Self-Organization, Layered Structure, and Aggregation Enhance Persistence of a Synthetic Biofilm Consortium

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.

Cell morphology drives spatial patterning in microbial communities

“…Metabolic exchanges between species are often associated with a layered structure in biofilms (36)(37)(38)(53)(54)(55), which suggests that shapemediated self-organization could be used by experimenters to promote desirable colony structures. Furthermore, our results show that cell shape can affect the degree of strain mixing within the colony, which could in turn be used to control selective pressures for or against certain social strategies.…”

Interplay of physical mechanisms and biofilm processes: review of microfluidic methods

“…A growing number of synthetic biology efforts are focusing on either engineering cells for operation within a biofilm context or manipulating biofilms [188–190]. LOC devices can aid the characterization and optimization of future pursuits in this area by providing control over cell confinement, hydrodynamics, and inducer concentrations.…”

Synthetic Biology: opportunities for Chilean bioindustry and education

“…The engineering of multicellular populations could lead to the programming of pattern formation, artifi cial cell consortia and synthetic ecosystems (Brenner et al, 2008, Brenner and Arnold, 2011, Shou et al, 2007Wintermute and Silver, 2010;Chuang, 2012). The establishment and maintenance of distinct cohorts of cells might be used for example to facilitate the optimization of metabolic pathways by separating inhibitory intermediate metabolites.…”