Complete Mitochondrial Genome Sequence of Three Tetrahymena Species Reveals Mutation Hot Spots and Accelerated Nonsynonymous Substitutions in Ymf Genes

Moradian, Mike M.; Beglaryan, Denis; Skozylas, Jill M.; Kerikorian, Varand

doi:10.1371/journal.pone.0000650

Cited by 31 publications

(45 citation statements)

References 49 publications

(49 reference statements)

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“…An exception to this trend was the ribosomal protein gene rpl2 , whose Ka/Ks ratio indicates a relaxed selective constraint in combination with moderate sequence divergence. In Tetrahymena , no elevated Ka/Ks ratios were observed for this gene [2,3]. In the present study, putative ORFs had significantly (2.5fold) higher Ka/Ks values compared to known protein-coding genes, indicating a lower selective pressure on those non-annotated genes.…”

Section: Discussioncontrasting

confidence: 46%

The mitochondrial genome sequence of the ciliate Paramecium caudatum reveals a shift in nucleotide composition and codon usage within the genus Paramecium

Barth

Berendonk

2011

BMC Genomics

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BackgroundDespite the fact that the organization of the ciliate mitochondrial genome is exceptional, only few ciliate mitochondrial genomes have been sequenced until today. All ciliate mitochondrial genomes are linear. They are 40 kb to 47 kb long and contain some 50 tightly packed genes without introns. Earlier studies documented that the mitochondrial guanine + cytosine contents are very different between Paramecium tetraurelia and all studied Tetrahymena species. This raises the question of whether the high mitochondrial G+C content observed in P. tetraurelia is a characteristic property of Paramecium mtDNA, or whether it is an exception of the ciliate mitochondrial genomes known so far. To test this question, we determined the mitochondrial genome sequence of Paramecium caudatum and compared the gene content and sequence properties to the closely related P. tetraurelia.ResultsThe guanine + cytosine content of the P. caudatum mitochondrial genome was significantly lower than that of P. tetraurelia (22.4% vs. 41.2%). This difference in the mitochondrial nucleotide composition was accompanied by significantly different codon usage patterns in both species, i.e. within P. caudatum clearly A/T ending codons dominated, whereas for P. tetraurelia the synonymous codons were more balanced with a higher number of G/C ending codons. Further analyses indicated that the nucleotide composition of most members of the genus Paramecium resembles that of P. caudatum and that the shift observed in P. tetraurelia is restricted to the P. aurelia species complex.ConclusionsSurprisingly, the codon usage bias in the P. caudatum mitochondrial genome, exemplified by the effective number of codons, is more similar to the distantly related T. pyriformis and other single-celled eukaryotes such as Chlamydomonas, than to the closely related P. tetraurelia. These differences in base composition and codon usage bias were, however, not reflected in the amino acid composition. Most probably, the observed picture is best explained by a hitherto unknown (neutral or adaptive) mechanism that increased the guanine + cytosine content in P. tetraurelia mtDNA on the one hand, and strong purifying selection on the ancestral amino acid composition on the other hand. These contradicting forces are counterbalanced by a considerably altered codon usage pattern.

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Section: Discussioncontrasting

confidence: 46%

The mitochondrial genome sequence of the ciliate Paramecium caudatum reveals a shift in nucleotide composition and codon usage within the genus Paramecium

Barth

Berendonk

2011

BMC Genomics

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“…The dN / dS values here were obtained for each gene under the assumption that dN / dS remains constant across the phylogeny using CODEML, PAML (Yang 2007; version 4.9a). Ciliate-specific Ymf genes therefore exhibit a relatively higher rate of evolution than other genes, with as little as 30% sequence identity between P. aurelia , P. caudatum , and P. multimicronucleatum , similar to observations in Tetrahymena (Moradian, et al 2007), as well as with higher values of π n /π s in P. tetraurelia , P. sexaurelia , P. caudatum , and P. multimicronucleatum (Supplementary Figure 10).…”

Section: Resultssupporting

confidence: 55%

Population genetics ofParameciummitochondrial genomes: recombination, mutational spectrum, and efficacy of selection

Johri

Marinov

Doak

et al. 2018

Preprint

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RUNNING TITLE: Evolution of Paramecium mitochondrial genomes. 43 44 ABSTRACT 47 The evolution of mitochondrial genomes and their population-genetic environment among 48 unicellular eukaryotes are understudied. Ciliate mitochondrial genomes exhibit a unique 49 combination of characteristics, including a linear organization and the presence of multiple 50 genes with no known function or detectable homologs in other eukaryotes. Here we study 51 the variation of ciliate mitochondrial genomes both within and across thirteen highly 52 diverged Paramecium species, including multiple species from the P. aurelia species 53 complex, with four outgroup species: P. caudatum, P. multimicronucleatum, and two strains 54 that may represent novel related species. We observe extraordinary conservation of gene 55 order and protein-coding content in Paramecium mitochondria across species. In contrast, 56 significant differences are observed in tRNA content and copy number, which is highly 57 conserved in species belonging to the P. aurelia complex but variable among and even 58 within the other Paramecium species. There is an increase in GC content from ~20% to 59 ~40% on the branch leading to the P. aurelia complex. Patterns of polymorphism in 60 population-genomic data and mutation-accumulation experiments suggest that the increase 61 in GC content is primarily due to changes in the mutation spectra in the P. aurelia species. 62Finally, we find no evidence of recombination in Paramecium mitochondria and find that 63 the mitochondrial genome appears to experience either similar or stronger efficacy of 64 purifying selection than the nucleus. 65 66 67 68 Mitochondrial genomes have played integral roles in furthering our understanding of 69 relationships among species as well as revealing population structure and demographic history.70 As a consequence, we have obtained insights into the unique population-genetic properties of 71 mitochondrial genomes. In most species, mitochondria are inherited uniparentally (but see Barr, 72 et al. 2005). Although mitochondrial genomes are known to frequently undergo recombination in 73 plants (Stadler and Delph 2002; Mackenzie 2007) as well as fungi (Fritsch, et al. 2014), no 74 recombination has been detected in animals (Ballard and Whitlock 2004; Piganeau and Eyre-75 Walker 2004). Because of the unique mode of transmission and lack of recombination in some 76 species, mitochondria have been suggested to have lower effective population sizes than their 77 nuclear counterparts and therefore to accumulate more deleterious mutations (Lynch and 78 Blanchard 1998; Neiman and Taylor 2009). In addition, mitochondrial genomes experience 79 much higher spontaneous rates of mutation than their corresponding nuclear genomes in animals, 80 but exhibit the opposite trend in plants (Lynch, et al. 2006). 81 82 Unlike the relatively uniform and conserved properties of metazoan mitochondrial genomes, 83 mitochondrial genomes in unicellular eukaryotes exhibit remarkable variation in genome 84 structure and ...

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“…This is likely due to the fact that the only available sequences of cox-1 in ciliates are those from species of the genera Paramecium and Tetrahymena. To date, only six complete ciliate mtDNA genomes are available: for Tetrahymena thermophila, Tetrahymena pyriformis, Tetrahymena paravorax, Tetrahymena malaccensis, Tetrahymena pigmentosa, and P. aurelia (9,10,46,52).…”

Section: Discussionmentioning

confidence: 99%

High-Level Genetic Diversity but No Population Structure Inferred from Nuclear and Mitochondrial Markers of the Peritrichous CiliateCarchesium polypinumin the Grand River Basin (North America)

Gentekaki

Lynn

2009

Appl Environ Microbiol

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Studies that assess intraspecific genetic variation in ciliates are few and quite recent. Consequently, knowledge of the subject and understanding of the processes that underlie it are limited. We sought to assess the degree of intraspecific genetic variation in Carchesium polypinum (Ciliophora: Peritrichia), a cosmopolitan, freshwater ciliate. We isolated colonies of C. polypinum from locations in the Grand River basin in Southwestern Ontario, Canada. We then used the nuclear markers-ITS1, ITS2, and the hypervariable regions of the large subunit rRNA-and an 819-bp fragment of the mitochondrial cytochrome c oxidase I gene (cox-1) to investigate the intraspecific genetic variation of C. polypinum and the degree of resolution of the above-mentioned markers at the population level. We also sought to determine whether the organism demonstrated any population structure that mapped onto the geography of the region. Our study shows that there is a high degree of genetic diversity at the isolate level, revealed by the mitochondrial markers but not the nuclear markers. Furthermore, our results indicate that C. polypinum is likely not a single morphospecies as previously thought.Studies of intraspecific genetic variation in macroorganisms have provided insights into microevolutionary processes and speciation in these organisms. However, our understanding of the intraspecific genetic diversity of microbial eukaryotes and its temporal and spatial distribution is neither deep nor broad due to the limited number of studies that deal with these topics (2,5,7,31).Many of the studies assessing within-species genetic variation and its distribution have used random amplified polymorphic DNA (RAPD) fingerprinting. Typically, the amount of genetic variation is very low within a species (35,36,56), with some exceptions (20, 57). However, there are several problems arising from the use of RAPDs as the sole source of data, including reproducibility and scoring concerns (54).Sequences of the internal transcribed spacers (ITS), namely, ITS1 and ITS2, of the rRNA region have also been used to study the genetic diversity and population structure of protists (2, 6, 44). In several instances, the ITS sequences of populations of ciliates from across the globe have been nearly identical, indicating very low genetic variation (4, 13, 59, 62). On the other hand, the hypervariable regions of the large subunit (LSU) rRNA have revealed moderate genetic diversity in ciliates at the population level (15, 51).Mitochondrial DNA (mtDNA) has been employed only sparingly in population studies of protists, even though it is routinely used in similar studies of metazoans (3,7,8). Of the mitochondrial genes, the apocytochrome b gene (cob) and the cytochrome c oxidase I (cox-1) gene (cox-1) have been used for population-level analyses of ciliates. Estimation of intraspecific nucleotide diversity of the cob gene from three species of the prostome ciliate Coleps showed only minor differences (5). On the other hand, the cox-1 gene revealed genetic diversity that...

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Complete Mitochondrial Genome Sequence of Three Tetrahymena Species Reveals Mutation Hot Spots and Accelerated Nonsynonymous Substitutions in Ymf Genes

Cited by 31 publications

References 49 publications

The mitochondrial genome sequence of the ciliate Paramecium caudatum reveals a shift in nucleotide composition and codon usage within the genus Paramecium

The mitochondrial genome sequence of the ciliate Paramecium caudatum reveals a shift in nucleotide composition and codon usage within the genus Paramecium

Population genetics ofParameciummitochondrial genomes: recombination, mutational spectrum, and efficacy of selection

High-Level Genetic Diversity but No Population Structure Inferred from Nuclear and Mitochondrial Markers of the Peritrichous CiliateCarchesium polypinumin the Grand River Basin (North America)

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