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Analysis of transcriptome data reveals multifactor constraint on codon usage in Taenia multiceps.

ABSTRACT: BACKGROUND:Codon usage bias (CUB) is an important evolutionary feature in genomes that has been widely observed in many organisms. However, the synonymous codon usage pattern in the genome of T. multiceps remains to be clarified. In this study, we analyzed the codon usage of T. multiceps based on the transcriptome data to reveal the constraint factors and to gain an improved understanding of the mechanisms that shape synonymous CUB. RESULTS:Analysis of a total of 8,620 annotated mRNA sequences from T. multiceps indicated only a weak codon bias, with mean GC and GC3 content values of 49.29% and 51.43%, respectively. Our analysis indicated that nucleotide composition, mutational pressure, natural selection, gene expression level, amino acids with grand average of hydropathicity (GRAVY) and aromaticity (Aromo) and the effective selection of amino-acids all contributed to the codon usage in T. multiceps. Among these factors, natural selection was implicated as the major factor affecting the codon usage variation in T. multiceps. The codon usage of ribosome genes was affected mainly by mutations, while the essential genes were affected mainly by selection. In addition, 21codons were identified as "optimal codons". Overall, the optimal codons were GC-rich (GC:AU, 41:22), and ended with G or C (except CGU). Furthermore, different degrees of variation in codon usage were found between T. multiceps and Escherichia coli, yeast, Homo sapiens. However, little difference was found between T. multiceps and Taenia pisiformis. CONCLUSIONS:In this study, the codon usage pattern of T. multiceps was analyzed systematically and factors affected CUB were also identified. This is the first study of codon biology in T. multiceps. Understanding the codon usage pattern in T. multiceps can be helpful for the discovery of new genes, molecular genetic engineering and evolutionary studies.

SUBMITTER: Huang X

PROVIDER: S-EPMC5397707 | biostudies-literature | 2017 Apr

REPOSITORIES: biostudies-literature

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Analysis of transcriptome data reveals multifactor constraint on codon usage in Taenia multiceps.

Huang Xing X Xu Jing J Chen Lin L Wang Yu Y Gu Xiaobin X Peng Xuerong X Yang Guangyou G

BMC genomics 20170420 1

<h4>Background</h4>Codon usage bias (CUB) is an important evolutionary feature in genomes that has been widely observed in many organisms. However, the synonymous codon usage pattern in the genome of T. multiceps remains to be clarified. In this study, we analyzed the codon usage of T. multiceps based on the transcriptome data to reveal the constraint factors and to gain an improved understanding of the mechanisms that shape synonymous CUB.<h4>Results</h4>Analysis of a total of 8,620 annotated m ...[more]

PMID: 28427327

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Project description:BackgroundCodon usage bias is an important evolutionary feature in a genome and has been widely documented in many genomes. Analysis of codon usage bias has significance for mRNA translation, design of transgenes, new gene discovery, and studies of molecular biology and evolution, etc. However, the information about synonymous codon usage pattern of T. saginata genome remains unclear. T. saginata is a food-borne zoonotic cestode which infects approximataely 50 million humans worldwide, and causes significant health problems to the host and considerable socio-economic losses as a consequence. In this study, synonymous codon usage in T. saginata were examined.MethodsTotal RNA was isolated from T. saginata cysticerci and 91,487 unigenes were generated using Illumina sequencing technology. After filtering, the final sequence collection containing 11,399 CDSs was used for our analysis.ResultsNeutrality analysis showed that the T. saginata had a wide GC3 distribution and a significant correlation was observed between GC12 and GC3. NC-plot showed most of genes on or close to the expected curve, but only a few points with low-ENC values were below it, suggesting that mutational bias plays a major role in shaping codon usage. The Parity Rule 2 plot (PR2) analysis showed that GC and AT were not used proportionally. We also identified twenty-three optimal codons in the T. saginata genome, all of which were ended with a G or C residue. These results suggest that mutational and selection forces are probably driving factors of codon usage bias in T. saginata genome. Meanwhile, other factors such as protein length, gene expression, GC content of genes, the hydropathicity of each protein also influence codon usage.ConclusionsHere, we systematically analyzed the codon usage pattern and identified factors shaping in codon usage bias in T. saginata. Currently, no complete nuclear genome is available for codon usage analysis at the genome level in T. saginata. This is the first report to investigate codon biology in T. sagninata. Such information does not only bring about a new perspective for understanding the mechanisms of biased usage of synonymous codons but also provide useful clues for molecular genetic engineering and evolutionary studies.

Project description:BackgroundThe larval stage of Taenia multiceps, a global cestode, encysts in the central nervous system (CNS) of sheep and other livestock. This frequently leads to their death and huge socioeconomic losses, especially in developing countries. This parasite can also cause zoonotic infections in humans, but has been largely neglected due to a lack of diagnostic techniques and studies. Recent developments in next-generation sequencing provide an opportunity to explore the transcriptome of T. multiceps.Methodology/principal findingsWe obtained a total of 31,282 unigenes (mean length 920 bp) using Illumina paired-end sequencing technology and a new Trinity de novo assembler without a referenced genome. Individual transcription molecules were determined by sequence-based annotations and/or domain-based annotations against public databases (Nr, UniprotKB/Swiss-Prot, COG, KEGG, UniProtKB/TrEMBL, InterPro and Pfam). We identified 26,110 (83.47%) unigenes and inferred 20,896 (66.8%) coding sequences (CDS). Further comparative transcripts analysis with other cestodes (Taenia pisiformis, Taenia solium, Echincoccus granulosus and Echincoccus multilocularis) and intestinal parasites (Trichinella spiralis, Ancylostoma caninum and Ascaris suum) showed that 5,100 common genes were shared among three Taenia tapeworms, 261 conserved genes were detected among five Taeniidae cestodes, and 109 common genes were found in four zoonotic intestinal parasites. Some of the common genes were genes required for parasite survival, involved in parasite-host interactions. In addition, we amplified two full-length CDS of unigenes from the common genes using RT-PCR.Conclusions/significanceThis study provides an extensive transcriptome of the adult stage of T. multiceps, and demonstrates that comparative transcriptomic investigations deserve to be further studied. This transcriptome dataset forms a substantial public information platform to achieve a fundamental understanding of the biology of T. multiceps, and helps in the identification of drug targets and parasite-host interaction studies.

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Analysis of transcriptome data reveals multifactor constraint on codon usage in Taenia multiceps.

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Analysis of transcriptome data reveals multifactor constraint on codon usage in Taenia multiceps.

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