Fungal extracellular polymeric substance matrices – Highly specialized microenvironments that allow fungi to control soil organic matter decomposition reactions

Filamentous fungi play a key role in the terrestrial carbon cycle as they are the primary decomposers of lignocellulose in soil organic matter (SOM). Fungi secrete a wide range of oxidative and hydrolytic enzymes, and generate radicals through extracellular secondary metabolites to decompose SOM. To study fungal decomposition of SOM, the activities of isolated enzymes are typically studied as proxies for the decomposition activity of fungi. However, extracellular enzymes involved in lignocellulose decomposition are often bound to fungal extracellular polymeric substance (EPS) matrices. This association between extracellular enzymes and EPS matrices affects the activities of the enzymes. Moreover, extracellular enzymes and fungal cells are prone to attack by radicals and proteolytic enzymes themselves. Hence, these seemingly incompatible decomposition mechanisms must be regulated in some way in the fungal extracellular space to allow efficient decomposition of SOM, while preventing damage to secreted extracellular enzymes or the fungal cells themselves. We here review studies investigating the associations between fungal extracellular enzymes and EPS matrices and how these associations affect hydrolytic and oxidative reactions involved in SOM decomposition. Based on the knowledge compiled in the current review, we propose that fungal EPS matrices should be viewed as highly dynamic and functional parts of the fungal extracellular decomposition machinery. We also build a conceptual illustration that describes how the molecular composition and structure of fungal EPS matrices ensure that extracellular decomposition reactions only proceed at the right time and in the right place.