Twisted Tales: Insights into Genome Diversity of Ciliates Using Single-Cell ‘Omics

Abstract

The emergence of robust single-cell ‘omics techniques enables studies of uncultivable species, allowing for the (re)discovery of diverse genomic features. In this study, we combine single-cell genomics and transcriptomics to explore genome evolution in ciliates (a > 1 Gy old clade). Analysis of the data resulting from these single-cell ‘omics approaches show: 1) the description of the ciliates in the class Karyorelictea as “primitive” is inaccurate because their somatic macronuclei contain loci of varying copy number (i.e., they have been processed by genome rearrangements from the zygotic nucleus); 2) gene-sized somatic chromosomes exist in the class Litostomatea, consistent with Balbiani’s (1890) observation of giant chromosomes in this lineage; and 3) gene scrambling exists in the underexplored Postciliodesmatophora (the classes Heterotrichea and Karyorelictea, abbreviated here as the Po-clade), one of two major clades of ciliates. Together these data highlight the complex evolutionary patterns underlying germline genome architectures in ciliates and provide a basis for further exploration of principles of genome evolution in diverse microbial lineages.

Evolutionary origins and impacts of genome architecture in ciliates

“…) . While nonscrambled germ‐line organization is common across the ciliate phylogeny, emerging evidence from poorly sampled lineages suggests that scrambled germ‐line loci may be more common than previously expected …”

“…In these taxa, there is evidence for substantially greater purifying selection acting on orthologous and paralogous genes compared to ciliates able to divide their macronuclei through amitosis (unpublished data). This appears to occur despite germ‐line genome architectures similar to other ciliate taxa and indicates the ability that amitosis has to enhance patterns of protein evolution.…”

“…Due to mechanistic similarities between the developmentally regulated genome rearrangements in ciliates and transposon regulation in other taxa, Klobutcher and Herrick proposed that evolution of nuclear dualism in ciliates was an evolutionary response to TE invasion, providing the means to purge them from the somatic genome. While the somatic genomes of most ciliates studied to date are effectively free of TEs, the germ‐line genomes are enriched with repetitive regions/sequences that interrupt gene‐coding sequences (an exception being the model ciliate Tetrahymena thermophila , where these regions are predominantly intergenic or intronic) and need to be excised during development of a new somatic genome . While the evolutionary origin of these repetitive regions is unclear given their vast diversity within a single germ‐line genome, many harbor signatures of once functional TEs (i.e., repetitive boundary sequences or small terminal inverted repeats, such as TA; Fig.…”

“…More recently, a survey of IESs from the complete T. thermophila germ‐line genome has found that ∼42% of the IESs (comprising 10.9 Mbp of the 150 Mbp germ‐line genome) are putative TEs and their decayed remnants . While all IESs identified among diverse ciliate lineages, spanning ∼1 GYA, are demarcated by direct repeats at their MDS–IES boundaries, these data suggest that TEs have played a role in the origin of some of the IESs found in ciliate germ‐line genomes.…”

“…[18][19][20][21][22][23][24] This involves the elimination of germline-limited DNA (e.g., TEs, centromeres, germline-limited genes, and internally eliminated sequences (IESs)) and the assembly of functional somatic regions (i.e., macronuclear-destined sequences (MDS)). 18,[25][26][27][28][29][30] Although details differ across ciliate lineages, the delineation during development between somatic MDSs and the germline-limited IESs, which separate MDSs, involves RNA-guided mechanisms that resemble epigenetic responses to TE invasion/control in other eukaryotes. 17,[19][20][21][22][23][24] Here, we describe how the atypical genome architectures in ciliates, coupled with a predominantly asexual life cycle punctuated by rare sexual events (similar to yeasts and other protists), provide them with an immense evolutionary potential and the means for rapid adaptation.…”