Abstract

For billions of years, photosynthetic microbes have evolved under the variable exposure to sunlight in diverse ecosystems and microhabitats all over our planet. Their abilities to dynamically respond to alterations of the luminous intensity, including phototaxis, surface association and diurnal cell cycles, are pivotal for their survival. If these strategies fail in the absence of light, the microbes can still sustain essential metabolic functionalities and motility by switching their energy production from photosynthesis to oxygen respiration. For suspensions of motile C. reinhardtii cells above a critical density, we demonstrate that this switch reversibly controls collective microbial aggregation. Aerobic respiration dominates over photosynthesis in conditions of low light, which causes the microbial motility to sensitively depend on the local availability of oxygen. For dense microbial populations in self-generated oxygen gradients, microfluidic experiments and continuum theory based on a reaction–diffusion mechanism show that oxygen-regulated motility enables the collective emergence of highly localized regions of high and low cell densities.

Highlights

  • Photosynthesis is a fundamental process of life that converts light into chemical energy [1]

  • For suspensions of motile C. reinhardtii cells above a critical density, we demonstrate that this switch reversibly controls collective microbial aggregation

  • Aerobic respiration dominates over photosynthesis in conditions of low light, which causes the microbial motility to sensitively depend on the local availability of oxygen

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Summary

Introduction

Photosynthesis is a fundamental process of life that converts light into chemical energy [1]. It is ubiquitous in highly diverse groups of species, ranging from higher level plants to prokaryotic cyanobacteria [2] and eukaryotic microalgae [3] These unicellular photosynthetic microbes inhabit almost any ecosystem on our planet and are dispersed to heterogeneous microhabitats. Photosynthetic microbes can still survive and produce energy through aerobic respiration, allowing them to produce ATP by the consumption of oxygen [16] This consumption can result in self-generated dark anoxia [17,18], where the cell is deprived of both light and oxygen. The appearance as well as the dynamics of aggregation are governed by the light intensity and wavelength as control parameters, providing a direct link between the activity of the photosynthetic machinery, microbial motility and large-scale self-organization

Aggregation of photosynthetic microbes at low light intensity
Inhibition of photosynthesis regulates microbial motility and aggregation
Statistical analysis of the microbial motility in dense suspensions
Effect of the oxygen concentration field and continuum modelling
Discussion
Cell cultivation
Experimental set-up
Light conditions
Data recording and cell tracking
Chlorophyll absorbance
Chlorophyll auto-fluorescence
Findings
Continuum model for cell aggregation
Full Text
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