Complex history of cell mobility

Imagine any mode of locomotion, no matter how eccentric: it is likely that the cells already use it. Not only do most of them move independently, but the mechanisms they implement are full of ingenuity. In mammals, for example, spermatozoa are propelled by their flagellum, and certain white blood cells are extracted from the blood capillary by detaching the cells from the wall using processes called “pseudopodia.” During embryogenesis, cells migrate, making their way between their sisters. Even fixed cells cause relative movement of the environment, such as bronchial hair cells expelling impurities, or fallopian tube cells causing egg migration. In a word, everything moves, including in the unicellular world. In fresh or marine waters, eukaryotic cells (equipped with a nucleus) swim with the help of cilia or flagella, such as euglena, dinoflagellates or ciliates. Others use cytoplasmic extensions, such as the large prolegs of amoebas or the narrow reticulate projections of the foraminiferal membrane. Don’t forget about the drop (physarum polycephalum)a myxomycete fungus which at one stage of its cycle becomes a multinucleated giant cell whose very special crawl is based on the pulsation of fluid.

In 2020, Kenichi Wakabayashi of the Tokyo Institute of Technology in Japan and colleagues identified at least 18 ways cells move, including about ten in eukaryotes. For evolutionary biologists, this diversity raises questions: how and when did different modes of cellular locomotion appear on the tree of life?

In particular, in eukaryotic cells, experts agree that locomotion is based mainly on two categories of mechanisms: a flagellum for swimming and deformation of the actin network, one of the key components of the cytoskeleton, for crawling. Did these two categories exist even before the appearance of eukaryotes? To find out, Lillian Fritz-Leylin of the University of Massachusetts Amherst, USA, studied the knowledge accumulated in recent years. If everything is clear for the flagellum, then the situation is more complicated with actin …

Flagellum and cilium, the same fight

First of all, remember that the eukaryotic flagellum has nothing to do with the bacterial flagellum. Consisting of a single filament formed by an assembly of the monomer, flagellin, the bacterial flagellum is a hollow, coiled tube propelled and screwed in by a proton engine. The eukaryotic flagellum consists of nine doublets of microtubules surrounding a central doublet. Microtubules are polymers of another protein, tubulin. The beating of the flagellum occurs due to the movement of microtubules, which slide relative to each other thanks to molecular motors called “dyneins”. Therefore, we must be careful with terminology, especially since, on the contrary, eukaryotic cilia and flagella have a very similar structure.

moth Noctiluca scintillans flagellum

Noctilucus Noctiluca sparklingbioluminescent marine plankton, also known as sea sparkle, is another eukaryote and moves with the help of a flagellum.

© Rattya Thongdumhyu/Shutterstock

From the middle of the twentiethe century, studying them using electron microscopy, biologists were struck by their structural identity, which testified to a single evolutionary origin. This still needed to be shown … Then molecular biology appeared, which made it possible to study in detail the genes encoding tubulin. Thus, throughout the eukaryotic world, there appeared to be a great identity of these genes, a sign that they were descended from the same ancestral gene. But the evolutionary history of flagella is still unresolved because microtubules are used for more than just motility. They are the main components of the eukaryotic cytoskeleton, which make up the entire cytoplasm. All eukaryotic cells, flagellated or not, carry the tubulin gene, so the phylogeny of these genes is not useful for accessing the phylogeny of flagella.

However, auxiliary proteins necessary for the functioning of the flagellum have been described for about twenty years. And they exist only in species with flagella or cilia. From an evolutionary point of view, there are two possibilities: either the genes encoding these proteins are inherited from a common ancestor, conserved in lines with flagella or cilia, and lost in lines without them; or they are transferred by horizontal transfer from one line to another. However, since the phylogenetic trees of these genes are similar to those of the species, this latter hypothesis is untenable: therefore, eukaryotic flagella and cilia do indeed share a common ancestor.

What did he look like? Because neither bacteria nor archaea (two other major domains of life with eukaryotes) have known genes homologous to flagellate-specific genes, we cannot go beyond the last common ancestor of eukaryotes. Without a group outside of eukaryotes carrying such genes, further research is not possible.

At sources of creep

The evolutionary history of cell creep is much more complex. The flagellum is a structure external to the cell: when it beats, the cell does not change shape. On the contrary, creeping movements depend on a network of actin filaments within the cytoplasm and lead to the deformation of a large part of the cell – even the whole of it. Lamellipodia, treadmills, filopodia… the types of mobility described seem so different that a single evolutionary origin seems unlikely. As for the flagellum, to move forward, it is necessary to find auxiliary proteins associated with the actin network and designed exclusively for motility.

pseudopodia lamellopodia filopodia

This is what Lilian Fritz-Leylin dedicated herself to, having carefully studied the Arp2/3 protein complex. This complex triggers the budding of actin filaments on existing filaments and is involved in the formation of the actin network of lamellipodia. The phylogeny of the genes encoding Arp2/3 does not in itself provide any indication of the history of movement because this complex is also involved in endocytosis, the cellular process of ingestion and digestion. But Lillian Fritz-Leylin puts forward two regulators of this complex – SCAR / WAVE and WASP: in 2017, looking through eukaryotic genomes with colleagues, she noticed that only eukaryotes representing the genes encoding these two proteins switch to pseudopodia. Thus, this duo will exclusively interfere with cellular motility by activating the formation of an extensive actin network – an argument in favor of the sole origin of this motility mechanism. However, there are other systems as well. And convergences are also beginning to be described. Thus, in nematode worms, spermatozoa have lost their flagellum and are moved by amoeboid movements driven by the polymerization dynamics of a protein other than actin.

Thus, the evolutionary history of cellular mobility is far from being deciphered. This requires more exhaustive research – the various lines have not been studied – and, above all, more special genes that allow us to answer questions. Will we ever know the answers?

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