Employment of self-organisation to achieve economy of scale in biology

Abstract

Self-organisation is a striking phenomenon that fascinates many. Especially in homogeneous environments, the question why - and how - heterogeneous structure emerges is intriguing. We find a novel function of self-organisation in biology at the colony margin of the fungus Aspergillus niger. Here, the collection of interconnected hyphae splits into two subpopulations with differential expression of amylolytic enzymes. These enzymes are secreted and together break down starch in a multi-step process. We show with a mathematical model that concentrating production and secretion of all enzymes by part of the hyphae results in more efficient substrate degradation, as compared to equal distribution over all hyphae. This model result is corroborated by experimental observations of increased metabolic activity of the wild type that displays hyphal heterogeneity as compared to a mutant that lost this heterogeneity. The intermediate product (iso)maltose is known to induce upregulation of amylolytic enzymes. Incorporating this in the model enables the formation of hyphal heterogeneity through self-organisation. We generalize our results to a large class of multi- step processes and demonstrate wide applicability. Importantly, this shows that self-organisation may not be incidental, but favorable and thus selectable since it enhances efficiency. Due to its impact on system functioning, its study is not only of academic interest but also of practical value.