Patterns of spatial positioning of individuals within microbial communities are often critical to community function. However, understanding patterning in natural communities is hampered by the multitude of cell–cell and cell–environment interactions as well as environmental variability. Here, through simulations and experiments on communities in defined environments, we examined how ecological interactions between two distinct partners impacted community patterning. We found that in strong cooperation with spatially localized large fitness benefits to both partners, a unique pattern is generated: partners spatially intermixed by appearing successively on top of each other, insensitive to initial conditions and interaction dynamics. Intermixing was experimentally observed in two obligatory cooperative systems: an engineered yeast community cooperating through metabolite-exchanges and a methane-producing community cooperating through redox-coupling. Even in simulated communities consisting of several species, most of the strongly-cooperating pairs appeared intermixed. Thus, when ecological interactions are the major patterning force, strong cooperation leads to partner intermixing.
Microorganisms such as bacteria, archaea and tiny eukaryotes are found throughout the biosphere. Some of these microorganisms are pathogens that cause diseases in animals, while others provide nutrients, including essential amino acids and vitamins; there are also microorganisms that have critical roles in recycling elements such as carbon, nitrogen and oxygen in the biosphere. In the natural world, microorganisms interact with their environment and with each other, often competing for space, light and nutrients, but sometimes they act cooperatively, which benefits all parties involved.
Microbial communities exhibit spatial patterns that reflect the relative positioning of different microbes in a community. These patterns can be critical for the proper functioning of a microbial community. For example, in the microbial granules that digest organic compounds in waste water, the stratified pattern of different microbial species can be thought of as a sequence of catalysts needed to perform a series of biochemical processing steps. Thus, it is important to understand the mechanisms that drive pattern formation in multispecies communities.
Now, through a combination of simulations and experiments, Momeni et al. have identified two features of spatial patterns in two-population microbial communities when pattern formation is driven by fitness effects related to the ecological interactions between cells. First, interactions that confer significant advantages to at least one of the populations can potentially result in the generation of a stable community; the community is stable in the sense that if it is disturbed, it will return to its stable population composition following the disturbance. Indeed, in engineered Saccharomyces cerevisiae communities, very different initial population ratios converged to the same value over time when one strain depended on the other strain, or when the two strains depended on each other, but not when the two strains competed.
The second feature applies to microbial communities composed of two cooperating populations: whereas two populations that compete with each other tend to segregate, cooperation results in the members of the two populations mixing together. Momeni et al. observe the formation of such an “intermixed” community in simulations, and also in two experimental systems that involve cooperation—a community containing two different strains of yeast cooperating through metabolite exchange, and a biofilm in which Methanococcus maripaludis, an archaeon that produces methane, cooperates with the bacterium Desulfovibrio vulgaris.
These two features of spatial patterning are conceptually similar to the competitive exclusion principle, which states that two species competing for the same resources cannot stably coexist if competition is the sole force at work. This principle has, therefore, encouraged scientists to search for the other forces that must be responsible for the coexistence of different species. Similarly, by predicting the sorts of patterns that will form when the fitness effects of ecological interactions between cells are the only forces at work, Momeni et al. lay the groundwork for investigations into other mechanisms, such as cell–environment interactions and active cell motility, that can govern pattern formation in microbial communities.