Mechanism of signal propagation in Physarum polycephalum

Abstract

Complex behaviors are typically associated with animals, but the capacity to integrate information and function as a coordinated individual is also a ubiquitous but poorly understood feature of organisms such as slime molds and fungi. Plasmodial slime molds grow as networks and use flexible, undifferentiated body plans to forage for food. How an individual communicates across its network remains a puzzle, but Physarum polycephalum has emerged as a novel model used to explore emergent dynamics. Within P. polycephalum, cytoplasm is shuttled in a peristaltic wave driven by cross-sectional contractions of tubes. We first track P. polycephalum's response to a localized nutrient stimulus and observe a front of increased contraction. The front propagates with a velocity comparable to the flow-driven dispersion of particles. We build a mathematical model based on these data and in the aggregate experiments and model identify the mechanism of signal propagation across a body: The nutrient stimulus triggers the release of a signaling molecule. The molecule is advected by fluid flows but simultaneously hijacks flow generation by causing local increases in contraction amplitude as it travels. The molecule is initiating a feedback loop to enable its own movement. This mechanism explains previously puzzling phenomena, including the adaptation of the peristaltic wave to organism size and P. polycephalum's ability to find the shortest route between food sources. A simple feedback seems to give rise to P. polycephalum's complex behaviors, and the same mechanism is likely to function in the thousands of additional species with similar behaviors. acellular slime mold | transport network | behavior | Taylor dispersion O ne of the great challenges of unraveling biological complexity is understanding what kind of and how much computational power is required for an organism to generate sophisticated behaviors. Behaviors are typically associated with a nervous system, but many organisms without nervous systems integrate information and function as coordinated individuals (1); examples range from the ability of Escherichia coli to move up chemical gradients (2) to the ability of a multicellular fungus to sense and precisely explore unoccupied space (3). A recently published and striking example of a complex behavior involves bacteria within a biofilm: When a Bacillus subtilis biofilm is deprived of nutrients, bacteria are able to grow networks of channels and evaporatively pump flows, creating intricate structures that benefit the entire community (4).Perhaps the archetypal example of an apparently simple organism able to generate sophisticated behaviors is the slime mold Physarum polycephalum, whose behaviors are repeatedly characterized as "intelligent." This slime mold is able to navigate mazes by finding the shortest route between different food sources (5) and has used its ability to reconstruct the transportation maps of major cities (6). The organism can structure its connections to different nutrient sources to optimize its diet...

Slime mould: The fundamental mechanisms of biological cognition

“…Composition of a set of networks basic topologies [110] Rules for biologically inspired design adaptive networks [107] Creating minimum transport networks [108] Decision making and "scatter" or state of indecision between different attractors for foraging [95] Adaptation Morphodynamic changes that depend on the environment for motility [119] Adaptation Rules for Biologically Inspired Design Adaptive Networks [107] The stimulus comes from attractants or repellants (external) provides the impetus for morphological adaptation [109]. Maximizing internal flows by adapting patterns of contraction to size [120].…”

Bidirectional Propagation of Signals and Nutrients in Fungal Networks via Specialized Hyphae

“…The concept of acropetal and basipetal cytoplasmic flows within a fungal colony is not new. Previous studies demonstrated bidirectional nutrient translocation within cords or rhizomorphs of saprophytic and ectomycorrhizal basidiomycetes [8,10,20,23,41,47,48]. Bidirectionality was explained to be due to dedicated acro-and basipetally oriented hyphal bundles within cords or rhizomorphs.…”

“…Bidirectionality was explained to be due to dedicated acro-and basipetally oriented hyphal bundles within cords or rhizomorphs. The use of periodic cytoplasmic flows to increase the dispersion of a molecule was also described for the network of syncytical veins in the slime mold Physarum polycepharum [48,49]. Tlalka et al showed for the first time that N transport (2-aminoisobutyric acid, [ 14 C]AIB) within cords of Phaenerochate velutina underlies a certain periodicity that was dependent on the subdomain of mycelium observed [50].…”

Oscillatory fluid flow drives scaling of contraction wave with system size

“…Fluid flows are fundamental to the functioning of all organisms. They play an important role in homeostasis, by spreading resources and biochemical signals [1], [2], [3]. They power deformations driving migration of many motile cells [4], [5], [6], and can even directly impact on organism size [7].…”

“…Again, flows are known to power organism migration [6], [20]. Moreover, stimulants that alter cortex contractility have recently been found to be advected with the fluid flows inside the cell [2]. This observation suggests that the physical transport by fluid flows is the key to longranged spatial coordination of cortex contractions and fluid flows.…”