Abstract
As a model organism for studies of cell and environmental biology, the free-living and cosmopolitan ciliate Euplotes vannus shows intriguing features like dual genome architecture (i.e., separate germline and somatic nuclei in each cell/organism), "gene-sized" chromosomes, stop codon reassignment, programmed ribosomal frameshifting (PRF) and strong resistance to environmental stressors. However, the molecular mechanisms that account for these remarkable traits remain largely unknown. Here we report a combined analysis of de novo assembled high-quality macronuclear (MAC; i.e., somatic) and partial micronuclear (MIC; i.e., germline) genome sequences for E.vannus, and transcriptome profiling data under varying conditions. The results demonstrate that: (a) the MAC genome contains more than 25,000 complete "gene-sized" nanochromosomes (~85Mb haploid genome size) with the N50 ~2.7kb; (b) although there is a high frequency of frameshifting at stop codons UAA and UAG, we did not observe impaired transcript abundance as a result of PRF in this species as has been reported for other euplotids; (c) the sequence motif 5'-TA-3' is conserved at nearly all internally-eliminated sequence (IES) boundaries in the MIC genome, and chromosome breakage sites (CBSs) are duplicated and retained in the MAC genome; (d) by profiling the weighted correlation network of genes in the MAC under different environmental stressors, including nutrient scarcity, extreme temperature, salinity and the presence of ammonia, we identified gene clusters that respond to these external physical or chemical stimulations, and (e) we observed a dramatic increase in HSP70 gene transcription under salinity and chemical stresses but surprisingly, not under temperature changes; we link this temperature-resistance to the evolved loss of temperature stress-sensitive elements in regulatory regions. Together with the genome resources generated in this study, which are available online at Euplotes vannus Genome Database (http://evan.ciliate.org), these data provide molecular evidence for understanding the unique biology of highly adaptable microorganisms.
Highlights
Single-celled microorganisms were the first forms of life that developed on Earth approximately ~3.2 billion years ago, firstly as prokaryotic forms and evolved into eukaryotic cells between 1.4-2.0 billion years ago (Cavalier-Smith 2006; Schopf et al., 2018)
The distance between the transcription start site (TSS) for each gene and the upstream telomere is generally less than 80 nt (Figure S3b). 32755 protein-coding genes were identified in the final somatic genome assembly, along with 109 tRNAs comprising 48 codon types for 20 amino acids (Table S3)
Our results show no significant difference between the abundance of transcripts that incorporate a frameshifting event and those without frameshifting and implied that the decoding delay induced by ribosomal frameshifting would not be compensated by transcript abundance change
Summary
Single-celled microorganisms were the first forms of life that developed on Earth approximately ~3.2 billion years ago, firstly as prokaryotic forms and evolved into eukaryotic cells between 1.4-2.0 billion years ago (Cavalier-Smith 2006; Schopf et al., 2018). Microbes have been evolving and developed a wide variety of biological mechanisms to survive in the long history of the Earth. Ciliates possess both the compact germline micronucleus (MIC) and the transcriptionally active somatic macronucleus (MAC) within each cell (Katz 2001; Prescott 1994). Ciliates have great ability to survive in a wide range of harsh conditions, and feature strong tolerance to an array of environmental stressors. Many of these conditions, such as heavy metal contamination, are believed to induce evolutionarily conserved molecular defense mechanisms (Kim et al, 2018). It is important to elucidate the molecular mechanisms employed by the single cells in response to external stresses
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