Adaptation of Borrelia burgdorferi to its natural hosts by synonymous codon and amino acid usage

Abstract

Lyme disease, caused by Borrelia burgdorferi, is a focally endemic tick‐transmitted zoonotic infection. In this study, the major factors underlying synonymous codon‐related amino acid usage in the B. burgdorferi genome and bias in synonymous codon usage of the translation initiation region of coding sequences were analyzed. Additionally, adaptation of B. burgdorferi to several of its hosts was analyzed in the context of synonymous codon usage. Principal component analysis (PCA) revealed that nucleotide content at the third synonymous position of a codon influenced the synonymous codon usage pattern, but the strand‐specific factor did not influence the synonymous codon usage pattern of B. burgdorferi. In terms of the low GC content of B. burgdorferi coding sequences, the effective number of codons (ENC) showed a significant correlation with GC3 content (at the synonymous position). For the amino acid usage pattern for B. burgdorferi, PCA showed that the strand‐specific factor did not contribute to this pattern, while the properties (aromaticity and hydrophobicity) of the amino acids themselves showed strong correlations with this pattern. Under‐represented codons, which were frequently selected in the translation initiation region, possibly play roles in regulating gene expression in B. burgdorferi. In terms of co‐evolution and synonymous codon usage patterns, adaptation of B. burgdorferi to different intermediate hosts was apparent to different degrees, and the degree of adaptation of this spirochete to wild animals was stronger than that of humans or mice.

Significance and roles of synonymous codon usage in the evolutionary process of Proteus

“…Even though mutation pressure derived from nucleotide composition constraint is regarded as the dominant evolutionary dynamic in evolutionary trends of Proteus spp., other evolutionary dynamics, such as natural selection and fine‐tune translation, also modify codon usage‐derived evolutionary trends in these species. In previous studies, nucleotide usage variations are considered as an evolutionary dynamic for reflecting the effects of nucleotide composition constraint on synonymous codon usage patterns for microorganisms [27,30,42–46]. The four types of nucleotide base can serve as cornerstones for evolutionary trends of different organisms.…”

Synonymous Codon Usages as an Evolutionary Dynamic for Chlamydiaceae

“…Although mutation pressure derived from nucleotide usages was identified as the dominant evolutionary dynamic in genomes of Chlamydia spp., other evolutionary dynamics, such as natural selection, also influenced codon usage patterns to modify the evolutionary trends of Chlamydia spp. In previous reports, GC3 content was regarded as a ruler, which is often used for reflecting influences of the overall nucleotide composition variations on codon usages at gene levels [31,40,41,42,43]. The four nucleotide bases are regarded as footstones for genomic organization of microorganisms, the systemic and general estimation of four nucleotide usage patterns is better than the estimation of GC3 content or AT3 content when displaying the roles of nucleotide usage patterns in formation of synonymous codon usage patterns [44,45].…”

“…Nucleotide usage variation was considered as an important evolutionary dynamic, however, synonymous codon usages were able to minimize error impacts by increasing tolerance for some point mutations to stabilize amino acid usages [26,27,28,29,30]. Investigations of synonymous codon usage identified several evolutionary dynamics which impact overall codon usage patterns, including natural/translation selection, mutation pressure, hydrophobicity and hydrophilicity of the protein, protein folding, and host preferences [31,32,33,34,35,36]. Depending on the information about nucleotide, synonymous codon, and amino acid usage from the available genomes of Chlamydia spp., we tried to identify the evolutionary dynamics in shaping the unique genetic features of these bacteria in the family of Chlamydiaceae .…”