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Review
. 2023 Nov 27:57:391-410.
doi: 10.1146/annurev-genet-071819-104035.

Paramecium Genetics, Genomics, and Evolution

Hongan Long  1   2 , Parul Johri  3 , Jean-Francois Gout  4 , Jiahao Ni  1 , Yue Hao  5   6 , Timothy Licknack  6 , Yaohai Wang  1 , Jiao Pan  1 , Berenice Jiménez-Marín  6 , Michael Lynch  6
Affiliations
Review

Paramecium Genetics, Genomics, and Evolution

Hongan Long et al. Annu Rev Genet. .

Abstract

The ciliate genus Paramecium served as one of the first model systems in microbial eukaryotic genetics, contributing much to the early understanding of phenomena as diverse as genome rearrangement, cryptic speciation, cytoplasmic inheritance, and endosymbiosis, as well as more recently to the evolution of mating types, introns, and roles of small RNAs in DNA processing. Substantial progress has recently been made in the area of comparative and population genomics. Paramecium species combine some of the lowest known mutation rates with some of the largest known effective populations, along with likely very high recombination rates, thereby harboring a population-genetic environment that promotes an exceptionally efficient capacity for selection. As a consequence, the genomes are extraordinarily streamlined, with very small intergenic regions combined with small numbers of tiny introns. The subject of the bulk of Paramecium research, the ancient Paramecium aurelia species complex, is descended from two whole-genome duplication events that retain high degrees of synteny, thereby providing an exceptional platform for studying the fates of duplicate genes. Despite having a common ancestor dating to several hundred million years ago, the known descendant species are morphologically indistinguishable, raising significant questions about the common view that gene duplications lead to the origins of evolutionary novelties.

Keywords: Paramecium; ciliates; evolutionary cell biology; gene duplication; genome evolution; population genomics.

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Figures

Figure 1
Figure 1
Phylogeny and morphology of Paramecium species. (a) A maximum-likelihood tree based on mitochondrial coxI sequences [National Center for Biotechnology Information (NCBI) GenBank Accession numbers are given as prefixes]. Species under the scale bar (0.5 substitutions per site) do not have available coxI sequences; nodes without numbers have bootstrap values <50. (b) Paramecium tetraurelia, (c) Paramecium biaurelia, (d) Paramecium biaurelia after ammoniacal silver carbonate staining, (e) Paramecium bursaria, and (f) Paramecium biaurelia after Hoechst 33342 staining.
Figure 2
Figure 2
The life cycle of Paramecium. Note that there are two MICs in most Paramecium aurelia species; for simplicity, in this diagram, conjugation and binary fission start with homozygous nuclei. Abbreviations: MAC, macronucleus; MIC, micronucleus.
Figure 3
Figure 3
Illustration of micronuclear versus macronuclear mutations. In a layout similar to that in multicellular animals, ciliates (in a single cell) harbor a transcriptionally silent germline nucleus (small dots) and a transcriptionally active macronucleus (large blobs), which is disposed of and replaced following meiosis via autogamy or conjugation. (Left) In the micronucleus, mutations accumulate neutrally during vegetative growth because transcription is confined to the macronucleus. However, these are then exposed after autogamy/conjugation and the construction of a new macronucleus from prior micronuclear material. Ostensibly, to reduce the high mutation load after extended periods of asexual reproduction, Paramecium species have evolved very low micronuclear mutation rates. (Right) This panel illustrates the possibility that the fitness effects of mutations accumulating in the macronucleus may be very small as a consequence of the masking effects resulting from the polyploid nature of the macronuclear genome. Not shown, however, is the potential drift of numbers of macronuclear copies of individual chromosomes and resultant stoichiometric imbalance.
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