A dinoflagellate adaptive behavior model: response to internal biochemical cues

Abstract

In this study we built two models to simulate vertical movements of an individual dinoflagellate. In the models, we laid out the flows of the chemical substances inside the cell and their changes in response to such environmental changes as nitrate concentration and light intensity. One of the models is called the Clock-Driven Model, in which the cell moves only according to the clock time and exhibits a regular vertical diel movement. The other model, which we call the Decision-Making Model, contains a network to make decisions for the next move, based on the interactions among biochemicals inside the phytoplankter and its environment. In this model, the decision emerges from the results of a cell's internal biochemical fluxes controlled by the threshold setting. The simulation results of both models with different nutrient conditions were compared in terms of the cell's behavioral patterns and the amount of protein produced by the cell. The results indicated that balances among the biochemicals and their fluxes can play a significant role in the directional decisions made by dinoflagellates under some environmental nitrate conditions, and that irregularity in a cell's movements may be affected by nitrate availability. Also, the simulation results suggest that irregular migration produced to meet the predefined criteria for biochemical fluxes inside the cell can benefit the cell in terms of protein accumulation. We propose that the essence of a cell's adaptivity to the environment resides in the internal cellular condition represented here by threshold values associated with biochemical fluxes and their balances, and that it is important to consider an organism's internal condition when constructing an adaptive behavior model.

Introduction

Observational studies on single-cell phytoplankton demonstrate adaptive behaviors according to changes in the physical environment (Kamykowski, 1981a, Cullen and Horrigan, 1981, MacIntyre et al., 1997). Many phytoplankton are not mere passive particles carried by the turbulence or currents in the ocean, but move autonomously from the surface to the deeper section of the ocean to accommodate themselves to various environmental conditions (Jennings, 1976). Although phytoplankton do not have neurons, they function as though they have sense organs for light and gravity (Levandowsky and Kaneta, 1987). Their adaptivity, however, may come not only from a sensitivity to external cues but also from mechanical or perceived changes in their internal state by mechanisms that are poorly defined at present (Jones, 1993, Kamykowski, 1995). Since marine phytoplankton live by depending on photosynthesis and the nutrients in the ocean, their decision to swim up or sink/swim down should be associated with the relation between plankton’s internal condition and the outside physical state.

In this study we have focused on the behavior of planktonic algae called dinoflagellates, which typically are single-cell organisms that autonomously migrate in the ocean. They gain energy and carbon/hydrogen/oxygen through photosynthesis and absorb other necessary nutrients from the surrounding seawater. We built models for an individual dinoflagellate’s vertical swimming behavior and formulated these models to identify the key elements in its adaptation to the environment. Most individual-based models for plankton describe relationships between changes in the external environment and an organisms' behavior, but not the organism's internal state (Murdoch, 1992). We, however, here considered the fluxes and changes of its internal biochemicals which are influenced by changes in the external environment. To construct models, we translated the external environmental changes into a plankter’s internal changes, viewing its behavior as an emergent result of interacting processes inside the organism.