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Concept: Physarum polycephalum

218

Several recent studies hint at shared patterns in decision-making between taxonomically distant organisms, yet few studies demonstrate and dissect mechanisms of decision-making in simpler organisms. We examine decision-making in the unicellular slime mould Physarum polycephalum using a classical decision problem adapted from human and animal decision-making studies: the two-armed bandit problem. This problem has previously only been used to study organisms with brains, yet here we demonstrate that a brainless unicellular organism compares the relative qualities of multiple options, integrates over repeated samplings to perform well in random environments, and combines information on reward frequency and magnitude in order to make correct and adaptive decisions. We extend our inquiry by using Bayesian model selection to determine the most likely algorithm used by the cell when making decisions. We deduce that this algorithm centres around a tendency to exploit environments in proportion to their reward experienced through past sampling. The algorithm is intermediate in computational complexity between simple, reactionary heuristics and calculation-intensive optimal performance algorithms, yet it has very good relative performance. Our study provides insight into ancestral mechanisms of decision-making and suggests that fundamental principles of decision-making, information processing and even cognition are shared among diverse biological systems.

Concepts: Biology, Microorganism, Eukaryote, Bacteria, Decision making, Organism, Physarum polycephalum, Computational complexity theory

147

Slime mould Physarum polycephalum is a single cell visible by the unaided eye. Let the slime mould span two electrodes with a single protoplasmic tube: if the tube is heated to approximately ≈40 °C, the electrical resistance of the protoplasmic tube increases from ≈3 MΩ to ≈10,000 MΩ. The organism’s resistance is not proportional nor correlated to the temperature of its environment. Slime mould can therefore not be considered as a thermistor but rather as a thermic switch. We employ the P. polycephalum thermic switch to prototype hybrid electrical analog summator, NAND gates, and cascade the gates into Flip-Flop latch. Computing operations performed on this bio-hybrid computing circuitry feature high repeatability, reproducibility and comparably low propagation delays.

Concepts: Electronic engineering, Heat, Series and parallel circuits, Electric current, Resistor, Slime molds, Slime mold, Physarum polycephalum

143

Mitochondrial RNAs in the acellular slime mold Physarum polycephalum contain nucleotides that are not encoded in the mitochondrial genes from which they are transcribed. These site-specific changes are quite extensive, comprising ~4% of the residues within mRNAs and ~2% of rRNAs and tRNAs. These “extra” nucleotides are added co-transcriptionally, but the means by which this is accomplished have not been elucidated. The cox1 mRNA also contains four sites of C to U changes, which occur post-transcriptionally, most likely via targeted deamination. The currently available in vitro systems for studying P. polycephalum editing are limited in that the template is the entire ~63,000 bp mitochondrial genome. This presents a significant challenge when trying to define the signals that specify editing sites. In an attempt to overcome this issue, a method for introducing DNA into isolated P. polycephalum mitochondria via electroporation has been developed. Exogenous DNA is expressed, but the transcripts synthesized from these templates are not edited under the conditions tested. However, transcripts derived from the mitochondrial genome are accurately edited after electroporation, indicating that the editing machinery is still functional. These findings suggest that this method may ultimately provide a feasible approach to elucidating editing signals.

Concepts: Messenger RNA, Gene expression, Bacteria, Genetics, Physarum polycephalum, Gene, RNA, DNA

37

Spatial memory enhances an organism’s navigational ability. Memory typically resides within the brain, but what if an organism has no brain? We show that the brainless slime mold Physarum polycephalum constructs a form of spatial memory by avoiding areas it has previously explored. This mechanism allows the slime mold to solve the U-shaped trap problem-a classic test of autonomous navigational ability commonly used in robotics-requiring the slime mold to reach a chemoattractive goal behind a U-shaped barrier. Drawn into the trap, the organism must rely on other methods than gradient-following to escape and reach the goal. Our data show that spatial memory enhances the organism’s ability to navigate in complex environments. We provide a unique demonstration of a spatial memory system in a nonneuronal organism, supporting the theory that an externalized spatial memory may be the functional precursor to the internal memory of higher organisms.

Concepts: Fungus, Psychology, Biology, Slime molds, Slime mold, Brain, Hippocampus, Physarum polycephalum

28

In spite of the ecological importance of protists, few data are available on their distribution in soil. This investigation is the first of its kind on what could be the major components of the soil protistan community, the Myxomycetes or plasmodial slime-moulds, a monophyletic class in the phylum Amoebozoa. Myxomycetes have a complex life cycle culminating in the formation of mainly macroscopic fruiting bodies, highly variable in shape and colour, that can be found in every terrestrial biome. Despite their prevalence, they are paradoxically absent from environmental DNA sampling studies. We obtained myxomycete SSU rRNA gene sequences from soil-extracted RNAs by using specific primers. Soil samples were collected in three mountain ranges (France, Scotland and Japan). Our study revealed an unexpectedly high diversity of dark-spored Myxomycetes with the recovery of 74 phylotypes. Of these, 74 % had less than 98 % identity with known sequences, thus showing a hidden diversity; there was little overlap between localities, implying biogeographical patterns. Few phylotypes were dominant and many were unique, consistent with the “rare biosphere” phenomenon. Our study provides first detailed insight into community composition of this ecologically important group of protists, establishing means for future studies of their distribution, abundance and ecology. © 2012 Federation of European Microbiological Societies. Published by Blackwell Publishing Ltd.All rights reserved.

Concepts: Ecosystem, Physarum polycephalum, Biodiversity, Ribosomal RNA, Protist, RNA, Slime mold, Ecology

24

An amoeboid unicellular organism, a plasmodium of the true slime mold Physarum polycephalum, exhibits complex spatiotemporal oscillatory dynamics and sophisticated information processing capabilities while deforming its amorphous body. We previously devised an ‘amoeba-based computer (ABC),’ that implemented optical feedback control to lead this amoeboid organism to search for a solution to the traveling salesman problem (TSP). In the ABC, the shortest TSP route (the optimal solution) is represented by the shape of the organism in which the body area (nutrient absorption) is maximized while the risk of being exposed to aversive light stimuli is minimized. The shortness of the TSP route found by ABC, therefore, serves as a quantitative measure of the optimality of the decision made by the organism. However, it remains unclear how the decision-making ability of the organism originates from the oscillatory dynamics of the organism. We investigated the number of coexisting traveling waves in the spatiotemporal patterns of the oscillatory dynamics of the organism. We show that a shorter TSP route can be found when the organism exhibits a lower number of traveling waves. The results imply that the oscillatory dynamics are highly coordinated throughout the global body. Based on the results, we discuss the fact that the decision-making ability of the organism can be enhanced not by uncorrelated random fluctuations, but by its highly coordinated oscillatory dynamics.

Concepts: Feedback, Microorganism, Function problem, Protist, Operations research, Travelling salesman problem, Slime mold, Physarum polycephalum

18

Learning, defined as a change in behaviour evoked by experience, has hitherto been investigated almost exclusively in multicellular neural organisms. Evidence for learning in non-neural multicellular organisms is scant, and only a few unequivocal reports of learning have been described in single-celled organisms. Here we demonstrate habituation, an unmistakable form of learning, in the non-neural organism Physarum polycephalum In our experiment, using chemotaxis as the behavioural output and quinine or caffeine as the stimulus, we showed that P. polycephalum learnt to ignore quinine or caffeine when the stimuli were repeated, but responded again when the stimulus was withheld for a certain time. Our results meet the principle criteria that have been used to demonstrate habituation: responsiveness decline and spontaneous recovery. To distinguish habituation from sensory adaptation or motor fatigue, we also show stimulus specificity. Our results point to the diversity of organisms lacking neurons, which likely display a hitherto unrecognized capacity for learning, and suggest that slime moulds may be an ideal model system in which to investigate fundamental mechanisms underlying learning processes. Besides, documenting learning in non-neural organisms such as slime moulds is centrally important to a comprehensive, phylogenetic understanding of when and where in the tree of life the earliest manifestations of learning evolved.

Concepts: Protist, Cell, Psychology, Species, Physarum polycephalum, Microorganism, Bacteria, Organism

9

Self-organized mechanisms are frequently encountered in nature and known to achieve flexible, adaptive control and decision-making. Noise plays a crucial role in such systems: It can enable a self-organized system to reliably adapt to short-term changes in the environment while maintaining a generally stable behavior. This is fundamental in biological systems because they must strike a delicate balance between stable and flexible behavior. In the present paper we analyse the role of noise in the decision-making of the true slime mold Physarum polycephalum, an important model species for the investigation of computational abilities in simple organisms. We propose a simple biological experiment to investigate the reaction of P. polycephalum to time-variant risk factors and present a stochastic extension of an established mathematical model for P. polycephalum to analyze this experiment. It predicts that-due to the mechanism of stochastic resonance-noise can enable P. polycephalum to correctly assess time-variant risk factors, while the corresponding noise-free system fails to do so. Beyond the study of P. polycephalum we demonstrate that the influence of noise on self-organized decision-making is not tied to a specific organism. Rather it is a general property of the underlying process dynamics, which appears to be universal across a wide range of systems. Our study thus provides further evidence that stochastic resonance is a fundamental component of the decision-making in self-organized macroscopic and microscopic groups and organisms.

Concepts: Decision theory, Decision making, Life, Slime mold, Risk, Organism, Biology, Physarum polycephalum

4

How social groups and organisms decide between alternative feeding sites or shelters has been extensively studied both experimentally and theoretically. One key result is the existence of a symmetry-breaking bifurcation at a critical system size, where there is a switch from evenly distributed exploitation of all options to a focussed exploitation of just one. Here we present a decision-making model in which symmetry-breaking is followed by a symmetry restoring bifurcation, whereby very large systems return to an even distribution of exploitation amongst options. The model assumes local positive feedback, coupled with a negative feedback regulating the flow toward the feeding sites. We show that the model is consistent with three different strains of the slime mold Physarum polycephalum, choosing between two feeding sites. We argue that this combination of feedbacks could allow collective foraging organisms to react flexibly in a dynamic environment.

Concepts: Slime molds, Cybernetics, Biology, Slime mold, Positive feedback, Negative feedback, Feedback, Physarum polycephalum

3

Physarum Polycephalum is a single cell visible by unaided eye. This is a plasmodial, vegetative stage of acellular slime mould. This single cell has myriad of nuclei which contribute to a network of bio-chemical oscillators responsible for the slime mould’s distributed sensing, concurrent information processing and decision making, and parallel actuation. When presented with a spatial configuration of sources of nutrients, the slime mould spans the sources with networks of its protoplasmic tube. These networks belong to a family of planar proximity graphs. The protoplasmic networks also show a degree of similarity to vehicular transport networks. Previously, we have shown that the foraging behaviour of the slime mould can be applied in archaeological research to complement and enhance conventional geographic information system tools. The results produced suffered from limitation of a flat substrate: transport routes imitated by the slime mould did not reflect patterns of elevations. To overcome the limitation of the ‘flat world’ we constructed a three-dimensional model of Balkans. In laboratory experiments and computer modelling we uncovered patterns of the foraging behaviour that might shed a light onto development of Roman roads in the Balkans during the imperial period (1st century BC - 4th century AD).

Concepts: Geographic information system, 4th century, Roman roads, Road, Centuries, Slime mold, Physarum polycephalum, Ancient Rome