Research Article: A lumped parameter model of endoplasm flow in Physarum polycephalum explains migration and polarization-induced asymmetry during the onset of locomotion

Date Published: April 23, 2019

Publisher: Public Library of Science

Author(s): Christina Oettmeier, Hans-Günther Döbereiner, David Umulis.

http://doi.org/10.1371/journal.pone.0215622

Abstract

The plasmodial slime mold Physarum polycephalum exhibits strong, periodic flow of cytoplasm through the veins of its network. In the special case of mesoplasmodia, a newly described starvation-induced, shape-constant morphotype, this periodic endoplasm streaming is the basis of locomotion. Furthermore, we presume that cytoplasm flow is also involved in signal transmission and signal processing. Mesoplasmodia motility resembles amoeboid locomotion. In contrast to other amoebae, however, mesoplasmodia move without extending pseudopods and retain a coherent, fan-shaped morphology throughout their steady locomotion. Attaining sizes of up to 2 mm2, mesoplasmodia are also much bigger than other amoebae. We characterize this particular type of locomotion and identify patterns of movement. By using the analogy between pulsatile fluid flow through a network of elastic tubes and electrical circuits, we build a lumped model that explains observed fluid flow patterns. Essentially, the mesoplasmodium acts as a low-pass filter, permitting only low-frequency oscillations to propagate from back to front. This frequency selection serves to optimize flow and reduces power dissipation. Furthermore, we introduce a distributed element into the lumped model to explain cell polarization during the onset of chemotaxis: Biochemical cues (internal or external) lead to a local softening of the actin cortex, which in turn causes an increased flow of cytoplasm into that area and, thus, a net forward movement. We conclude that the internal actin-enclosed vein network gives the slime mold a high measure of control over fluid transport, especially by softening or hardening, which in turn leads to polarization and net movement.

Partial Text

The acellular, multi-nucleated slime mold P. polycephalum can take on many shapes and sizes, depending on the mode of cultivation and various environmental parameters (e.g. nutrients, temperature, light). Typically, the slime mold forms large extended networks, characterized by a regular and vigorous flow of endoplasm (called shuttle streaming) through its veins. When placed in liquid shaking culture, shear forces tear the macroplasmodium apart and quasi-spherical, floating microplasmodia with diameters of a few hundred micrometers are produced. Regardless of shape and size, rhythmic oscillations of the cell periphery and the resulting flow of endoplasm are a characteristic feature of P. polycephalum. Cytoplasmic flow serves several purposes. First, it distributes nutrients, oxygen and cellular components throughout the cell body. Second, it is crucial for cell motility. In this work, we show that cytoplasmic flow is also a means of signal processing and distribution.

Recently, P. polycephalum has become the focus of research on the fundamental mechanisms of cognition and decision-making (for a review, see [42]). The question of how the slime mold processes information in the absence of a nervous system is still unanswered. For its apparent reminiscential capabilities, a model based on memristors has been put forward [43]. The selection of frequencies is an example of hydrodynamic information processing. We speculate that cytoplasm flow is a means for the slime mold to transmit information throughout its cell body, and to process this information so that an observable change in behavior takes place. The input signal, e.g., a chemotactic stimulus, could cause a change in the oscillation pattern which is then transmitted through the entire organism. On the other hand, based on internal cues (e.g. the cell cycle or nutritional status), the slime mold could control, globally or locally, the radius and stiffness of its veins via the actin cytoskeleton. This would change the fluidic properties (resistance, capacitance), and thus the flow. The internal flow pattern, in turn, changes the morphology and behavior of the organism.

 

Source:

http://doi.org/10.1371/journal.pone.0215622

 

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