Enhanced transport of nutrients powered by microscale flows of the self-spinning dinoflagellate Symbiodinium sp.

Zheng Zhu,Quan-Xing Liu

doi:10.1242/jeb.197947

Abstract

ABSTRACTThe metabolism of a living organism (e.g. bacteria, algae, zooplankton) requires a continuous uptake of nutrients from the surrounding environment. However, within local spatial scales, nutrients are quickly used up under dense concentrations of organisms. Here, we report that self-spinning dinoflagellates Symbiodinium sp. (clade E) generate a microscale flow that mitigates competition and enhances the uptake of nutrients from the surrounding environment. Our experimental and theoretical results reveal that this incessant active behavior enhances transport by approximately 80-fold when compared with Brownian motion in living fluids. We found that the tracer ensemble probability density function for displacement is time-dependent, but consists of a Gaussian core and robust exponential tails (so-called non-Gaussian diffusion). This can be explained by interactions of far-field Brownian motions and a near-field entrainment effect along with microscale flows. The contribution of exponential tails sharply increases with algal density, and saturates at a critical density, implying a trade-off between aggregated benefit and negative competition for the spatially self-organized cells. Our work thus shows that active motion and migration of aquatic algae play key roles in diffusive transport and should be included in theoretical and numerical models of physical and biogeochemical ecosystems.

Highlights

Motile microorganisms display fascinating spatial patterns and collective behaviors, evoking the focus of attention of biologists, biophysicists and ecologists over the past three decades (Bartumeus et al, 2016; Katija, 2012; Katija et al, 2015; Woodson and McManus, 2007)
Density-dependent turbulence and active transport Symbiodinium sp. are unicellular with a body size of d≈12±3 μm in diameter and possess two dissimilar flagella arising from the ventral side that are responsible for a rotational speed of ω≈25±5 rad s−1, according to our laboratory experimental measurements
The trajectories of particles influenced by microorganisms can be divided into three types: intrinsic Brownian motion, circle-like behavior induced by hydrodynamics and entrainment effects caused by collision with active swimmers

Summary

Introduction

Motile microorganisms display fascinating spatial patterns and collective behaviors, evoking the focus of attention of biologists, biophysicists and ecologists over the past three decades (Bartumeus et al, 2016; Katija, 2012; Katija et al, 2015; Woodson and McManus, 2007). Numerous experimental observations and theoretical models have reported that the active motions of microorganisms have significant effects on their search strategies for resources such as bacteria and algal cells. One may hypothesize that the enhanced diffusion should relate to anomalous nonGaussian behavior, but the underpinning mechanisms remain largely elusive from experimental points of view (Bechinger et al, 2016; Höfling and Franosch, 2013). A better biological model still remains to be developed to unravel the underlying mechanisms

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