Hierarchical Structure of the Program Used by Filamentous Fungi to Navigate in Confining Microenvironments.

Abstract

The spatial navigation of filamentous fungi was compared for three species, namely Pycnoporus cinnabarinus, Neurospora crassa wild type and ro-1 mutant, and Armillaria mellea, in microfluidic structures. The analysis of the navigation of these filamentous fungi in open and especially confining environments suggests that they perform space exploration using a hierarchical, three-layered system of information processing. The output of the space navigation of a single hypha is the result of coordination and competition between three programs with their corresponding subroutines: (i) the sensing of narrow passages (remote- or contact-based); (ii) directional memory; and (iii) branching (collision-induced or stochastic). One information-processing level up, the spatial distribution of multiple, closely collocated hyphae is the result of a combination of (i) negative autotropism and (ii) cytoplasm reallocation between closely related branches (with anastomosis as an alternative subroutine to increase robustness). Finally, the mycelium is the result of the sum of quasi-autonomous sub-populations of hyphae performing distribution in space in parallel based on the different spatial conditions and constraints found locally. The efficiency of space exploration by filamentous fungi appears to be the result of the synergy of various biological algorithms integrated into a hierarchical architecture of information processing, balancing complexity with specialization.