Abstract

Author SummaryThe macronuclear genome of the ciliate Oxytricha trifallax, contained in its somatic nucleus, has a unique genome architecture. Unlike its diploid germline genome, which is transcriptionally inactive during normal cellular growth, the macronuclear genome is fragmented into at least 16,000 tiny (∼3.2 kb mean length) chromosomes, most of which encode single actively transcribed genes and are differentially amplified to a few thousand copies each. The smallest chromosome is just 469 bp, while the largest is 66 kb and encodes a single enormous protein. We found considerable variation in the genome, including frequent alternative fragmentation patterns, generating chromosome isoforms with shared sequence. We also found limited variation in chromosome amplification levels, though insufficient to explain mRNA transcript level variation. Another remarkable feature of Oxytricha's macronuclear genome is its inordinate fondness for telomeres. In conjunction with its possession of tens of millions of chromosome-ending telomeres per macronucleus, we show that Oxytricha has evolved multiple putative telomere-binding proteins. In addition, we identified two new domesticated transposase-like protein classes that we propose may participate in the process of genome rearrangement. The macronuclear genome now provides a crucial resource for ongoing studies of genome rearrangement processes that use Oxytricha as an experimental or comparative model.

Highlights

  • Oxytricha trifallax is a distinctive ciliate [1]—an ancient lineage of protists named for their coats of cilia

  • Macronuclear Genome Assemblies To assemble the Oxytricha macronuclear genome for the type strain—JRB310 [1]—we chose to build upon three assemblies, from ABySS [34], IDBA [35], and paired end (PE)-Assembler [36]/SSAKE [37], based on Illumina sequences, and supplemented by a Sanger/454 assembly

  • We developed a specialized meta-assembly pipeline

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Summary

Introduction

Oxytricha trifallax is a distinctive ciliate [1]—an ancient lineage of protists named for their coats of cilia. In the model ciliates Oxytricha trifallax, Tetrahymena thermophila, and Paramecium tetraurelia, varying amounts of micronuclear DNA are deleted (including the ‘‘internally eliminated sequences,’’ or IESs, interspersed between ‘‘macronuclear destined sequences,’’ or MDSs) during conjugation or autogamy (two forms of sexual development) to give rise to the information-rich macronuclear genome (Figure 1). A much larger fraction of the Oxytricha micronuclear genome—,96% of the micronuclear complexity [2]—is eliminated during the macronuclear formation than in the oligohymenophoreans, Tetrahymena and Paramecium (which both eliminate ,30% of their micronuclear genomes [4,5]). The most remarkable difference in macronuclear development between Oxytricha and the two oligohymenophoreans is that the micronuclear-encoded MDSs that give rise to the macronuclear chromosomes may be nonsequential, or even in different orientations in the micronuclear genome [6]. Unlike the oligohymenophoreans, Oxytricha needs to unscramble its micronuclear genome during macronuclear development

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