DEDB Workshop: Animal Cell Types: Their Origin and Evolution

Saturday January 6th, 6:30pm to 9:30pm.
Room: Foothills G

OPEN BAR DURING THE WORKSHOP!

 

In this workshop we bring together researchers working on a variety of systems to discuss the nature and the evolutionary origin of cell types in animals. Cell types are the fundamental building blocks of animals and the evolution of animal body plan complexity is intimately linked to an increase of the number of cell types. Recent advances in functional genomics has put scalable genomic research on cell types within the reach of investigators making it urgent to clarify the nature of cell types and the evolutionary history of cell types. In addition, advances in stem cell biology suggest models for the mechanistic underpinnings of cell type identity that need to be integrated into the research program of comparative biologists. We hope to stimulate an engaged discussion about these topics with the invited speakers and the audience.

Organizers: Günter P. Wagner, Yale University, and Detlev Arendt, EMBL, Heidelberg

 

PROGRAM

 

6:30 – 6:45 Detlev Arendt: Introduction to cell type evolution

6:45 – 7:10 Leonid L. Moroz: Origin of Animals, Neurons & Muscles through the Lens of Single-cell Genomics: First one million scRNA-seq across phyla

7:10 – 7:40     Sally P. Leys: Evolution of a sensory (epithelial) cell type

7:40 – 8:10     Jacob Musser: Single-cell RNAseq uncovers cell type diversity in sponges and sheds light on the ancestral complement of animal cell types

8:10 – 8:20     Break

8:20 – 8:45     Patrick Steinmetz: A non-bilaterian perspective on the origin and evolution of muscle cell types

8:45 – 9:10     Oscar A. Tarazona: Cell type evolution and the origin of cartilage

9:10 – 9:35     Eric Erkenbrack: The role of a classical cellular stress response in the evolution of a novel cell type in eutherian mammals

 

ABSTRACTS

 

Origin of Animals, Neurons & Muscles through the Lens of Single-cell Genomics: First one million scRNA-seq across phyla

By Leonid L. Moroz & Andrea B. Kohn

University of Florida, USA

There is more than one way to develop cell and tissue complexity, and animals frequently use different molecular toolkits to achieve similar functional outcomes (=convergent evolution). However, the genomic bases of convergent evolution are largely unknown. Here, we used a combination of microfluidic and massive-parallel single-cell RNAs (scRNA-seq) to capture thousands cell types in representatives of ten animal phyla (>1 million neurons). These species also represent major transitions in the formation of mesoderm, muscle and neural organizations as well as origins of complex organ systems (from comb jellies to cephalopods). First, we revisited the animal phylogeny and start to develop a metric to quantitate each cell’s type transcriptional relationships as well as criteria for cell-/neuronal homologies. Second, we showed that for many species tested, virtually all neurons are unique in their RNA modifications, non-coding RNAs, and secretory molecules, providing the foundation for the natural neuronal classification. The discovered molecular complexity of the numerically “simpler” neural systems and the emerging single-cell data suggest the hypothesis: neurons are different not only because they have different functions, but also because neurons and circuits have different genealogies, and perhaps independent origins at the broadest evolutionary scale from ctenophores and cnidarians to mollusks and chordates. Origins of neurons (and synapses) from different types of ancestral secretory cells might have occurred at least three times during Metazoa evolution. It appeared that mesoderm and muscles, including striated muscles, evolved independently. Also, our reconstructions suggest 9-12 independent events of nervous system centralizations from a common bilaterian/cnidarian ancestor with diffuse-like neural systems.  Thus, using examples of convergent evolution, we set up a foundation toward natural genealogical classification of cell classes across phyla. Perhaps, there is a type of the Periodic System of Neurons, which might be an analog of the Periodic System of chemical elements, with a predictive power for cellular phenotypes.

 

Evolution of a sensory (epithelial) cell type

Leys SP

All cells receive information from the environment, with the nature of the signal determining how the information is used. In the most basally branching metazoans, sponges and ctenophores, the transfers of information that occur – from the reception to delivery to effector cell – are still largely unknown. Epithelia function as barriers to the external environment and are likely to have been a cell type that became fixed early in the evolution of tissues. As the barrier cells, epithelia are prime targets for becoming specialized for sensory function. Did one of these cell types, only, retain a core regulatory complex that was retained in the cohort that continued on to become nerve cells in neuralians, or could this have occurred several times, in different cell cohorts, and in different phyla? If we consider all animals equally fitted for their environment, the view that cell type is an inheritable complex seems to entrench the counter-idea that some animals have more advanced cell types than others, despite the almost equal time they have had to evolve. Non-bilaterian phyla do not have smaller genomes than those of bilaterians. Their gene complement is not lower than that of bilaterians, but as with all groups, it does depend on divergence time and specialization of function. Until much more genomic and functional data is available for the cell types of the most basally branching phyla, it is not possible to say that cell types did not

 

Single-cell RNAseq uncovers cell type diversity in sponges and sheds light on the ancestral complement of animal cell types

Jacob Musser, EMBL, Heidelberg, Germany

A key transition in early animal evolution was the origin and diversification of specialized cell types. Sponges diverged early in animal evolution and apparently lack homologs of specialized cell types found in other animals, including neurons and muscles. However, sponge genomes contain many important neuronal and muscle genes. Here, we present a comparative single cell-transcriptomic study in sponges that investigates the gene expression programs of sponge cell types and sheds light on cell type diversification in early animals. We used an unbiased approach to characterize cell types in two species of demosponge, first dissociating entire mature individuals, and then conducting single-cell RNAseq on hundreds of cells. We then visualized and correlated distinct expression programs with cellular morphology using single-molecule fluorescent in situ hybridization (smFISH), a new method that overcomes previous limitations for visualizing expression in sponges. We show that sponges exhibit a diverse array of cell types, including epithelial cells expressing cell adhesion and signal transduction genes, collagenous cells, and ciliated cells enriched for genes implicated in sensory perception. Many homologs of neuronal genes are broadly expressed across different sponge cell types. However, we also identified several genes implicated in neurotransmitter synthesis and reception that are specific to different sponge cell types. Our results suggest that although sponges lack a morphologically-distinct nervous system, they do differentially deploy genes important in sensing the environment and intercellular communication.

 

A non-bilaterian perspective on the origin and evolution of muscle cell types

Steinmetz, P.R.H.

Sars Centre for Marine Molecular Biology, University of Bergen, Thormøhlensgt. 55, N-5006 Bergen, Norway

Animal muscle cells can be subdivided into smooth and striated types based on their ultrastructural characteristics. Their evolution was key to fundamental animal processes such as locomotion, digestion and communication. Increasing genomic and molecular biology resources from major non-bilaterian animal groups and even close relatives of metazoans have allowed addressing questions about the evolutionary origin and history of these muscle cell types. I will reconstruct the origin and evolution of structural components typical of striated or smooth muscle cell types using a phylogenomic and a comparative gene expression approach. The analysis shows that striated muscles, although sharing a specific subset of structural or regulatory proteins, have evolved multiple times independently during animal evolution. A comparison of the transcription factor expression profile between cnidarian and bilaterian muscles reveals that a smooth, cardiac-like muscle was likely ancestral to cnidarian and bilaterian animals.

 

Cell type evolution and the origin of cartilage

Oscar A. Tarazona, Leslie A. Slota, Davys H. Lopez, GuangJun Zhang, and Martin J. Cohn

University of Florida, Gainesville, FL 32610, USA

Evolution of novel cell types was central to the emergence of new tissues and organs during the diversification of animals. Cartilage is a specialized tissue generally considered to be unique to vertebrates. Cartilage matrix consists predominantly of type II collagen, encoded by the ColA gene Col21. We showed previously that the Col21 gene originated in stem vertebrates and may have been critical for evolution of the vertebrate cartilaginous skeleton. However, classical zoological studies reported the existence of enigmatic cartilage-like tissues in numerous invertebrates. Here we show that protostome and deuterostome cartilage shares structural and chemical properties, and that the mechanisms of cartilage development are extensively conserved — from induction of chondroprogenitor cells by Hedgehog and -catenin signaling, to chondrocyte differentiation and matrix synthesis by SoxE and SoxD regulation of ColA genes — suggesting that the chondrogenic GRN evolved in the common ancestor of Bilateria. These results reveal deep homology of the genetic program for cartilage development in Bilateria and suggest that activation of this ancient core chondrogenic network underlies the parallel evolution of cartilage tissues in Ecdysozoa, Lophotrochozoa and Deuterostomia.

 

The role of a classical cellular stress response in the evolution of a novel cell type in eutherian mammals

Eric Erkenbrack, Yale University

Decidual stromal cells (DSCs) are essential for establishing the fetal-maternal interface during pregnancy of eutherian (placental) mammals. DSCs differentiate in cell culture from precursor endometrial stromal fibroblasts (ESFs) upon stimulation with cyclic AMP/PKA (cAMP) signaling and progesterone (P4). To determine how the DSC differentiation cascade evolved, we isolated ESFs from the opossum (MdESFs), a member of the sister taxon marsupial mammals. We find MdESFs also express many transcription factors critical to DSC differentiation. However, upon stimulation with cAMP and P4, they fail to express classical DSC markers. In contrast, MdESF activate genes related to oxidative stress and apoptosis. We propose that the mechanistic
origins of DSC differentiation evolved from the brief fetal attachment phase of marsupials, a pro-inflammatory environment. In the lineage leading to modern eutherians, the regulatory genes active in the resulting cellular stress response were then re-programmed away from oxidative stress and apoptosis towards an anti-inflammatory phenotype.