Theoretical and Experimental Dissection of Gravity-Dependent Mechanical Orientation in Gravitactic Microorganisms

Abstract

Mechanisms of gravitactic behaviors of aquatic microorganisms were investigated in terms of their mechanical basis of gravity-dependent orientation. Two mechanical mechanisms have been considered as possible sources of the orientation torque generated on the inert body. One results from the differential density within an organism (the gravity-buoyancy model) and the other from the geometrical asymmetry of an organism (the drag-gravity model). We first introduced a simple theory that distinguishes between these models by measuring sedimentation of immobilized organisms in a medium of higher density than that of the organisms. Ni2+-immobilized cells of Paramecium caudatum oriented downwards while floating upwards in the Percoll-containing hyper-density medium but oriented upwards while sinking in the hypo-density control medium. This means that the orientation of Paramecium is mechanically biased by the torque generated mainly due to the anterior location of the reaction center of hydrodynamic stress relative to those of buoyancy and gravity; thus the torque results from the geometrical fore-aft asymmetry and is described by the drag-gravity model. The same mechanical property was demonstrated in gastrula larvae of the sea urchin by observing the orientation during sedimentation of the KCN-immobilized larvae in media of different density: like the paramecia, the gastrulae oriented upwards in hypo-density medium and downwards in hyper-density medium. Immobilized pluteus larvae, however, oriented upwards regardless of the density of the medium. This indicates that the orientation of the pluteus is biased by the torque generated mainly due to the posterior location of the reaction center of gravity relative to those of buoyancy and hydrodynamic stress; thus the torque results from the fore-aft asymmetry of the density distribution and is described by the gravity-buoyancy model. These observations indicate that, during development, sea urchin larvae change the mechanical mechanism for the gravitactic orientation. Evidence presented in the present paper demonstrates a definite relationship between the morphology and the gravitactic behavior of microorganisms.

Behavioral responses of invertebrate larvae to water column cues

“…Despite the absence of a statocyst-like structure, our results support early observations that larval urchins have mechanoreception ability and are capable of adjusting their propulsive behaviors accordingly [59,84,85]. Further work on ciliary motion control [86,87] and gene expression (e.g., orthologs of vertebrate mechanosensory genes, e.g.…”

“…Ontogenetic changes in larval shape may play a role in the larval ability to maintain an upright orientation, and hence, stability in flow. Older, heavier larval urchins have increased skeleton weight as ballast which could enhance stability [78,59]. However, the additions of arms and increased size could also compromise stability by affecting the separation distance between the center of gravity and center of buoyancy [78].…”

“…through their development. Plutei are characterized by fore-aft asymmetry [57] and in some species, a distinct density differential in which mass is concentrated in the posterior [59].…”

“…Fore-aft asymmetry coupled with negative buoyancy produces a gravity-induced hydrodynamic torque [60], while a differential density produces a torque proportional to the distance between the larva's centre of gravity and centre of buoyancy [59,60]. Both mechanisms likely play a role in observed reorientation of larvae in flow, but previous experimental evidence suggests that urchin larvae primarily rely on non-homogeneous density, or "bottom heaviness" to reorient [59]. Larval-turbulence interaction is therefore a combination of both active behavioral choices such as those of barnacle cyprids and larval oysters and passive biomechanical limitations imposed by the pluteus morphologies of larval sand dollars and sea urchins.…”

Responses to Hypergravity in Proliferation of Paramecium tetraurelia

“…P av would increase when there is an increase in the fraction of cells orienting upwards. Mogami et al (2001) demonstrated that the gravitactic orientation of Paramecium is mechanically biased by the torque generated mainly due to the fore-aft asymmetry of the cell body. The upward-orienting torque increases in proportion to gravity, so that the fraction of cells orienting upwards, i.e., F(φ) for a large φ, increases under hypergravity, and decreases under microgravity.…”