A unicellular relative of animals generates an epithelium-like cell layer by actomyosin-dependent cellularization
Preprint posted on February 28, 2019 https://www.biorxiv.org/content/10.1101/563726v1
(Transiently) Comfortable in its own “skin”: formation of epithelium-like multicellular structures in a unicellular organism through conserved actomyosin-dependent mechanisms.Paul Gerald L. Sanchez and Stefano Vianello
In multicellular organisms, cells arrange over time and space to give rise to tissues with distinct architectures and functional properties. Cells will arrange themselves as ordered arrays in epithelial tissues, they will be loose and sparse in connective tissues, they will give rise to even more distinctive architectures in muscle and nervous tissues. Of all these forms of organisations however, epithelia seem to hold a special place in biology. During early embryonic development of mammalian species, it is indeed as an epithelium that cells first arrange themselves when forming the blastocyst. It is still an epithelium that acts as the substrate of gastrulation in chicken, mouse, and humans. It is again to an epithelium that cells apparently default to when even just seeded within a matrix. Epithelia can fold, form sheets and tubes, and they can support morphogenesis. Epithelia have a barrier function and a polarity: they compartmentalise space and they can distinguish and generate differences between these compartments.
Motivating the work highlighted by this preLight, epithelia have been suggested to be the first form of multicellular organisation to arise during evolution. While their ubiquitous presence across all animals clearly makes them a characteristic feature of this group, the discovery of polarized animal-like epithelia in social amoebae raised the possibility that these structures might even pre-date animals, and as such reflect an even more ancestral cellular programme. Yet, the evolutionary branches separating animals from slime moulds are also populated by unicellular life forms: epithelial organisation might thus just be the result of convergent independent evolution of epithelial-like organisation from a non epithelial ancestor.
The authors here investigate an intermediate branch of the evolutionary space separating animals from slime-moulds (i.e. the ichthyosporeans branch), and beautifully describe here too an epithelial-like life stage. Even more interestingly, the cellularization process giving rise to such epithelium occurs via animal-like mechanisms, strengthening evolutionary models that see epithelial structures as a basal characteristic of not only animals but of all unikonts.
The authors previously found that the single-cell ichthyosporean Sphaeroforma arctica transits through a multicellular stage [Ondracka et al, 2018]. They find that this stage displays features typical of an epithelium (Figure A). Such a transient epithelial-like structure originates by cellularization of a coenocyte, a shared multinucleated cytoplasm generated by rounds of cell division without cytokinesis.
By using a combination of membrane and cytoskeleton marking, live imaging, and RNA sequencing of cultured organisms, the authors find that this cellularization process occurs through animal-like mechanisms. Specifically, they find that it occurs through the stepwise assembly and deployment of a cortical network of actin and myosin (Figure B):
- nucleation of actin at the cortex,
- formation of filaments,
- myosin-dependent crosslinking,
- membrane invagination to compartmentalise the underlying cytoplasm
Concomitantly, the organism undergoes a drastic transcriptional shift to genes involved in cell-cell and cell-matrix interactions, as well as in cytoskeletal components. Morphologically, and mechanistically, the process is conserved with what is seen in animal models of cellularization (e.g. in Drosophila); yet also reveals ichthyosporean-specific features such as the role of transcriptional changes.
This study identifies animal-like mechanisms of epithelial formation in yet another branch of the evolutionary tree. That is, in addition to that of the slime moulds, where the identification of catenin-based epithelial structures prompted hypothesis of a pre-animal emergence of epithelial programmes [Dickinson et al, 2012]. The S. arctica studied here (ichthyosporean) belongs to a lineage even closer to the animal branchpoint. While previous descriptions in slime moulds could have just been the result of independent evolution in slime moulds and animals, finding conserved molecular mechanisms in ichthyosporeans strengthens the hypothesis of common descent from an ancestor that did already have epithelial-like life stages. Such epithelial programmes would have been maintained in the animal, ichthyosporean, and slime-mould lineages, and lost in the many exclusively unicellular life-forms observed in between these branches.
We particularly appreciated how elegant the experimental design is, considering the limited tools available when studying an emerging model system. The authors maximized the amount of biological insight obtained from membrane/cytoskeleton labelling and targeted small molecule inhibition of different steps of cytoskeletal organisation. Of notice is also the RNA sequencing data collection, aligned to a genome re-assembled by the authors themselves!
- You seem always very careful about talking about “epithelium-like” tissue, and not “epithelium”. Could you elaborate on this distinction? What features do you see as still missing to define this as an epithelium?
- Could you elaborate on the differences you see when comparing to Drosophila? What do you think these reveal about the requirements and evolutionary strategies of cellularization?
- What tools would you like to have available to prove the actual involvement of catenins? And to test the function of the epithelium?
- Animal epithelia rarely form through cellularization of a coenocyte. Could you elaborate on that? How widespread is epithelialisation (rather than cellularization) outside of the animal group?
- Kinesin 2 is one of the few microtubule motors that also undergoes upregulation upon cellularization. Do you have any ideas on whether it contributes to membrane folding too?
- Coenocyte sizes seem to vary during growth. Do bigger coenocytes take shorter time to burst after the flip event, explaining the observed variability? Do they release more/bigger cells?
A comprehensive review on epithelia and their function:
- Rodriguez-Boulan, Enrique, and Ian G. Macara. “Organization and execution of the epithelial polarity programme.” Nature Reviews Molecular Cell Biology 15.4 (2014): 225.
Overview of the current evolutionary considerations on the origin of epithelia:
- Dickinson, Daniel J., W. James Nelson, and William I. Weis. “An epithelial tissue in Dictyostelium challenges the traditional origin of metazoan multicellularity.” Bioessays 34.10 (2012): 833-840.
A previous paper by the same lab as this preprint:
- Ondracka, Andrej, Omaya Dudin, and Iñaki Ruiz-Trillo. “Decoupling of Nuclear Division Cycles and Cell Size during the Coenocytic Growth of the Ichthyosporean Sphaeroforma arctica.” Current Biology 28.12 (2018): 1964-1969.
An article on the root as a polarized epithelium in plants:
- Maizel, Alexis. “Plant Biology: The Making of an Epithelium.” Current Biology 28.17 (2018): R931-951.
Posted on: 5th April 2019Read preprint
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