Highlight: Origins of Multicellularity Revealed by Single-Celled Amoebae

The transition from a unicellular to a multicellular lifestyle has occurred multiple times—most notably in the lineages leading to plants, animals, and fungi. How this transition is made, however, has remained a major question among biologists, and new evidence may come from an unlikely quarter: The study of single-celled amoebae. In plants, animals, and fungi, dividing cells remain attached to each other, forming multicellular organisms. In many protist lineages, however, multicellularity involves the coming together of dispersed cells under starvation conditions to form a structure known as a fruiting body, which produces airborne spores (fig. 1). These spores are the organism’s way of playing the evolutionary lottery; the hope is that some of these spores find their way to better living conditions, thus perpetuating the lineage. It appears that this particular form of multicellularity has evolved multiple times, including in the model organism Dictyostelium discoideum and its relatives in the Amoebozoa. A study of Dictyostelium genes by Gernot Glöckner and colleagues in 2016 revealed the presence of several unique membrane or secreted proteins that may have enabled the evolution of multicellularity in this lineage (Glöckner et al. 2016). For Glöckner, a professor at the University of Cologne, the natural next question was: where did these genes come from? To answer this question, Glöckner looked to protosteloid amoebae, single-celled relatives of Dictyostelium. Protosteloid fruiting bodies are composed of one or a few spores on the end of a stalk, but unlike in Dictyostelium, the entire fruiting body is derived from a single cell. In a recent article inGenome Biology and Evolution (Hillmann et al. 2018), Glöckner, along with Falk Hillmann of the Hans Knöll Institute and other colleagues, compared the gene repertoires and expression patterns of the protosteloid amoebae Protostelium aurantium and Protostelium mycophagum with those of the distantly related multicellular Dictyostelium. In doing so, they hoped to distinguish genes related to fruiting body development, a process shared by Dictyostelium and Protostelium, from those related to multicellularity, found only in Dictyostelium. Among the genes used for fruiting body development in Dictyostelium, Glöckner et al. were able to identify orthologs involved in the same process in the two Protostelium species. “It was exciting to see that developmental signaling is conserved from simple to multicellular systems,” says Glöckner. However, they noticed that the regulation of these genes was often in opposite directions in Protostelium andDictyostelium. Forexample, thegene statA isupregulatedduringfruitingbody development in Dictyostelium, where it plays a major role in chemical sensing and the formation of the fruiting body stalk. In contrast, its ortholog in P. aurantium is downregulated during fruitingbodydevelopment. Thiswasa surpriseaccording to Glöckner, as it indicates that “the genes involved in fruiting body formation were most likely independently recruited to this task in different lineages of Amoebozoa.” Also unexpected, according to Pauline Schaap, co-author of the study, was the exceptional number of genes involved in signaling and environmental sensing in the protosteloid amoebae. These genes are necessary for finding prey, evading predators, and adapting to environmental change, and it was somewhat surprising to find more of these genes in the unicellular Protostelium than inDictyosteliumwith its complex multicellular life cycle. Glöckner and colleagues note that such a large collection of signaling genes likely reflects the ability of the Amoebozoa to adapt to various environmental conditions, and they speculate that these signaling molecules provided the buildingblocks forcell–cell communication inearlymulticellular forms. Adds Schaap, “This suggests that their interactions with each other and with other organisms in their habitat are much more complex than is generally thought.” For Glöckner, these results offer a new paradigm for thinking about the evolution of complex traits like fruiting body formation and multicellularity. “Some researchers currently