Slime Mold Physarum Research Articles

Discovery of the first unconventional myosin: Acanthamoeba myosin-I.

Having characterized actin from Acanthamoeba castellanii (Weihing and Korn, Biochemistry, 1971, 10, 590-600) and knowing that myosin had been isolated from the slime mold Physarum (Hatano and Tazawa, Biochim. Biophys. Acta, 1968, 154, 507-519; Adelman and Taylor, Biochemistry, 1969, 8, 4976-4988), we set out in 1969 to find myosin in Acanthamoeba. We used K-EDTA-ATPase activity to assay myosin, because it is a unique feature of muscle myosins. After slightly less than 3years, we purified a K-EDTA ATPase that interacted with actin. Actin filaments stimulated the Mg-ATPase activity of the crude enzyme, but this was lost with further purification. Recombining fractions from the column where this activity was lost revealed a "cofactor" that allowed actin filaments to stimulate the Mg-ATPase of the purified enzyme. The small size of the heavy chain and physical properties of the purified myosin were unprecedented, so many were skeptical, assuming that our myosin was a proteolytic fragment of a larger myosin similar to muscle or Physarum myosin. Subsequently our laboratories confirmed that Acanthamoeba myosin-I is a novel unconventional myosin that interacts with membrane lipids (Adams and Pollard, Nature, 1989, 340 (6234), 565-568) and that the cofactor is a myosin heavy chain kinase (Maruta and Korn, J. Biol. Chem., 1977, 252, 8329-8332). Phylogenetic analysis (Odronitz and Kollmar, Genome Biology, 2007, 8, R196) later established that class I myosin was the first myosin to appear during the evolution of eukaryotes.

The Incubascope: a simple, compact and large field of view microscope for long-term imaging inside an incubator.

Optical imaging has rapidly evolved in the last decades. Sophisticated microscopes allowing optical sectioning for three-dimensional imaging or sub-diffraction resolution are available. Due to price and maintenance issues, these microscopes are often shared between users in facilities. Consequently, long-term access is often prohibited and does not allow to monitor slowly evolving biological systems or to validate new models like organoids. Preliminary coarse long-term data that do not require acquisition of terabytes of high-resolution images are important as a first step. By contrast with expensive all-in-one commercialized stations, standard microscopes equipped with incubator stages offer a more cost-effective solution despite imperfect long-run atmosphere and temperature control. Here, we present the Incubascope, a custom-made compact microscope that fits into a table-top incubator. It is cheap and simple to implement, user-friendly and yet provides high imaging performances. The system has a field of view of 5.5 × 8 mm2, a 3 μm resolution, a 10 frames per second acquisition rate, and is controlled with a Python-based graphical interface. We exemplify the capabilities of the Incubascope on biological applications such as the hatching of Artemia salina eggs, the growth of the slime mould Physarum polycephalum and of encapsulated spheroids of mammalian cells.

Iteratively reweighted least squares and slime mold dynamics: connection and convergence

We present a connection between two dynamical systems arising in entirely different contexts: the Iteratively Reweighted Least Squares (IRLS) algorithm used in compressed sensing and sparse recovery to find a minimum $$\ell _1$$ -norm solution in an affine space, and the dynamics of a slime mold (Physarum polycephalum) that finds the shortest path in a maze. We elucidate this connection by presenting a new dynamical system – Meta-Algorithm – and showing that the IRLS algorithms and the slime mold dynamics can both be obtained by specializing it to disjoint sets of variables. Subsequently, and building on work on slime mold dynamics for finding shortest paths, we prove convergence and obtain complexity bounds for the Meta-Algorithm that can be viewed as a “damped” version of the IRLS algorithm. A consequence of this latter result is a slime mold dynamics to solve the undirected transshipment problem that computes a $$(1+\varepsilon )-$$ approximate solution in time polynomial in the size of the input graph, maximum edge cost, and $$\frac{1}{\varepsilon }$$ – a problem that was left open by the work of (Bonifaci V et al. [10] Physarum can compute shortest paths. Kyoto, Japan, pp. 233–240).

Memory inception and preservation in slime moulds: the quest for a common mechanism.

Learning and memory are indisputably key features of animal success. Using information about past experiences is critical for optimal decision-making in a fluctuating environment. Those abilities are usually believed to be limited to organisms with a nervous system, precluding their existence in non-neural organisms. However, recent studies showed that the slime mould Physarum polycephalum, despite being unicellular, displays habituation, a simple form of learning. In this paper, we studied the possible substrate of both short- and long-term habituation in slime moulds. We habituated slime moulds to sodium, a known repellent, using a 6 day training and turned them into a dormant state named sclerotia. Those slime moulds were then revived and tested for habituation. We showed that information acquired during the training was preserved through the dormant stage as slime moulds still showed habituation after a one-month dormancy period. Chemical analyses indicated a continuous uptake of sodium during the process of habituation and showed that sodium was retained throughout the dormant stage. Lastly, we showed that memory inception via constrained absorption of sodium for 2 h elicited habituation. Our results suggest that slime moulds absorbed the repellent and used it as a 'circulating memory'. This article is part of the theme issue 'Liquid brains, solid brains: How distributed cognitive architectures process information'.

Symmetry breaking and inter-clonal behavioural variability in a slime mould.

Cells are dynamic systems capable of switching from isotropic growth to polarized growth even in the absence of any pre-existing external asymmetry. Here, we study this process of symmetry breaking in the acellular slime mould Physarum polycephalum. In these experiments, slime moulds could grow on two identical opposed sources of calcium. We highlighted a positive correlation between growth dynamic, level of symmetry breaking and calcium concentration. We identified three populations of slime moulds within our clonal lineage with similar symmetry breaking behaviours but different motility characteristics. These behavioural differences between slime moulds emerged in the absence of any environmental differences. Such behavioural plasticity could generate cellular diversity, which can be critical for survival.

Fluid flows shaping organism morphology.

A dynamic self-organized morphology is the hallmark of network-shaped organisms like slime moulds and fungi. Organisms continuously reorganize their flexible, undifferentiated body plans to forage for food. Among these organisms the slime mould Physarum polycephalumhas emerged as a model to investigate how an organism can self-organize their extensive networks and act as a coordinated whole. Cytoplasmic fluid flows flowing through the tubular networks have been identified as the key driver of morphological dynamics. Inquiring how fluid flows can shape living matter from small to large scales opens up many new avenues for research. This article is part of the theme issue 'Self-organization in cell biology'.

Direct transfer of learned behaviour via cell fusion in non-neural organisms.

Cell fusion is a fundamental phenomenon observed in all eukaryotes. Cells can exchange resources such as molecules or organelles during fusion. In this paper, we ask whether a cell can also transfer an adaptive response to a fusion partner. We addressed this question in the unicellular slime mould Physarum polycephalum, in which cell-cell fusion is extremely common. Slime moulds are capable of habituation, a simple form of learning, when repeatedly exposed to an innocuous repellent, despite lacking neurons and comprising only a single cell. In this paper, we present a set of experiments demonstrating that slime moulds habituated to a repellent can transfer this adaptive response by cell fusion to individuals that have never encountered the repellent. In addition, we show that a slime mould resulting from the fusion of a minority of habituated slime moulds and a majority of unhabituated ones still shows an adaptive response to the repellent. Finally, we further reveal that fusion must last a certain time to ensure an effective transfer of the behavioural adaptation between slime moulds. Our results provide strong experimental evidence that slime moulds exhibit transfer of learned behaviour during cell fusion and raise the possibility that similar phenomena may occur in other cell-cell fusion systems.

Periodic traction in migrating large amoeba of Physarum polycephalum.

The slime mould Physarum polycephalum is a giant multinucleated cell exhibiting well-known Ca(2+)-dependent actomyosin contractions of its vein network driving the so-called cytoplasmic shuttle streaming. Its actomyosin network forms both a filamentous cortical layer and large fibrils. In order to understand the role of each structure in the locomotory activity, we performed birefringence observations and traction force microscopy on excised fragments of Physarum. After several hours, these microplasmodia adopt three main morphologies: flat motile amoeba, chain types with round contractile heads connected by tubes and motile hybrid types. Each type exhibits oscillations with a period of about 1.5 min of cell area, traction forces and fibril activity (retardance) when fibrils are present. The amoeboid types show only peripheral forces while the chain types present a never-reported force pattern with contractile rings far from the cell boundary under the spherical heads. Forces are mostly transmitted where the actomyosin cortical layer anchors to the substratum, but fibrils maintain highly invaginated structures and contribute to forces by increasing the length of the anchorage line. Microplasmodia are motile only when there is an asymmetry in the shape and/or the force distribution.

Enhancing adaptability of amoeboid robot by synergetically coupling two decentralized controllers inspired by true slime mold

Autonomous decentralized control is a key concept for understanding the adaptive and versatile behaviors of living systems. To establish a design methodology for such a controller for robotic systems, we have proposed a fully decentralized control system, inspired by biochemical oscillators in true slime mold ( Physarum polycephalum), which allows a modular robot to exhibit adaptive and versatile behaviors. However, in real living systems, many adaptation mechanisms with different time constants co-exist without conflict in the body (e.g., reflex, learning, growth and evolution); this contributes to the amazingly resilient and intelligent behaviors of living systems. It is well known that in true slime mold, long time-scale morphological changes coexist with the oscillatory behavior stemming from biochemical oscillators. In the present study, we have designed a mathematical model and real physical robot in which two decentralized controllers are incorporated. Numerical and experimental results show that by combining the controllers with different time constants, a robot can use the proposed model to successfully negotiate a narrow aisle by deforming its body shape dynamically.

A survey of PPR proteins identifies DYW domains like those of land plant RNA editing factors in diverse eukaryotes

The pentatricopeptide repeat modules of PPR proteins are key to their sequence-specific binding to RNAs. Gene families encoding PPR proteins are greatly expanded in land plants where hundreds of them participate in RNA maturation, mainly in mitochondria and chloroplasts. Many plant PPR proteins contain additional carboxyterminal domains and have been identified as essential factors for specific events of C-to-U RNA editing, which is abundant in the two endosymbiotic plant organelles. Among those carboxyterminal domain additions to plant PPR proteins, the so-called DYW domain is particularly interesting given its similarity to cytidine deaminases. The frequency of organelle C-to-U RNA editing and the diversity of DYW-type PPR proteins correlate well in plants and both were recently identified outside of land plants, in the protist Naegleria gruberi. Here we present a systematic survey of PPR protein genes and report on the identification of additional DYW-type PPR proteins in the protists Acanthamoeba castellanii, Malawimonas jakobiformis, and Physarum polycephalum. Moreover, DYW domains were also found in basal branches of multi-cellular lineages outside of land plants, including the alga Nitella flexilis and the rotifers Adineta ricciae and Philodina roseola. Intriguingly, the well-characterized and curious patterns of mitochondrial RNA editing in the slime mold Physarum also include examples of C-to-U changes. Finally, we identify candidate sites for mitochondrial RNA editing in Malawimonas, further supporting a link between DYW-type PPR proteins and C-to-U editing, which may have remained hitherto unnoticed in additional eukaryote lineages.

Current-reinforced random walks for constructing transport networks

Biological systems that build transport networks, such as trail-laying ants and the slime mould Physarum, can be described in terms of reinforced random walks. In a reinforced random walk, the route taken by ‘walking’ particles depends on the previous routes of other particles. Here, we present a novel form of random walk in which the flow of particles provides this reinforcement. Starting from an analogy between electrical networks and random walks, we show how to include current reinforcement. We demonstrate that current-reinforcement results in particles converging on the optimal solution of shortest path transport problems, and avoids the self-reinforcing loops seen in standard density-based reinforcement models. We further develop a variant of the model that is biologically realistic, in the sense that the particles can be identified as ants and their measured density corresponds to those observed in maze-solving experiments on Argentine ants. For network formation, we identify the importance of nonlinear current reinforcement in producing networks that optimize both network maintenance and travel times. Other than ant trail formation, these random walks are also closely related to other biological systems, such as blood vessels and neuronal networks, which involve the transport of materials or information. We argue that current reinforcement is likely to be a common mechanism in a range of systems where network construction is observed.

Speed–accuracy trade-offs during foraging decisions in the acellular slime mould Physarum polycephalum

Speed-accuracy trade-offs (SATs) are thought to be a fundamental feature of biological information processing, yet most evidence of SATs comes from animals. Here, we examine SATs in the foraging decisions of an acellular, amoeboid organism: the slime mould Physarum polycephalum. Slime moulds were given a simple discrimination task: selecting the highest-quality food item from a set of three options. We investigated the effect of two stressors, light exposure and hunger, on the speed and accuracy of decision-making. We also examined the effect of task difficulty. When given a difficult discrimination task, stressed individuals tend to make faster decisions than non-stressed individuals. This effect was reversed in plasmodia given easy discrimination tasks, where stressed individuals made slower decisions than non-stressed individuals. We found evidence of SATs, such that individuals who made fast decisions were more likely to make costly errors by selecting the worst possible food option. Our results suggest that SATs occur in a wider range of taxa than previously considered.

Irrational decision-making in an amoeboid organism: transitivity and context-dependent preferences

Most models of animal foraging and consumer choice assume that individuals make choices based on the absolute value of items and are therefore 'economically rational'. However, frequent violations of rationality by animals, including humans, suggest that animals use comparative valuation rules. Are comparative valuation strategies a consequence of the way brains process information, or are they an intrinsic feature of biological decision-making? Here, we examine the principles of rationality in an organism with radically different information-processing mechanisms: the brainless, unicellular, slime mould Physarum polycephalum. We offered P. polycephalum amoebas a choice between food options that varied in food quality and light exposure (P. polycephalum is photophobic). The use of an absolute valuation rule will lead to two properties: transitivity and independence of irrelevant alternatives (IIA). Transitivity is satisfied if preferences have a consistent, linear ordering, while IIA states that a decision maker's preference for an item should not change if the choice set is expanded. A violation of either of these principles suggests the use of comparative rather than absolute valuation rules. Physarum polycephalum satisfied transitivity by having linear preference rankings. However, P. polycephalum's preference for a focal alternative increased when a third, inferior quality option was added to the choice set, thus violating IIA and suggesting the use of a comparative valuation process. The discovery of comparative valuation rules in a unicellular organism suggests that comparative valuation rules are ubiquitous, if not universal, among biological decision makers.

Sampling Gene Diversity Across the Supergroup Amoebozoa: Large EST Data Sets from Acanthamoeba castellanii, Hartmannella vermiformis, Physarum polycephalum, Hyperamoeba dachnaya and Hyperamoeba sp.

From comparative analysis of EST data for five taxa within the eukaryotic supergroup Amoebozoa, including two free-living amoebae (Acanthamoeba castellanii, Hartmannella vermiformis) and three slime molds (Physarum polycephalum, Hyperamoeba dachnaya and Hyperamoeba sp.), we obtained new broad-range perspectives on the evolution and biosynthetic capacity of this assemblage. Together with genome sequences for the amoebozoans Dictyostelium discoideum and Entamoeba histolytica, and including partial genome sequence available for A. castellanii, we used the EST data to identify genes that appear to be exclusive to the supergroup, and to specific clades therein. Many of these genes are likely involved in cell-cell communication or differentiation. In examining on a broad scale a number of characters that previously have been considered in simpler cross-species comparisons, typically between Dictyostelium and Entamoeba, we find that Amoebozoa as a whole exhibits striking variation in the number and distribution of biosynthetic pathways, for example, ones for certain critical stress-response molecules, including trehalose and mannitol. Finally, we report additional compelling cases of lateral gene transfer within Amoebozoa, further emphasizing that although this process has influenced genome evolution in all examined amoebozoan taxa, it has done so to a variable extent.

Graviresponses in fungi and slime molds

AbstractThe analysis of gravisensing in fungi has not yet proceeded as far as in other systems, such as sensory cells for maintenance of equilibrium in crustaceans and vertebrates, Chara rhizoids or plant roots with regard to positive gravitropism. However, considerable progress has recently been made with several fungal systems in the field of graviresponses. This particularly holds true for the molecular basis of primary events. In this review three systems of increasing complexity are considered: the slime molds Physarum and Dictyostelium, which exhibit gravitaxis, the negative gravitropic sporangium of the zygomycete Phycomyces as a single cell structure with the fastest graviresponses known so far, and the fruit bodies of the basidiomycetes Coprinus and Flammulina as highly complex structures with the ability to generate positional information and cell signalling in the context of negative gravitropism.

FLOW IN A CONTRACTILE TUBE AS A MODEL FOR PLASMODIAL STREAMING

Analytic solutions are obtained for two versions of the creeping-flow problem for Navier-Stokes fluid in an elastically deformable tube, driven by oscillatory inhomogeneous tension in the tube. In version I, the tube possesses dilatational elastic stiffness and solutions are obtained by Stokes's stream function. The amplitudes of radial oscillations, and of the applied force needed to maintain constant tube length, are enhanced by Marangoni effects arising from flow-induced surface stresses, but are still much smaller than observed in strands of the slime-mould Physarum polycephalum because of the low frequency of oscillation (≃ 0.01 Hz). Low-frequency radial motions of the surface can be obtained if the surface tube displays shear viscosity and the period of oscillation is comparable with the shear relaxation time. Solutions -are found in the low-frequency limit (version II) where the bulk fluid is in hydrostatic equilibrium

Regulation of actin polymerization by non-polymerizable actin-like proteins.

Three functionally distinct actin-capping proteins from the slime mould Physarum are structurally closely related to actin itself. In Physarum, actin polymerization is regulated by a set of non-polymerizable actin-like proteins. It remains to be established whether these proteins and actin are each encoded by separate genes.

Map and function ofgadmutations inPhysarum polycephalum

SUMMARYAmoebae and plasmodia are alternate vegetative forms in the life cycle of the acellular slime mouldPhysarum polycephalum. Haploid amoebae carrying heterothallic alleles of thematA(ormt) locus ordinarily form plasmodia only by crossing, but occasionally give rise to mutants that form plasmodia by selfing as well as by crossing. Twelve independently isolated mutants of this type have been studied. Eight carry mutations (termedgador greater asexual differentiation mutations) within approximately 0·2 map units ofmatA. Another mutation (gad-12) is linked neither tomatAnor to any of 9 other markers tested. The remaining three mutations are linked tomatAand map as follows:matA–0·5 units –gad-4–4 units –gad-6– 8 units –gad-11. One mutation,gad-11, has been tested in strains carrying each of the fivematAalleles (matAl, 2, 3, 4, andh) available in a common genetic background; the mutation is expressed with all five alleles. The mutationnpfF1(formerlyaptA1), which was isolated as a suppressor of selfing in Colonia (matAh) amoebae, suppresses the action of each of the 12gadmutations. The similarly isolated mutationnpfA1is also epistatic to eight of the mutations, but permits selfing withgad-5, 6, 12and13. For double mutant strains containinggad-12andgad-1, 2, 4, 6or11, the selfing behaviour of each double mutant differs from that of either single mutant. Mixtures ofgad−npfF1withgad+npf+amoebae readily form plasmodia, a result suggesting thatgadmutations are dominant or semi-dominant. We conclude that the commitment of a cell to differentiate into a plasmodium is under the control of a complex group of genes linked tomatA.

FACTS AND MECHANISMS: A COMPARATIVE SURVEY

FACTS AND MECHANISMS: A COMPARATIVE SURVEY