New genomes of unicellular holozoans shed light onto the origins of complex animal gene architecture

Abstract

The origin of animal multicellularity is a major event in eukaryotic evolution. Metazoans share many novelties in genome content and structure related to their multicellular lifestyle, like gene families (transcription factors and specific signaling pathways) and regulatory mechanisms (alternative splicing or enhancer-enabled introns). Since many of these traits predate metazoans, the study of their unicellular holozoan relatives is key to understand animal origins. We analyse the evolution of gene architecture using new ichthyosporean genomes, choanoflagellates and the filasterean Capsaspora owczarzaki, plus 40 other eukaryote genomes. This two-fold analysis focuses on the evolution of 1) intron/exon structure and 2) protein domain architectural rearrangements (which define gene families’ function and diversification). Animals have complex gene architectures, intron-rich and with high protein domain diversity. We find that such enrichments occur in differentially-timed innovation bursts. For example, the most important premetazoan intronization event occurred in the last common ancestor of choanoflagellates and animals (>80% homologous introns when compared to the urme-tazoan). Conversely, animal-specific protein domain arrangements often appear before, in the urholozoan (~12% of novel arrangements, compared to frequent contractions in later-branching lineages). Our results support a scenario of sudden innovation processes within holozoans followed by gradual simplifications in extant protistan lineages, while Metazoa retain most novelties and develop more of their own. This is observed for both intronization and protein rearrangements. Yet, these aspects of gene architecture are decoupled in time and mechanis- tics: non-coding and coding gene elements are under different evolutionary pressures, and innovation bursts are identified in different ancestors.