Abstract

Codon usage bias (CUB)—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 Drosophila 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 (Ne), with fluctuations in population size and linked selection limiting long-term Ne and rendering selection for optimal codons less efficient. For example, genetic diversity (pi ~0.02 at silent sites) in Skeletonema marinoi corresponds to Ne of about 10 million individuals, which is likely many orders of magnitude lower than its census size. Still, Ne ~107 should be large enough to make selection for optimal codons efficient. Thus, we propose that an alternative process—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 3rd codon positions (GC3). For example, GC3 ranges from 0.6 to 1 in most Chaetoceros species, while for Chaetoceros dichaeta 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.

Highlights

  • The redundancy of the genetic code is due to multiple codons which encode the same amino acid

  • Escherichia coli in 1980 revealed that more actively expressed genes have stronger codon usage bias (CUB) [3]—a finding that was later confirmed in Drosophila and other species [4]

  • The extent of codon bias is often measured with the Effective Number of Codons (ENC [43]) which ranges from

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Summary

Introduction

The redundancy of the genetic code is due to multiple codons which encode the same amino acid. The usage of synonymous codons is non-random in most organisms studied so far, with one of the codons being used preferentially—the so-called codon usage bias (CUB) [1,2]. The extent of CUB varies between species and among genes in the same genome. Escherichia coli in 1980 revealed that more actively expressed genes have stronger CUB [3]—a finding that was later confirmed in Drosophila and other species [4]. The debate about the causes of CUB has favored two selective explanations—translational accuracy [5,6,7] and efficiency [8,9], though biases in underlying mutational patterns can affect or mask CUB [10].

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