Lu, M. W. | Search bioRxiv

bioRxiv2022

Comparative genomics reveals insight into the evolutionary origin of massively scrambled genomes.

Ciliates are microbial eukaryotes that undergo extensive programmed genome rearrangement that converts long germline chromosomes into smaller gene-rich somatic chromosomes. Three well-studied ciliates include Oxytricha trifallax, Tetrahymena thermophila and Paramecium tetraurelia, but only the Oxytricha lineage has a massively scrambled genome whose assembly requires hundreds of thousands of precise DNA joining events. Here we study the emergence of genome complexity by examining the origin and evolution of discontinuous and scrambled genes in the Oxytricha lineage. We sequenced, assembled and annotated the germline and somatic genomes of Euplotes woodruffi and the germline genome of Tetmemena sp., and compared their genome rearrangement features to that of the model ciliate Oxytricha trifallax. The germline genome of Tetmemena is as massively scrambled and interrupted as Oxytrichas: 13.6% of its gene loci rearrange via translocations and/or inversions. This study revealed that the earlier-diverged spirotrich, E. woodruffi, also has a scrambled genome, but approximately half as many loci (7.3%) are scrambled, supporting its position as a possible evolutionary intermediate in this lineage, in the process of accumulating complex genome rearrangements. Scrambled loci are more often associated with local duplications, supporting a simple model for the origin of scrambled genes via DNA duplication and decay.

evolutionary biology↗

bioRxiv2020

Transcribed germline-limited coding sequences in Oxytricha trifallax

The germline-soma divide is a fundamental distinction in developmental biology, and different genes are expressed in germline and somatic cells throughout metazoan life cycles. Ciliates, a group of microbial eukaryotes, exhibit germline-somatic nuclear dimorphism within a single cell with two different genomes. The ciliate Oxytricha trifallax undergoes massive RNA-guided DNA elimination and genome rearrangement to produce a new somatic macronucleus (MAC) from a copy of the germline micronucleus (MIC). This process eliminates noncoding DNA sequences that interrupt genes and also deletes hundreds of germline-limited open reading frames (ORFs) that are transcribed during genome rearrangement. Here, we update the set of transcribed germline-limited ORFs (TGLOs) in O. trifallax. We show that TGLOs tend to be expressed during nuclear development and then are absent from the somatic MAC. We also demonstrate that exposure to synthetic RNA can reprogram TGLO retention in the somatic MAC and that TGLO retention leads to transcription outside the normal developmental program. These data suggest that TGLOs represent a group of developmentally regulated protein coding sequences whose gene expression is terminated by DNA elimination.

genomics↗