Multicellular behavior enables cooperation in microbial cell aggregates

During the degradation of biological materials such as biopolymers, extracellular enzymes liberate oligosaccharides that act as common goods and become available for all cells in the local neighborhood. This phenomenon can lead to cooperative growth, whereby cell-cell aggregation increases both the per-capita availability of resources and the per cell growth rate. However, aggregation can also have detrimental consequences for growth, as gradients form within aggregates limiting the resource accessibility. We used a computational model to show that high bacterial densities and high enzyme secretion rates restrict cooperation in aggregates larger than 10m, due to the emergence of polymer and oligomer counter-gradients. We compared these predictions against experiments performed with two well-studied alginate degrading Vibrios, one of which displayed a strong density dependent growth. We observed that both strains can form large aggregates (<50m), overcoming diffusion limitation by rearranging their internal structure. The non-cooperative, strong enzyme producer formed aggregates with internal channels that allowed exchange between the bulk environment and the aggregate core, whereas the cooperative, weak enzyme producer formed dense aggregates that developed a hollow structure as they grew. These internal structures allowed cells to avoid overcrowded areas near the core, enabling the development of large cell aggregates. Our study shows that bacterial behavior can help overcome competition imposed by resource gradients within cell aggregates.