystems are outlined.

Cooperation mitigates diversity loss in a spatially expanding microbial population

“…However, it has been difficult to directly connect the empirical observations to theory (25), in part because these natural expansions cannot be replicated, and also because numerous environmental factors cannot be well-controlled. Microcosm experiments have helped address this chasm between theory and experiments by partially trading off realism for much better controlled and replicable biological systems (26)(27)(28)(29)(30).…”

Promoting synthetic symbiosis under environmental disturbances

“…If we undermine this dependency, it will affect the stability of the mutualistic interaction. Typically the system can be undermined by the introduction of a parasite [18]. We choose to change the environment itself without altering the genotypes of the interacting strains.…”

“…Via genetic manipulation, synthetic, cross-feeding, cooperation can be engineered within microbial communities [15, 16, 17, 13, 18]. Complex population dynamics in response to temporal, spatial, and environmental factors can thus be dissected by fine-tuning and manipulating these synthetic systems [19, 18]. We use Saccharomyces cerevisiae synthetic mutualism systems that rely on cross-feeding of amino acids between two strains [15].…”

“…The system uses feedback resistance (fbr) mutations in adenine and lysine biosynthesis pathways that results in overproduction of the corresponding amino acid. The strains used are referred to here as LYS↑ and dynamics of this cross-feeding system is comparableto a simple, but powerful theoretical model of self-organisation – a hypercycle – implicated at the origin of life as well as the formation of complex communities [20, 21, 11, 22, 18]. Here we develop a simple, but powerful and easily extendable phenomenological model.…”

Phase Transitions in Mutualistic Communities under Invasion

“…This type of symbiotic network is abundant in nature, appearing everywhere from auxotrophic bacteria [20,21] to nitrogen fixation in plant root microecosystems [22]. In particular, amino acid cross-feeding has been extensively characterized both theoretically and experimentally [23][24][25][26]. Fig.…”