Dictyostelium discoideum chemotaxis is altered by hypoxia to orient streaming toward higher oxygen level independently of aerotaxis.

Abstract

BackgroundDictyostelium discoideum (Dd) exhibits a unique life cycle marked by its transition from single-cell amoeboid movement to multicellular development in response to environmental stimuli. While its chemotactic response to cyclic adenosine monophosphate (cAMP) has been extensively studied, experiments are usually carried out in a high oxygen environment (21% O2, also called normoxia) that might not reflect the natural condition for a soil amoeba as hypoxia is common underground. Our recent research has unveiled a novel phenomenon termed aerotaxis, wherein Dd cells migrate towards oxygen-rich environments under low oxygen (hypoxia). ResultsWe tested Dd response when submitted to two different stress sources: starvation and hypoxia. While both stresses induce a motile response, namely chemotaxis and aerotaxis, we were able to decoupled both type of responses to explore potential shared mechanisms. Importantly, aerotaxis appears to be operated independently of known chemotactic pathways, demonstrating unique signaling pathways and cellular responses. Aerotaxis contributes to Dd developmental processes by letting cells escape from acute hypoxia. Even though chemotactic response can occur at less than 2% O2, it does not lead to well organized or stable streaming. Furthermore, in an oxygen gradient, aggregation center for chemotactic response appears preferentially at higher O2 level. RT-qPCR analysis show that hypoxia only slightly reduces the expression of genes required for chemotactic response, suggesting that the bias toward high O2 might occur at another level. Reoxygenation of cells that have been starved in hypoxic condition for 18h allow rapid aggregation but require de novo protein synthesis. ConclusionAerotaxis and chemotaxis mechanisms do not interact directly. However, when cells are exposed to both hypoxia and starvation, both mechanisms can be combined to direct the migration of cells toward place with higher oxygen level. As hypoxia is frequent in the soil where Dd usually grow, formation of aggregation centers at, or close to the soil surface, where oxygen is abundant, will be advantageous. Low O2 level does not preclude cells to participate to streaming but seems to reduce or delay their ability to produce stable aggregation centers, resulting into bias favoring centers that form at higher oxygen level.