Population Genetics of Paramecium Mitochondrial Genomes

Recombination, Mutation Spectrum, and Efficacy of Selection

Parul Johri, Georgi K. Marinov, Thomas G. Doak, Michael Lynch

Research output: Contribution to journalArticle

Abstract

The evolution of mitochondrial genomes and their population-genetic environment among unicellular eukaryotes are understudied. Ciliate mitochondrial genomes exhibit a unique combination of characteristics, including a linear organization and the presence of multiple genes with no known function or detectable homologs in other eukaryotes. Here we study the variation of ciliate mitochondrial genomes both within and across 13 highly diverged Paramecium species, including multiple species from the P. aurelia species complex, with four outgroup species: P. caudatum, P. multimicronucleatum, and two strains that may represent novel related species. We observe extraordinary conservation of gene order and protein-coding content in Paramecium mitochondria across species. In contrast, significant differences are observed in tRNA content and copy number, which is highly conserved in species belonging to the P. aurelia complex but variable among and even within the other Paramecium species. There is an increase in GC content from ∼20% to ∼40% on the branch leading to the P. aurelia complex. Patterns of polymorphism in population-genomic data and mutation-accumulation experiments suggest that the increase in GC content is primarily due to changes in the mutation spectra in the P. aurelia species. Finally, we find no evidence of recombination in Paramecium mitochondria and find that the mitochondrial genome appears to experience either similar or stronger efficacy of purifying selection than the nucleus.

Original languageEnglish (US)
Pages (from-to)1398-1416
Number of pages19
JournalGenome biology and evolution
Volume11
Issue number5
DOIs
StatePublished - May 1 2019

Fingerprint

Paramecium
Mitochondrial Genome
Population Genetics
Genetic Recombination
population genetics
recombination
mutation
genome
Mutation
Base Composition
Eukaryota
Ciliophora
eukaryotic cells
Mitochondria
mitochondria
Urodela
Metagenomics
Gene Order
Caudata
eukaryote

Keywords

  • Paramecium
  • efficacy of purifying selection
  • mitochondria
  • mutation spectrum
  • recombination
  • telomeres

ASJC Scopus subject areas

  • Ecology, Evolution, Behavior and Systematics
  • Genetics

Cite this

Population Genetics of Paramecium Mitochondrial Genomes : Recombination, Mutation Spectrum, and Efficacy of Selection. / Johri, Parul; Marinov, Georgi K.; Doak, Thomas G.; Lynch, Michael.

In: Genome biology and evolution, Vol. 11, No. 5, 01.05.2019, p. 1398-1416.

Research output: Contribution to journalArticle

@article{196b990dec0842c285869e697cad1f11,
title = "Population Genetics of Paramecium Mitochondrial Genomes: Recombination, Mutation Spectrum, and Efficacy of Selection",
abstract = "The evolution of mitochondrial genomes and their population-genetic environment among unicellular eukaryotes are understudied. Ciliate mitochondrial genomes exhibit a unique combination of characteristics, including a linear organization and the presence of multiple genes with no known function or detectable homologs in other eukaryotes. Here we study the variation of ciliate mitochondrial genomes both within and across 13 highly diverged Paramecium species, including multiple species from the P. aurelia species complex, with four outgroup species: P. caudatum, P. multimicronucleatum, and two strains that may represent novel related species. We observe extraordinary conservation of gene order and protein-coding content in Paramecium mitochondria across species. In contrast, significant differences are observed in tRNA content and copy number, which is highly conserved in species belonging to the P. aurelia complex but variable among and even within the other Paramecium species. There is an increase in GC content from ∼20{\%} to ∼40{\%} on the branch leading to the P. aurelia complex. Patterns of polymorphism in population-genomic data and mutation-accumulation experiments suggest that the increase in GC content is primarily due to changes in the mutation spectra in the P. aurelia species. Finally, we find no evidence of recombination in Paramecium mitochondria and find that the mitochondrial genome appears to experience either similar or stronger efficacy of purifying selection than the nucleus.",
keywords = "Paramecium, efficacy of purifying selection, mitochondria, mutation spectrum, recombination, telomeres",
author = "Parul Johri and Marinov, {Georgi K.} and Doak, {Thomas G.} and Michael Lynch",
year = "2019",
month = "5",
day = "1",
doi = "10.1093/gbe/evz081",
language = "English (US)",
volume = "11",
pages = "1398--1416",
journal = "Genome Biology and Evolution",
issn = "1759-6653",
publisher = "Oxford University Press",
number = "5",

}

TY - JOUR

T1 - Population Genetics of Paramecium Mitochondrial Genomes

T2 - Recombination, Mutation Spectrum, and Efficacy of Selection

AU - Johri, Parul

AU - Marinov, Georgi K.

AU - Doak, Thomas G.

AU - Lynch, Michael

PY - 2019/5/1

Y1 - 2019/5/1

N2 - The evolution of mitochondrial genomes and their population-genetic environment among unicellular eukaryotes are understudied. Ciliate mitochondrial genomes exhibit a unique combination of characteristics, including a linear organization and the presence of multiple genes with no known function or detectable homologs in other eukaryotes. Here we study the variation of ciliate mitochondrial genomes both within and across 13 highly diverged Paramecium species, including multiple species from the P. aurelia species complex, with four outgroup species: P. caudatum, P. multimicronucleatum, and two strains that may represent novel related species. We observe extraordinary conservation of gene order and protein-coding content in Paramecium mitochondria across species. In contrast, significant differences are observed in tRNA content and copy number, which is highly conserved in species belonging to the P. aurelia complex but variable among and even within the other Paramecium species. There is an increase in GC content from ∼20% to ∼40% on the branch leading to the P. aurelia complex. Patterns of polymorphism in population-genomic data and mutation-accumulation experiments suggest that the increase in GC content is primarily due to changes in the mutation spectra in the P. aurelia species. Finally, we find no evidence of recombination in Paramecium mitochondria and find that the mitochondrial genome appears to experience either similar or stronger efficacy of purifying selection than the nucleus.

AB - The evolution of mitochondrial genomes and their population-genetic environment among unicellular eukaryotes are understudied. Ciliate mitochondrial genomes exhibit a unique combination of characteristics, including a linear organization and the presence of multiple genes with no known function or detectable homologs in other eukaryotes. Here we study the variation of ciliate mitochondrial genomes both within and across 13 highly diverged Paramecium species, including multiple species from the P. aurelia species complex, with four outgroup species: P. caudatum, P. multimicronucleatum, and two strains that may represent novel related species. We observe extraordinary conservation of gene order and protein-coding content in Paramecium mitochondria across species. In contrast, significant differences are observed in tRNA content and copy number, which is highly conserved in species belonging to the P. aurelia complex but variable among and even within the other Paramecium species. There is an increase in GC content from ∼20% to ∼40% on the branch leading to the P. aurelia complex. Patterns of polymorphism in population-genomic data and mutation-accumulation experiments suggest that the increase in GC content is primarily due to changes in the mutation spectra in the P. aurelia species. Finally, we find no evidence of recombination in Paramecium mitochondria and find that the mitochondrial genome appears to experience either similar or stronger efficacy of purifying selection than the nucleus.

KW - Paramecium

KW - efficacy of purifying selection

KW - mitochondria

KW - mutation spectrum

KW - recombination

KW - telomeres

UR - http://www.scopus.com/inward/record.url?scp=85066163818&partnerID=8YFLogxK

UR - http://www.scopus.com/inward/citedby.url?scp=85066163818&partnerID=8YFLogxK

U2 - 10.1093/gbe/evz081

DO - 10.1093/gbe/evz081

M3 - Article

VL - 11

SP - 1398

EP - 1416

JO - Genome Biology and Evolution

JF - Genome Biology and Evolution

SN - 1759-6653

IS - 5

ER -