Arp2/3 complex-mediated actin assembly drives microtubule-independent motility and phagocytosis in the evolutionarily divergent amoeba Naegleria
Posted on: 18 May 2020
Preprint posted on 15 May 2020
Article now published in Journal of Cell Biology at http://dx.doi.org/10.1083/jcb.202007158
Categories: cell biology, evolutionary biology, microbiology, zoology
Context
We all know actin is important – but why study it in brain-eating amoebae? Velle and Fritz-Laylin provide more than a few compelling reasons to do so in their elegant new preprint.
The beautiful textbook drawings of cells that many of us grew up with are based on decades of careful cell biology – research that has, for historical or pragmatic reasons, largely been limited to a very small number of animal and fungal model systems. Strange as it might seem, humans and yeast, both opisthokonts, are close cousins occupying a tiny fraction of the ever-expanding tree of life [1].
At the same time, the fundamental building blocks of eukaryotic cellular architecture – such as the actin, tubulin and ESCRTIII protein families – are over 2 billion years old, and were in fact directly inherited by the first eukaryotes from their archaeal ancestors [2]. Despite being finely tuned machines that exhibit an impressive degree of sequence conservation, these key proteins have had (literal) aeons to tweak interactions and modifications, acquire new binding partners, and to duplicate and diversify many times over [3]. It is becoming increasingly clear that our understanding of cytoskeletal function in complex processes such as cell migration and phagocytosis, and of their evolutionary origins [4], will remain incomplete until we do a better job of studying the cell biology of divergent branches of the species tree (Figure 1).
Enter the heterolobosean Naegleria gruberi and it’s brain-eating cousin Naegleria fowleri. Devoid of interphase cytoplasmic microtubules in their crawling amoeboid state, and possessed of a diverse complement of actins and actin-associated regulators, these little-studied cells provide excellent systems for the investigation of actin-driven motility and phagocytosis.
Key take-home
Velle and Fritz-Laylin combine advanced light and electron microscopy with an extensive toolkit of probes and small molecules used to label and perturb actin (it helps that Naegleria actin is 85% identical to mammalian actin) for their experiments.
They show that Naegleria assembles Arp2/3-dependent actin structures, including lamellae (Figure 2); if Arp2/3 activity is compromised, the cells can no longer migrate or phagocytose effectively; without Arp2/3, cellular actin is reorganised into filopodia. These actin network properties are shared with other amoeboid cell types across the tree, supporting the notion of a deeply conserved, ancient origin for actin-powered crawling motility.
Collectively, the authors’ systematic experiments establish Naegleria as a great new system for studying the emergent cellular behaviour of a complex actin cytoskeleton – without the confounding presence of microtubules.
Some questions for the authors
An obvious one: would the authors be willing to speculate on the possible nature of the hollow actin spheres?
Given that the regulatory networks involved in both phagocytosis and motility intersect with various signaling and trafficking pathways, it has been difficult to infer the composition of a “minimal” phagocytic or motility system, and equally challenging to reconstruct the likely actin machinery of early eukaryotes [4]. This in turn has major implications for models of eukaryogenesis. Could you comment on how your findings might influence the status quo?
It appears that Naegleria also presents a fantastic system for investigating – and perturbing – the control of nuclear division and spindle dynamics in mitosis without the confounding effects of disrupting interphase microtubules! Any thoughts?
Further reading
Don’t miss the beautiful movies and images in the first author’s tweetorial!
[1] Burki, F., Roger, A. J., Brown, M. W. & Simpson, A. G. B. The New Tree of Eukaryotes. Trends in Ecology and Evolution 35, 43–55 (2020).
[2] Eme, L., Spang, A., Lombard, J., Stairs, C. W. & Ettema, T. J. G. Archaea and the origin of eukaryotes. Nature Reviews Microbiology 15, 711–723 (2017).
[3] Stoddard, P. R., Williams, T. A., Garner, E. & Baum, B. Evolution of polymer formation within the actin superfamily. Molecular Biology of the Cell 28, 2461–2469 (2017).
[4] Burns, J. A., Pittis, A. A. & Kim, E. Gene-based predictive models of trophic modes suggest Asgard archaea are not phagocytotic. Nat. Ecol. Evol. 2, 697–704 (2018).
doi: https://doi.org/10.1242/prelights.20789
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