Abstract
Genomic tRNA copy numbers determine cytoplasmic tRNA abundances, which in turn influence translation efficiency, but the underlying mechanism is not well understood. Using the sea cucumber Apostichopus japonicus as a model, we combined genomic sequence, transcriptome expression and ecological food resource data to study its codon usage adaptation. The results showed that, unlike intragenic non-coding RNAs, transfer RNAs (tRNAs) tended to be transcribed independently. This may be attributed to their specific Pol III promoters that lack transcriptional regulation, which may underlie the correlation between genomic copy number and cytoplasmic abundance of tRNAs. Moreover, codon usage optimization was mostly restrained by a gene's amino acid sequence, which might be a compromise between functionality and translation efficiency for stress responses were highly optimized for most echinoderms, while enzymes for saponin biosynthesis (LAS, CYPs and UGTs) were especially optimized in sea cucumbers, which might promote saponin synthesis as a defence strategy. The genomic tRNA content of A. japonicus was positively correlated with amino acid content in its natural food particles, which should promote its efficiency in protein synthesis. We propose that coevolution between genomic tRNA content and codon usage of sea cucumbers facilitates their saponin synthesis and survival using food resources with low nutrient content.
Highlights
As adaptors that link amino acids to codons in messenger RNAs, transfer RNAs are a fundamental component of the translation machinery. tRNAs constitute up to 10% of all cellular RNA, making them the most abundant small non-coding RNAs [1]
Our analyses revealed that codon usage of enzymes catalysing saponin biosynthesis, the immune response to a stimulus and digestion was especially optimized for efficient translation
The genomic tRNA content of A. japoni- 2 cus was highly correlated with amino acid content in its natural food particles, which should help it to survive on marine debris with a very low nutritional content
Summary
As adaptors that link amino acids to codons in messenger RNAs (mRNAs), transfer RNAs (tRNAs) are a fundamental component of the translation machinery. tRNAs constitute up to 10% of all cellular RNA, making them the most abundant small non-coding RNAs (ncRNAs) [1]. TRNAs constitute up to 10% of all cellular RNA, making them the most abundant small non-coding RNAs (ncRNAs) [1] They outnumber other ncRNAs in terms of genomic loci, with copy numbers up to thousands in a single species [2]. Unlike most other ncRNAs or coding genes, the cellular concentrations of tRNAs are highly correlated with their genomic copy numbers [4,5,6]. Because differential translational efficiency can play key roles in phenotypic divergence, especially in the divergence of metabolic style [4], information about adaptation between codon usage and tRNA gene content would be indispensable for understanding the metabolic characteristics of sea cucumbers and other echinoderms. We surveyed tRNA genes in the recently published A. japonicus genome and analysed their correlation with codon usage in transcriptome data and amino acid content in the sea cucumber’s natural food particles. The genomic tRNA content of A. japoni- 2 cus was highly correlated with amino acid content in its natural food particles, which should help it to survive on marine debris with a very low nutritional content
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