Dynamics of Gene Loss following Ancient Whole-Genome Duplication in the CrypticParameciumComplex

Abstract

Whole-genome duplications (WGDs) have shaped the gene repertoire of many eukaryotic lineages. The redundancy created by WGDs typically results in a phase of massive gene loss. However, some WGD-derived paralogs are maintained over long evolutionary periods, and the relative contributions of different selective pressures to their maintenance is still debated. Previous studies have revealed a history of three successive WGDs in the lineage of the ciliate Paramecium tetraurelia and two of its sister species from the P. aurelia complex. Here, we report the genome sequence and analysis of 10 additional P. aurelia species and one additional outgroup, revealing aspects of post-WGD evolution in 13 species sharing a common ancestral WGD. Contrary to the morphological radiation of vertebrates that putatively followed two WGD events, members of the cryptic P. aurelia complex have remained morphologically indistinguishable after hundreds of millions of years. Biases in gene retention compatible with dosage constraints appear to play a major role opposing post-WGD gene loss across all 13 species. In addition, post-WGD gene loss has been slower in Paramecium than in other species having experienced genome duplication, suggesting that the selective pressures against post-WGD gene loss are especially strong in Paramecium. A near complete lack of recent single-gene duplications in Paramecium provides additional evidence for strong selective pressures against gene-dosage changes. This exceptional dataset of 13 species sharing an ancestral WGD and two closely related outgroup species will be a useful resource for future studies on Paramecium as a major model organism in the evolutionary cell biology.

Mitogenomic architecture and evolution of the soil ciliates Colpoda

“…6A through D, Gap1 was caused by the loss of ccmf gene, and Gap2 in C. cucullus was caused by the loss of ymf64 and ymf75 . In diploid nuclear genomes, gene deletion events generally occur after whole-genome duplication in an organism, leading to the loss of some functional genes ( 61 ). To explain the gene order change in mitogenomes, Boore and Brown ( 62 ) proposed the tandem duplication–random loss model, which attaches great importance to the duplication of mitogenes followed by gene loss.…”

Genome-wide identification of ATP-binding cassette transporter B subfamily, focusing on its structure, evolution and rearrangement in ciliates

“…An old WGD occurred before the separation of Paramecium and Tetrahymena lineages, and a more recent WGD occurred before differentiation of the Paramecium aurelia complex [ 56 ]. The collinearity of ABCB genes that we observed suggests that this WGD resulted in ABCB gene expansion in the P. aurelia complex [ 56 , 65 ].…”

Small‐RNA‐guided histone modifications and somatic genome elimination in ciliates

“…Ciliate cells contain one or more germline micronuclei (MICs) and one or more somatic macronuclei (MACs), with different genomes, epigenomes and modes of division. The model ciliate Paramecium , which will be the focus of this review, belongs to the Paramecium aurelia complex, a group of 15 cryptic species that share at least three past whole‐genome duplications (WGDs), the most recent one shortly predating the speciation events in the formation of the group (Aury et al, 2006; Gout et al, 2023; McGrath, Gout, Doak, et al, 2014; McGrath, Gout, Johri, et al, 2014). Paramecium aurelia species are well suited for genetic analyses because of their two alternative modes of sexual reproduction, as well as extremely low mutation rates such as observed in P. tetraurelia (Sung et al, 2012).…”