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Abstract
Microbial consortia constitute a majority of the earth's biomass, but little is known about how these cooperating communities persist despite competition among community members. Theory suggests that non-random spatial structures contribute to the persistence of mixed communities; when particular structures form, they may provide associated community members with a growth advantage over unassociated members. If true, this has implications for the rise and persistence of multi-cellular organisms. However, this theory is difficult to study because we rarely observe initial instances of non-random physical structure in natural populations. Using two engineered strains of Escherichia coli that constitute a synthetic symbiotic microbial consortium, we fortuitously observed such spatial self-organization. This consortium forms a biofilm and, after several days, adopts a defined layered structure that is associated with two unexpected, measurable growth advantages. First, the consortium cannot successfully colonize a new, downstream environment until it self-organizes in the initial environment; in other words, the structure enhances the ability of the consortium to survive environmental disruptions. Second, when the layered structure forms in downstream environments the consortium accumulates significantly more biomass than it did in the initial environment; in other words, the structure enhances the global productivity of the consortium. We also observed that the layered structure only assembles in downstream environments that are colonized by aggregates from a previous, structured community. These results demonstrate roles for self-organization and aggregation in persistence of multi-cellular communities, and also illustrate a role for the techniques of synthetic biology in elucidating fundamental biological principles.
Highlights
The vast majority of living biomass consists of single-celled organisms, but the existence of higher organisms demonstrates that interacting networks of cell populations can thrive despite competition between them [1,2]
We describe a synthetic symbiotic microbial consortium that allows us to address some of these questions
The synthetic symbiotic consortium consists of two engineered populations of Escherichia coli which are not viable alone, but can grow and form biofilms when grown together (Fig 1A)
Summary
The vast majority of living biomass consists of single-celled organisms, but the existence of higher organisms demonstrates that interacting networks of cell populations can thrive despite competition between them [1,2]. Experimental studies of the formation and benefits of specific physical structures in mixed microbial communities are few. An advantage of using synthetic, or engineered, consortia for studies of this nature is that complex communal behaviors such as symbiosis can be implemented under defined and tunable experimental control [9,19,20,21]. Very simple relative to naturally-occurring microbial consortia, engineered ecosystems can exhibit behaviors that mimic those found in nature and, because the interactions of engineered consortia can be controlled and more fully characterized, can provide insight into the development and persistence of natural communities
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