Rethinking the origin of multicellularity: Where do epithelia come from? (Comment on DOI 10.1002/bies.201100187)

Authors


Evolution happens slowly; and it also happens in major transitions. One of the earliest transitions involved the capture of a bacterium that became the mitochondrion of the eukaryotic cell. Another major transition resulted in multicellularity and the appearance of organisms with at least a few distinct cell types. Multicellularity has evolved repeatedly from independent unicellular lineages. In any multicellular body this requires coordinated developmental processes and controlled expression of cell type-specific genes. The primary building block providing for complex differentiation is the epithelium. Epithelia are sheet-like arrangements of “polarized” cells that have an apical surface with secretory vesicles. Furthermore, they use belt-like junctions for cell adhesion along their adjacent surfaces, and are attached to an extracellular matrix on their basal side (Fig. 1).

Figure 1.

Simplified scenario for the evolution of a polarized epithelium.

While all metazoans are composed of distinct cell types, until recently only the so-called “Eumetazoa” (i.e., the cnidarians and bilaterians) were considered to have an epithelium. However, molecular and physiological studies provide convincing evidence that functional epithelia may be traced back at least to some sponges, and therefore far outside the “Eumetazoa”. Thus, epithelia may be much older than previously thought. Who then invented them? And what is needed to build an epithelium?

Much of what we know so far about the evolution of multicellularity comes from a number of comparatively simple organisms such as Choanoflagellates. These single-celled protists are the closest living relatives of sponges, and have a surprisingly rich repertoire of cell adhesion molecules, with many members of gene families that the Metazoa also use. A new study by Dickinson et al. 1 and a hypothesis paper by the same authors in this issue of BioEssays 2 show that another group of simple organisms, the cellular slime molds or social amoebae, are equally informative for resolving the puzzle of when during evolution epithelia were invented. In fact, these studies seem to have pushed back the earliest evidence for the invention of epithelia by some 100 million years.

The group of dictyostelid social amoebae contains organisms such as Dictyostelium discoideum that hover between uni- and multicellularity. Dictyostelium starts its life as a unicellular amoeba, but when the amoebae run out of their bacterial food, they aggregate into a multicellular, motile slug. The slug forms a fruiting body with a stalk and a tip, which contains dispersal-ready spores. Advances in cell labeling, microscopy, and comparative genomics, as well as the results of decades of study of Dictyostelium, allowed Dickinson et al. to look at both the morphology of the multicellular fruiting body and the genes necessary to form epithelia. The researchers not only uncovered a bona fide polarized epithelium, capable of secreting extracellular matrix molecules; Dickinson et al. also identified β- and α-catenins as essential components of a hitherto poorly understood cell adhesion apparatus. The authors' main point is that the organizational principles of metazoan multicellularity may be more ancient than previously recognized. Another crucial observation in the work of Dickinson et al. is that the role of catenins in cell polarity appears to predate their involvement in the Wnt signaling cascade. This finding lays out a clear framework of the mechanisms utilized by the last common ancestor of metazoans to develop polarized epithelia. The article also contains interesting novel thoughts on the role of environmental conditions for the evolution of multicellularity.

While these studies certainly add a new dimension to our understanding of why and how epithelia evolved, they raise an even larger range of questions. What was the environmental context of this invention and major transition? Epithelia in metazoans function as both physical and chemical barriers that seal and control the ionic composition of the internal milieu; is this also true for Dictyostelium? What are the developmental processes that allow unicellular amoebae to differentiate into epithelial-like cells? How does catenin-based cell adhesion work in the absence of cadherins? What about cell adhesion to the extracellular matrix in Dictyostelium? Finally, have closely related protists such as the Ichthyosporea (Fig. 1) lost their multicellularity tool kit? Despite all those questions, it is obvious now that we have to look at very simple organisms if we want to elucidate some of the fundamental evolutionary transitions.

Ancillary