Sponges and evolutionary origins: Sponges represent our distant animal relatives. They do not have a nervous system but do have a simple body for filter feeding. Surveying the cell types in the freshwater sponge Spongilla lacustris , Musser et al . found that many genes important in synaptic communication are expressed in cells of the small digestive chambers. They found secretory machinery characteristic of the presynapse in small multipolar cells contacting all other cells and also the receptive apparatus of the postsynapse in the choanocytes that generate water flow and digest microbial food. These results suggest that the first directed communication in animals may have evolved to regulate feeding, serving as a starting point on the long path toward nervous system evolution. —BAP

Activation triggers the exchange of subunits in Ca²⁺/calmodulin-dependent protein kinase II (CaMKII), an oligomeric enzyme that is critical for learning, memory, and cardiac function. The mechanism by which subunit exchange occurs remains elusive. We show that the human CaMKII holoenzyme exists in dodecameric and tetradecameric forms, and that the calmodulin (CaM)-binding element of CaMKII can bind to the hub of the holoenzyme and destabilize it to release dimers. The structures of CaMKII from two distantly diverged organisms suggest that the CaM-binding element of activated CaMKII acts as a wedge by docking at intersubunit interfaces in the hub. This converts the hub into a spiral form that can release or gain CaMKII dimers. Our data reveal a three-way competition for the CaM-binding element, whereby phosphorylation biases it towards the hub interface, away from the kinase domain and calmodulin, thus unlocking the ability of activated CaMKII holoenzymes to exchange dimers with unactivated ones.

Filopodia are fine actin-based cellular projections used for both environmental sensing and cell motility, and they are essential organelles for metazoan cells. In this study, we reconstruct the origin of metazoan filopodia and microvilli. We first report on the evolutionary assembly of the filopodial molecular toolkit and show that homologs of many metazoan filopodial components, including fascin and myosin X, were already present in the unicellular or colonial progenitors of metazoans. Furthermore, we find that the actin crosslinking protein fascin localizes to filopodia-like structures and microvilli in the choanoflagellate Salpingoeca rosetta. In addition, homologs of filopodial genes in the holozoan Capsaspora owczarzaki are upregulated in filopodia-bearing cells relative to those that lack them. Therefore, our findings suggest that proteins essential for metazoan filopodia and microvilli are functionally conserved in unicellular and colonial holozoans and that the last common ancestor of metazoans bore a complex and specific filopodial machinery.

A fundamental breakthrough in neurobiology has been the formulation of the neuron doctrine by Santiago Ramón y Cajal, which stated that the nervous system is composed of discrete cells. Electron microscopy later confirmed the doctrine and allowed the identification of synaptic connections. In this work, we used volume electron microscopy and three-dimensional reconstructions to characterize the nerve net of a ctenophore, a marine invertebrate that belongs to one of the earliest-branching animal lineages. We found that neurons in the subepithelial nerve net have a continuous plasma membrane that forms a syncytium. Our findings suggest fundamental differences of nerve net architectures between ctenophores and cnidarians or bilaterians and offer an alternative perspective on neural network organization and neurotransmission.

Although collar cells are conserved across animals and their closest relatives, the choanoflagellates, little is known about their ancestry, their subcellular architecture, or how they differentiate. The choanoflagellate Salpingoeca rosetta expresses genes necessary for animal development and can alternate between unicellular and multicellular states, making it a powerful model for investigating the origin of animal multicellularity and mechanisms underlying cell differentiation. To compare the subcellular architecture of solitary collar cells in S. rosetta with that of multicellular ‘rosette’ colonies and collar cells in sponges, we reconstructed entire cells in 3D through transmission electron microscopy on serial ultrathin sections. Structural analysis of our 3D reconstructions revealed important differences between single and colonial choanoflagellate cells, with colonial cells exhibiting a more amoeboid morphology consistent with higher levels of macropinocytotic activity. Comparison of multiple reconstructed rosette colonies highlighted the variable nature of cell sizes, cell–cell contact networks, and colony arrangement. Importantly, we uncovered the presence of elongated cells in some rosette colonies that likely represent a distinct and differentiated cell type, pointing toward spatial cell differentiation. Intercellular bridges within choanoflagellate colonies displayed a variety of morphologies and connected some but not all neighbouring cells. Reconstruction of sponge choanocytes revealed ultrastructural commonalities but also differences in major organelle composition in comparison to choanoflagellates. Together, our comparative reconstructions uncover the architecture of cell differentiation in choanoflagellates and sponge choanocytes and constitute an important step in reconstructing the cell biology of the last common ancestor of animals. Choanoflagellates are microscopic aquatic organisms that can alternate between single-celled and multicellular states, and sequencing of their genomes has revealed that choanoflagellates are the closest single-celled relatives of animals. Moreover, choanoflagellates are a form of ‘collar cell’—a cell type crowned by an array of finger-like microvilli and a single, whip-like flagellum. This cell type is also found throughout the animal kingdom; therefore, studying the structure of the choanoflagellate collar cell can shed light on how this cell type and animal multicellularity might have evolved. We used electron microscopy to reconstruct in 3D the total subcellular composition of single-celled and multicellular choanoflagellates as well as the collar cells from a marine sponge, which represents an early-branching animal lineage. We found differences between single-celled and multicellular choanoflagellates in structures associated with cellular energetics, membrane trafficking, and cell morphology. Likewise, we describe a complex system of cell–cell connections associated with multicellular choanoflagellates. Finally, comparison of choanoflagellates and sponge collar cells revealed subcellular differences associated with feeding and cellular energetics. Taken together, this study is an important step forward in reconstructing the biology of the last common ancestor of the animals.