Evolution of Codon Usage Bias in Diatoms

• Main Authors: Marc Krasovec, Dmitry A. Filatov
• Format: Article
• Language: English
• Published: MDPI AG 2019-11-01
• Series: Genes
• Subjects: codon usage; phytoplankton evolution; diatoms; effective population size; codon bias
• Online Access: https://www.mdpi.com/2073-4425/10/11/894

Codon usage bias (CUB)&#8212;preferential use of one of the synonymous codons, has been described in a wide range of organisms from bacteria to mammals, but it has not yet been studied in marine phytoplankton. CUB is thought to be caused by weak selection for translational accuracy and efficiency. Weak selection can overpower genetic drift only in species with large effective population sizes, such as <i>Drosophila</i> that has relatively strong CUB, while organisms with smaller population sizes (e.g., mammals) have weak CUB. Marine plankton species tend to have extremely large populations, suggesting that CUB should be very strong. Here we test this prediction and describe the patterns of codon usage in a wide range of diatom species belonging to 35 genera from 4 classes. We report that most of the diatom species studied have surprisingly modest CUB (mean Effective Number of Codons, ENC = 56), with some exceptions showing stronger codon bias (ENC = 44). Modest codon bias in most studied diatom species may reflect extreme disparity between astronomically large census and modest effective population size (<i>N</i>_e), with fluctuations in population size and linked selection limiting long-term <i>N</i>_e and rendering selection for optimal codons less efficient. For example, genetic diversity (pi ~0.02 at silent sites) in <i>Skeletonema marinoi</i> corresponds to <i>N</i>_e of about 10 million individuals, which is likely many orders of magnitude lower than its census size. Still, <i>N</i>_e ~10⁷ should be large enough to make selection for optimal codons efficient. Thus, we propose that an alternative process&#8212;frequent changes of preferred codons, may be a more plausible reason for low CUB despite highly efficient selection for preferred codons in diatom populations. The shifts in the set of optimal codons should result in the changes of the direction of selection for codon usage, so the actual codon usage never catches up with the moving target of the optimal set of codons and the species never develop strong CUB. Indeed, we detected strong shifts in preferential codon usage within some diatom genera, with switches between preferentially GC-rich and AT-rich 3^rd codon positions (GC3). For example, GC3 ranges from 0.6 to 1 in most <i>Chaetoceros</i> species, while for <i>Chaetoceros dichaeta</i> GC3 = 0.1. Both variation in selection intensity and mutation spectrum may drive such shifts in codon usage and limit the observed CUB. Our study represents the first genome-wide analysis of CUB in diatoms and the first such analysis for a major phytoplankton group.