Codon usage bias and environmental adaptation in microbial organisms

Andrea Giansanti,Davide Arella,Maddalena Dilucca

doi:10.1007/s00438-021-01771-4

Andrea Giansanti, Davide Arella + Show 1 more

Open Access

https://doi.org/10.1007/s00438-021-01771-4

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Abstract

In each genome, synonymous codons are used with different frequencies; this general phenomenon is known as codon usage bias. It has been previously recognised that codon usage bias could affect the cellular fitness and might be associated with the ecology of microbial organisms. In this exploratory study, we investigated the relationship between codon usage bias, lifestyles (thermophiles vs. mesophiles; pathogenic vs. non-pathogenic; halophilic vs. non-halophilic; aerobic vs. anaerobic and facultative) and habitats (aquatic, terrestrial, host-associated, specialised, multiple) of 615 microbial organisms (544 bacteria and 71 archaea). Principal component analysis revealed that species with given phenotypic traits and living in similar environmental conditions have similar codon preferences, as represented by the relative synonymous codon usage (RSCU) index, and similar spectra of tRNA availability, as gauged by the tRNA gene copy number (tGCN). Moreover, by measuring the average tRNA adaptation index (tAI) for each genome, an index that can be associated with translational efficiency, we observed that organisms able to live in multiple habitats, including facultative organisms, mesophiles and pathogenic bacteria, are characterised by a reduced translational efficiency, consistently with their need to adapt to different environments. Our results show that synonymous codon choices might be under strong translational selection, which modulates the choice of the codons to differently match tRNA availability, depending on the organism’s lifestyle needs. To our knowledge, this is the first large-scale study that examines the role of codon bias and translational efficiency in the adaptation of microbial organisms to the environment in which they live.

Highlights

Following a quite shared view, microbial evolution is mainly driven by the adaptation to the environment (see, e.g. the nice database paper from Yana Bromberg’s lab (Zhu et al 2018)
The above quoted literature suggested the present investigation in which we explore whether lifestyles and habitats of microbial species are correlated with their codon bias, tRNA availability and an index that can be reasonably associated to their efficiency in producing proteins
Previous observations pointed to the fact that each bacterial species has a specific pattern of codon usage bias (CUB), Fig. 1 Heat map of relative synonymous codon usage (RSCU) values for each gene of E. coli strain K12 substrain MG1655

Summary

Introduction

Following a quite shared view, microbial evolution is mainly driven by the adaptation to the environment (see, e.g. the nice database paper from Yana Bromberg’s lab (Zhu et al 2018). The choice of preferred codons in a single genome is closely correlated with abundance of the cognate tRNA molecules (Bennetzen and Hall 1982; Ikemura 1981, 1985; Dong et al 1996) and further influenced by the genome’s GC content (Chen et al 2004; Hershberg and Petrov 2009) It was argued by Andersson and Kurland (1990) and substantiated by Kudla and his group (Kudla et al 2009) that selection towards highly adapted codons in highly expressed proteins has a global effect on the cell, resulting in an increased cellular fitness. Our observations reinforce the interpretation of the codon bias that emerges from the evolution of a microbial species as the result of multiple trade-offs between translation efficiency, biosynthetic costs, and varied availability of nutrients typical of different environments

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