Evolution of Codon Usage in the Smallest Photosynthetic Eukaryotes and Their Giant Viruses

Michely, Stéphanie; Toulza, Ève; Subirana, Lucie; John, Uwe; Cognat, Valérie; Maréchal-Drouard, Laurence; Grimsley, Nigel; Moreau, Hervé; Piganeau, Gwenaël

doi:10.1093/gbe/evt053

Cited by 26 publications

(18 citation statements)

References 67 publications

Supporting

Mentioning

Contrasting

Order By: Relevance

“…The absence of ribosomal RNAs disallows the ability to use such markers in the case of most viruses, although many NCLDV families possess abundant tRNA repertoires (MICHELY et al 2013). Nonetheless, some "fourth domain" signals in specific genes of the NCLDV have been proposed (CLAVERIE 2013;WOYKE and RUBIN 2014).…”

Section: Discussionmentioning

confidence: 99%

Eukaryotic core histone diversification in light of the histone doublet and DNA topo II genes of Marseilleviridae

Erives

2015

Preprint

View full text Add to dashboard Cite

A proto-eukaryotic origin for the MV replisome 2 AbstractWhile eukaryotic and archaean genomes encode the histone fold domain, only eukaryotes encode the core histones H2A, H2B, H3, and H4. Core histones assemble into a hetero-octamer rather than the homo-tetramer of Archaea. Thus it was unexpected that core histone "doublets" were identified in the cytoplasmic replication factories of the Marseilleviridae (MV), one family of Nucleo-Cytoplasmic Large DNA Viruses (NCLDV). Here we analyze the core histone doublet genes from all known Marseilleviridae genomes and show that they encode obligate H2B-H2A and H4-H3 dimers of likely proto-eukaryotic origin. Each MV core histone moiety forms a sister clade to a eukaryotic core histone clade inclusive of canonical core histone paralogs, suggesting that MV core histone moieties diverged prior to eukaryotic neofunctionalizations associated with paired linear chromosomes and variant histone octamer assembly. We also show that all MV genomes encode a eukaryote-like DNA topoisomerase II enzyme that forms a clade that is sister to the eukaryotic clade. As DNA topo II influences histone deposition and chromatin compaction and is the second most abundant nuclear protein after histones, we suggest MV genes underlie a proto-chromatinized replisome that diverged prior to diversification of eukaryotic core histone variants. Thus, combined domain architecture and phylogenomic analyses suggest that a primitive origin for MV chromatin genes is a more parsimonious explanation than horizontal gene transfers + gene fusions + long-branch attraction constrained to each core histone clade.These results imply that core histones were utilized ancestrally in viral DNA compaction, protection from host endonucleases, and/or other unknown processes associated with NCLDVlike progenitors.

show abstract

Section: Discussionmentioning

confidence: 99%

Eukaryotic core histone diversification in light of the histone doublet and DNA topo II genes of Marseilleviridae

Erives

2015

Preprint

View full text Add to dashboard Cite

show abstract

“…For example, the tRNA genes in mimiviruses do not correspond to the codons and/or amino acids most used by these viruses 31 while the tRNA genes of prasinoviruses 32 correspond to amino acids used least by their hosts. Our comparative study of amino acid and codon usage in cluster A mycobacteriophages provides support for both hypotheses, with somewhat greater support for amino acid usage (Fig.…”

Section: Codon Versus Amino Acid Usagementioning

confidence: 99%

Testing hypotheses for the presence of tRNA genes in mycobacteriophage genomes

et al. 2016

View full text Add to dashboard Cite

The presence of tRNA genes in bacteriophages has been explained on the basis of codon usage (tRNA genes are retained in the phage genome if they correspond to codons more common in the phage than in its host) or amino acid usage (independent of codon, the amino acid corresponding to the retained tRNA gene is more common in the phage genome than in the bacterial host). The existence of a large database of sequenced mycobacteriophages, isolated on the common host Mycobacterium smegmatis, allows us to test the above hypotheses as well as explore other hypotheses for the presence of tRNA genes. Our analyses suggest that amino acid rather than codon usage better explains the presence of tRNA genes in mycobacteriophages. However, closely related phages that differ in the presence of tRNA genes in their genomes are capable of lysing the common bacterial host and do not differ in codon or amino acid usage. This suggests that the benefits of having tRNA genes may be associated with either growth in the host or the ability to infect more hosts (i.e., host range) rather than simply infecting a particular host.

show abstract

“…This phenomenon has been termed codon usage bias (CUB), and many studies support a role of natural selection in this phenomenon (Shields et al 1988; Moriyama and Hartl 1993; Akashi et al 1998; Comeron and Kreitman 1998; Chamary et al 2006; Plotkin and Kudla 2011; Waldman et al 2011; Behura et al 2013; Kober and Pogson 2013). Proposed mechanisms influencing CUB include translational efficiency (Grantham et al 1981; Ikemura 1985; Bulmer 1991; Carlini and Stephan 2003; Rocha 2004; Stoletzki and Eyre-Walker 2007; Parmley and Huynen 2009; Hense 2010; Ran and Higgs 2010, 2012; Sharp et al 2010; Behura and Severson 2011; Shah and Gilchrist 2011; Qian et al 2012; Agashe et al 2013; Lawrie et al 2013; Michely 2013), mRNA stability or folding (Moriyama and Powell 1998; dos Reis et al 2004; Chamary and Hurst 2005; Chamary et al 2006; Novoa and Ribas de Pouplana 2012; Kober and Pogson 2013; Shabalina et al 2013), transcription factor binding (Stergachis 2013), overlap with other functional elements in the genome (Lin 2011), and/or a trade-off between rapid versus accurate translation (Yang et al 2014). …”

Section: Introductionmentioning

confidence: 99%

Effective population size does not predict codon usage bias in mammals

Kessler

Dean

2014

Ecology and Evolution

View full text Add to dashboard Cite

Synonymous codons are not used at equal frequency throughout the genome, a phenomenon termed codon usage bias (CUB). It is often assumed that interspecific variation in the intensity of CUB is related to species differences in effective population sizes (Ne), with selection on CUB operating less efficiently in species with small Ne. Here, we specifically ask whether variation in Ne predicts differences in CUB in mammals and report two main findings. First, across 41 mammalian genomes, CUB was not correlated with two indirect proxies of Ne (body mass and generation time), even though there was statistically significant evidence of selection shaping CUB across all species. Interestingly, autosomal genes showed higher codon usage bias compared to X-linked genes, and high-recombination genes showed higher codon usage bias compared to low recombination genes, suggesting intraspecific variation in Ne predicts variation in CUB. Second, across six mammalian species with genetic estimates of Ne (human, chimpanzee, rabbit, and three mouse species: Mus musculus, M. domesticus, and M. castaneus), Ne and CUB were weakly and inconsistently correlated. At least in mammals, interspecific divergence in Ne does not strongly predict variation in CUB. One hypothesis is that each species responds to a unique distribution of selection coefficients, confounding any straightforward link between Ne and CUB.

show abstract

Evolution of Codon Usage in the Smallest Photosynthetic Eukaryotes and Their Giant Viruses

Cited by 26 publications

References 67 publications

Eukaryotic core histone diversification in light of the histone doublet and DNA topo II genes of Marseilleviridae

Eukaryotic core histone diversification in light of the histone doublet and DNA topo II genes of Marseilleviridae

Testing hypotheses for the presence of tRNA genes in mycobacteriophage genomes

Effective population size does not predict codon usage bias in mammals

Contact Info

Product

Resources

About