Short jump from single-cell to multi-cell animals

Our single-celled ancestors lived about 800 million years ago. Now, new evidence suggests their leap to multi-celled organisms was not quite as mysterious as once believed.

In a Developmental Cell paper publishing October 13, 2016, researchers demonstrate how our single-celled ancestors likely had molecular mechanisms used in cells today. Way back when — these assisted development into different cell types and then into tissue types.

"We're looking into the past at an evolutionary transition that was important for the origin of all animals. We show that these early organisms already had some behaviors that we once thought were only in multicellular animals. From there, it would have been a simpler evolutionary leap."

Iñaki Ruiz-Trillo PhD, Evolutionary Biologist, Institute of Evolutionary Biology, Barcelona, Spain.

Researchers studied a single-celled amoeba called Capsaspora owczarzaki. Originally discovered living inside a freshwater snail, it has been studied by Ruiz-Trillo's group to learn more about animal evolution. His team sequenced the Capsaspora genome in an earlier project and discovered that the amoeba contained many genes, that in animals, relate to multicellular functions.

As a single-celled organism, Capsaspora doesn't have multiple cell types — as humans do. But, Capsaspora does change its cell type over time, from a single amoeba into a colony of cells in a cyst formation in its life cycle. The cyst is an aggregate of different Capsapora joining together, perhaps to survive desperate evironmental conditions, such as drought. Previously free-living, single cells gathered together do not have to be genetically identical.

The study examined whether Capsaspora uses the same molecular mechanisms to differentiate its one cell over time — as more complex animals use to differentiate into multiple cells and tissues.

In collaboration with the team of Eduard Sabidó at the Proteomics Unit of the Centre for Genomic Regulation and Universitat Pompeu Fabra, the group analyzed proteins in Capsaspora to determine its internal cell processes at different life stages.

"Mass spectrometry-based proteomics allows us to measure proteins being expressed and how they are being modified. Intracellular signaling depends on these protein modifications — so by analysis, we know not only what's in the cell, but also how the cell organizes and communicates internally."

Eduard Sabidó PhD, Head, Proteomics Core Facility, Centre for Genomic Regulation, University Pompeu Fabra, Barcelona, Spain.

Capsaspora owczarzaki can differentiate into two different cell types, (1) a cell type with filopodia-like structures; and (2) a naked, cyst form. Researchers discovered that from one stage to another, Capsaspora's suite of proteins use many of the same tools as multicellular animals to regulate change.

For example, Capsaspora activates proteins that bind to specific DNA sequences, thus controlling the rate of genetic information being transcribed from DNA to messenger RNA. It also has a tyrosine-kinase signaling system in it's two stages. Tyrosine kinase is an enzyme that transfers a phosphate group from ATP to a specific protein within a cell. The process functions as an "on" or "off" switch in cell functions and regulates protein formation.

"These are the same mechanisms that animals use to differentiate one cell type from another, but they haven't been observed in unicellular organisms before."

Iñaki Ruiz-Trillo PhD

The presence of these protein-regulating tools in both Capsaspora and animals means that the single-celled ancestor of all animals likely also possessed these systems — and was more complex than scientists have previously given it credit for. "The ancestor already had the tools that the cell needed to differentiate into different tissues," says Sabidó. "The cells that were around before animals were more or less prepared for this leap."

Abstract Highlights
•Proteome remodeling is linked to temporal differentiation in a unicellular context
•Dynamic phosphosignaling underlies unicellular temporal differentiation
•Parallel evolution of Ser/Thr and Tyr kinase phosphoregulatory networks
•Cell-type-specific phosphoactivation of Tyr kinases in Capsaspora

Summary
Cell-specific regulation of protein levels and activity is essential for the distribution of functions among multiple cell types in animals. The finding that many genes involved in these regulatory processes have a premetazoan origin raises the intriguing possibility that the mechanisms required for spatially regulated cell differentiation evolved prior to the appearance of animals. Here, we use high-throughput proteomics in Capsaspora owczarzaki, a close unicellular relative of animals, to characterize the dynamic proteome and phosphoproteome profiles of three temporally distinct cell types in this premetazoan species. We show that life-cycle transitions are linked to extensive proteome and phosphoproteome remodeling and that they affect key genes involved in animal multicellularity, such as transcription factors and tyrosine kinases. The observation of shared features between Capsaspora and metazoans indicates that elaborate and conserved phosphosignaling and proteome regulation supported temporal cell-type differentiation in the unicellular ancestor of animals.

This work was supported by the European Research Council, the Spanish Ministry of Economy and Competitiveness, the Qatar National Research Fund, the European Union, the Institució Catalana de Recerca i Estudis Avançats, and the Secretaria d'Universitats i Recerca del Departament d'Economia i Coneixement de la Generalitat de Catalunya.

Developmental Cell (@Dev_Cell), published by Cell Press, is a bimonthly, cross-disciplinary journal that brings together the fields of cell biology and developmental biology. Articles provide new biological insight of cell proliferation, intracellular targeting, cell polarity, membrane traffic, cell migration, stem cell biology, chromatin regulation and function, differentiation, morphogenesis and biomechanics, and regeneration and cellular homeostasis. Visit: http://www.cell.com/developmental-cell. To receive Cell Press media alerts, contact press@cell.com.

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