A morphospecies is defined as a taxonomic species based wholly on morphology, but often morphospecies consist of clusters of cryptic species that can be identified genetically or molecularly. The nature of the evolutionary novelty that accompanies speciation in a morphospecies is an intriguing question. Morphospecies are particularly common among ciliates, a group of unicellular eukaryotes that separates 2 kinds of nuclei—the silenced germline nucleus (micronucleus [MIC]) and the actively expressed somatic nucleus (macronucleus [MAC])—within a common cytoplasm. Because of their very similar morphologies, members of the Tetrahymena genus are considered a morphospecies. We explored the hidden genomic evolution within this genus by performing a comprehensive comparative analysis of the somatic genomes of 10 species and the germline genomes of 2 species of Tetrahymena . These species show high genetic divergence; phylogenomic analysis suggests that the genus originated about 300 million years ago (Mya). Seven universal protein domains are preferentially included among the species-specific (i.e., the youngest) Tetrahymena genes. In particular, leucine-rich repeat (LRR) genes make the largest contribution to the high level of genome divergence of the 10 species. LRR genes can be sorted into 3 different age groups. Parallel evolutionary trajectories have independently occurred among LRR genes in the different Tetrahymena species. Thousands of young LRR genes contain tandem arrays of exactly 90-bp exons. The introns separating these exons show a unique, extreme phase 2 bias, suggesting a clonal origin and successive expansions of 90-bp–exon LRR genes. Identifying LRR gene age groups allowed us to document a Tetrahymena intron length cycle. The youngest 90-bp exon LRR genes in T . thermophila are concentrated in pericentromeric and subtelomeric regions of the 5 micronuclear chromosomes, suggesting that these regions act as genome innovation centers. Copies of a Tetrahymena Long interspersed element (LINE)-like retrotransposon are very frequently found physically adjacent to 90-bp exon/intron repeat units of the youngest LRR genes. We propose that Tetrahymena species have used a massive exon-shuffling mechanism, involving unequal crossing over possibly in concert with retrotransposition, to create the unique 90-bp exon array LRR genes.

Certain ciliates of the subclass Scuticociliatia (scuticociliates) are facultative parasites of fishes in which they cause a suite of diseases collectively termed scuticociliatosis. Hitherto, comparatively little was known about genetics and genomics of scuticociliates or the mechanism of scuticociliatosis. In this study, a laboratory culture of the facultatively pathogenic scuticociliate Pseudocohnilembus persalinus was established and its genome sequenced, giving the first genome of a marine ciliate. Genome-wide horizontal gene transfer (HGT) analysis showed P. persalinus has acquired many unique prokaryote-derived genes that potentially contribute to the virulence of this organism, including cell adhesion, hemolysis and heme utilization genes. These findings give new insights into our understanding of the pathology of scuticociliates.

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Two populations of Epistylis chlorelligerum Shen 1980, a colonial limnetic peritrich ciliate, were collected from different locations in China: E. chlorelligerum 1 from West Lake, Hangzhou; E. chlorelligerum 2 from East Lake, Wuhan. The morphology, infraciliature and SSU rRNA gene sequence of the two populations were investigated based on living and protargol-stained specimens. Although both populations are consistent with previous descriptions of protargol-stained specimens of this species, some differences in the morphology in vivo were observed. The two populations had identical SSU rRNA gene sequences. A second species, Epistylis chrysemydis Bishop and Jahn 1941, was also collected from East Lake, Wuhan, and was investigated for its morphology, infraciliature and SSU rRNA gene sequence. Phylogenetic analyses based on SSU rRNA gene sequence data indicate that the two populations of E. chlorelligerum are nested within the Epistylididae clade near E. wenrichi and E. urceolata. Epistylis chrysemydis is sister to the group comprising E. chlorelligerum, E. wenrichi, and E. urceolata.

Resting cyst formation is a remarkable survival strategy used by ciliates in response to the adverse environmental conditions. However, the mechanisms underlying encystment are poorly understood. Here, the genetic basis of encystment in Colpoda aspera was examined through RNA sequencing to identify transcriptome-wide changes in gene expression between vegetative and encystment stages. After de novo assembly, 49,543 transcripts were identified. Gene annotation and pathway mapping analysis revealed marked changes in biosynthesis, energy metabolism, and autophagy pathways during cyst formation. In addition, some differentially regulated genes were predicted to function in the interconnected cAMP, AMPK, mTOR, and PI3K/AKT signaling pathways, potentially forming a regulatory network for encystment. The present study conducted a large-scale assessment of Colpoda aspera genomic resources and provides new insight into the molecular mechanisms underlying cyst formation.

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