The compact macronuclear genome of the ciliate halteria grandinella: A transcriptome-like genome with 23,000 nanochromosomes

Abstract

How to achieve protein diversity by genome and transcriptome processing is essential for organismal complexity and adaptation. The present work identifies that the macronuclear genome of Halteria grandinella, a cosmopolitan unicellu-lar eukaryote, is composed almost entirely of gene-sized nanochromosomes with extremely short nongenic regions. This challenges our usual understanding of chromosomal structure and suggests the possibility of novel mechvanisms in transcriptional regulation. Comprehensive analysis of multiple data sets reveals that Halteria transcription dynamics are influenced by: (i) nonuniform nanochromosome copy numbers correlated with gene-expression level; (ii) dynamic alterations at both the DNA and RNA levels, including alternative internal eliminated sequence (IES) deletions during macronucleus formation and large-scale alternative splicing in transcript maturation; and (iii) extremely short 59 and 39 untranslated regions (UTRs) and uni-versal TATA box-like motifs in the compact 59 subtelomeric regions of most chromo-somes. This study broadens the view of ciliate biology and the evolution of unicellu-lar eukaryotes, and identifies Halteria as one of the most compact known eukaryotic genomes, indicating that complex cell structure does not require complex gene architecture.