Abstract
Using a self-generated hypoxic assay, we show that the amoeba Dictyostelium discoideum displays a remarkable collective aerotactic behavior. When a cell colony is covered, cells quickly consume the available oxygen (O2) and form a dense ring moving outwards at constant speed and density. To decipher this collective process, we combined two technological developments: porphyrin-based O2 -sensing films and microfluidic O2 gradient generators. We showed that Dictyostelium cells exhibit aerotactic and aerokinetic response in a low range of O2 concentration indicative of a very efficient detection mechanism. Cell behaviors under self-generated or imposed O2 gradients were modeled using an in silico cellular Potts model built on experimental observations. This computational model was complemented with a parsimonious 'Go or Grow' partial differential equation (PDE) model. In both models, we found that the collective migration of a dense ring can be explained by the interplay between cell division and the modulation of aerotaxis.
Highlights
Oxygen is the main electron acceptor for aerobic organism to allow efficient ATP synthesis
In order to complement the methodology of the cellular Potts model, we developed a mean-field approximation of the latter: the cell density is subject to a reaction-advection-diffusion partial differential equation (PDE): q 1⁄4 Dr Á ðrÞ À r Á ðaðC; rCÞÞ þ rðCÞ
Our results demonstrate the ability of Dd cells to respond to hypoxia through both aerotactic and aerokinetic responses
Summary
Oxygen is the main electron acceptor for aerobic organism to allow efficient ATP synthesis. This high-energy metabolic pathway has contributed to the emergence and diversification of multicellular organism (Chen et al, 2015). While high O2 availability in the environment seems a given, its rapid local consumption can generate spatial and temporal gradients in many places, including within multicellular organism. Oxygen level and gradients are increasingly recognized as a central parameter in various physiopathological processes (Tonon et al, 2019), cancer and development. At low O2 levels, cells accumulate HIFa leading to the expression of genes that support cell functions appropriate to hypoxia (Pugh and Ratcliffe, 2017)
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