High-Throughput Proteomics Reveals the Unicellular Roots of Animal Phosphosignaling and Cell Differentiation
Arnau Sebé-Pedrós 1, 8, Marcia Ivonne Peña 2, 4, Salvador Capella-Gutiérrez 3, 4, 5, Meritxell Antó 1, Toni Gabaldón 3, 4, 6, Iñaki Ruiz-Trillo 1, 6, 7, Eduard Sabidó 2, 4, 9 ,
1 Institut de Biologia Evolutiva (CSIC-Universitat Pompeu Fabra), Passeig Marítim de la Barceloneta 37-49, 08003 Barcelona, Spain
2 Proteomics Unit, Centre for Genomic Regulation (CRG), Dr. Aiguader 88, 08003 Barcelona, Spain
3 Bioinformatics and Genomics Program, Centre for Genomic Regulation (CRG), Dr. Aiguader 88, 08003 Barcelona, Spain
4 Universitat Pompeu Fabra (UPF), Dr. Aiguader 88, 08003 Barcelona, Spain
5 CBS Fungal Biodiversity Centre, Uppsalalaan 8, 3584 LT Utrecht, the Netherlands
6 ICREA, Pg. Lluis Companys 23, 08010 Barcelona, Spain
7 Departament de Genètica, Microbilogia i Estadística, Universitat de Barcelona, Avinguda Diagonal 643, 08028 Barcelona, Spain
Received 1 October 2015, Revised 17 July 2016, Accepted 16 September 2016, Available online 13 October 2016
Published: October 13, 2016
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.
Keywords
multicellularity; tyrosine kinase; signaling; origin of metazoa; evolution gene expression; mass spectrometry; proteomics; phosphoproteomics; Capsaspora; evolution
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