Abstract

Transport efficiency and resilience in mycelial networks

Transport networks are vital components of multicellular organisms, distributing nutrients and removing waste products. Animal cardiovascular and respiratory systems, and plant vasculature, are fractal-like branching trees whose architecture determines universal scaling laws in these organisms. In contrast, transport systems in multicellular fungi are not expected to fit into this conceptual framework, as they have evolved to explore the environment rather than ramify as a three-dimensional organism. Many fungi grow as a foraging mycelium, formed by the branching and fusion of threadlike hyphae. This process gives rise to a complex network that continuously adapts to its environment. However, the properties of the network and its dynamic behaviour have not yet been characterised. Using a range of woodland saprotrophic basidiomycetes, we have examined network development and its nutrient transport characteristics over a range of scales, using a combination of imaging, modelling, gene expression profiling and metabolomics.

We have found that fungal networks can display both a high transport capacity and high resilience to damage. These properties are enhanced as the network grows, while the relative amount of material used to build the network decreases. Thus, mycelia achieve the seemingly competing goals of efficient transport and resilience, with decreasing relative investment, by selective reinforcement and recycling of transport pathways. The fungal network demonstrates that indeterminate, decentralised systems can yield highly adaptive networks.

To test the predictions from the theoretical analysis of transport, we have mapped the distribution of non-metabolised, radiolabelled amino-acid and sugar analogues during mycelial development in spatially heterogenous resource environments using photon-counting scintillation imaging. These studies have revealed a number of novel phenomena, including a marked pulsatile transport component superimposed on a rapid underlying flux, preferential resource allocation to C-rich sinks, abrupt switching between different pre-existing transport routes and organization of the network into well demarcated domains differing in phase or frequency of oscillations. Furthermore, fusion between compatible individuals leads to rapid nutrient re-distribution and formation of a fully synchronised super-colony.

Overall the spatial organisation of these mycelial systems provide an almost unique opportunity for any eukaryotic system to directly correlate metabolite levels, nutrient fluxes, gene expression patterns and morphological development.