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

Abstract

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.

Genetic Differentiation of the Mitochondrial Cytochrome Oxidase c Subunit I Gene in Genus Paramecium (Protista, Ciliophora)

“…S3 in file S3). Inconsistent sequences (FJ905146, FJ905147, EU056259, EU056258, DQ837977, DQ837982, JF741258, JF304183) are marked in red [14], [42], [47].…”

“…A number of ciliate mitochondrial genomes have now been sequenced and gene duplications are not that frequent [32], [42]–[44]. The rnl gene is duplicated in Tetrahymena spp.…”

Early evolution of eukaryote feeding modes, cell structural diversity, and classification of the protozoan phyla Loukozoa, Sulcozoa, and Choanozoa

“…However a few corticate neozoans have retained the bacterial Ccm system and did not replace it -ciliates in Chromista and unicellular red algae and streptophyte green plants in Plantae (Allen et al 2008). Some mitochondrial genomes retain yej genes coding for Ccm proteins (4 in the red alga Cyanidioschyzon (Ohta et al 1998), 3 in the jakobid Reclinomonas (Lang et al 1997) and one in Malawimonas (Lang et al 1999b) and ciliates (Barth and Berendonk 2011)), but in others all have been transferred to the nucleus (e.g. Percolozoa) or totally lost (e.g.…”

Highly Conserved Elements and Chromosome Structure Evolution in Mitochondrial Genomes in Ciliates

“…The mitochondria considered here code for tens of proteins [4,7,8,9,10,11,12,13,14,15]. The functions of some of them remain unclear, and they relatively rapidly accumulate substitutions [16].…”