Aerotaxis in the closest relatives of animals

  • Kirkegaard J
  • Bouillant A
  • Marron A
  • et al.
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Abstract

As the closest unicellular relatives of animals, choanoflagellates serve as useful model organisms for understanding the evolution of animal multicellularity. An important factor in animal evolution was the increasing ocean oxygen levels in the Precambrian, which are thought to have influenced the emergence of complex multicellular life. As a first step in addressing these conditions, we study here the response of the colony-forming choanoflagellate Salpingoeca rosetta to oxygen gradients. Using a microfluidic device that allows spatio-temporal variations in oxygen concentrations, we report the discovery that S. rosetta displays positive aerotaxis. Analysis of the spatial population distributions provides evidence for logarithmic sensing of oxygen, which enhances sensing in low oxygen neighborhoods. Analysis of search strategy models on the experimental colony trajectories finds that choanoflagellate aerotaxis is consistent with stochastic navigation, the statistics of which are captured using an effective continuous version based on classical run-and-tumble chemotaxis.Most animals are made up of millions of cells, yet all animals evolved from ancestors that spent their whole lives as single cells. Today the closest single-celled relatives of animals are a group of aquatic organisms called choanoflagellates. Certain species of choanoflagellates can also form swimming colonies. This kind of multicellularity might resemble that seen in the earliest of animals. As such, studies into modern-day choanoflagellates can give insights into how the first animals to evolve might have behaved.Many organisms can find their way towards favorable areas using different strategies. For instance, bacteria can bias their tumbling to gradually swim towards food, and algae can turn and move directly towards light. While choanoflagellates require oxygen, it was not known if they could also actively navigate towards it, or any other resource.Now, Kirkegaard et al. find that the choanoflagellate Salpingoeca rosetta can indeed navigate towards oxygen – an ability called aerotaxis. This was true for both individual cells and for colonies made up of many cells. This discovery suggests that the transition from living as a single cell to living as a simple multicellular organism could still have allowed the earliest animals to seek out and move towards resource-rich areas.Aerotaxis requires cells to both sense oxygen and react appropriately to changes in its concentration. Kirkegaard et al. watched choanoflagellate colonies swimming under controlled conditions and varied the oxygen concentration in the water over time. These experiments revealed that the colonies navigate based on the logarithm of the oxygen concentration, so that at low oxygen levels the cells were even more sensitive to small changes in oxygen concentration. This type of ‘logarithmic sensing’ is similar to how our ears sense sounds and our eyes sense light. Kirkegaard et al. went on to conclude that the colonies were not actively steering in the correct direction directly. Instead, the colonies appeared to choose directions at random and later decide whether such a turn was correct.It remains unclear whether the common ancestor of animals and choanoflagellates could also perform aerotaxis, and if so what mechanisms this involved. Further studies to compare aerotaxis and aerotaxis-related genes in simple animals and other single-celled relatives of animals would be needed to illuminate this. Future studies could also explore the maximum and minimum oxygen concentrations that choanoflagellates can detect, and how well they navigate at these upper and lower limits.

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Kirkegaard, J. B., Bouillant, A., Marron, A. O., Leptos, K. C., & Goldstein, R. E. (2016). Aerotaxis in the closest relatives of animals. ELife, 5. https://doi.org/10.7554/elife.18109

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