Nucleotide and codon usage biases involved in the evolution of African swine fever virus: A comparative genomics analysis

Pu, Feiyang; Wang, Rui; Yang, Xuanye; Hu, Xinyan; Wang, Jinqian; Zhang, Lijuan; Zhao, Yongqing; Zhang, Derong; Liu, Zewen; Liu, Junlin

doi:10.1002/jobm.202200624

Cited by 8 publications

(3 citation statements)

References 139 publications

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“…AT bias was observed in all the six genes irrespective of clade, which is consistent with a previous report [52]. Noteworthy is the strong AT bias but weak selective pressure in EP153R, which is consistent with prior observations that natural selection derived from host-dependent selection is important for the removal of CG dinucleotides from viral genomes [53][54][55], while also suggesting differences, especially at the gene level.…”

Section: Discussionsupporting

confidence: 91%

The evolutionary and genetic patterns of African swine fever virus

Cho,

Min,

Been

et al. 2023

Preprint

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Background: African swine fever (ASF) is a serious animal disease, and has spread to Africa, Europe and Asia, causing massive economic losses. African swine fever virus (ASFV) is transmitted from a reservoir host (warthog) to domestic pigs via a sylvatic cycle (transmission between warthogs and soft ticks) and a domestic cycle (transmission between domestic pigs) and survives by expressing a variety of genes related to virus–host interactions. Methods: We evaluated differences in codon usage patterns among ASFV genotypes and clades and explored the common and specific evolutionary and genetic characteristics of ASFV sequences. We analysed the evolutionary relationships, nucleotide compositions, codon usage patterns, selection pressures (mutational pressure and natural selection) and viral adaptation to host codon usage based on the coding sequences (CDS) of key functional genes of ASFV. Results: AT bias was detected in the six genes analysed, irrespective of clade. The AT bias of genes (A224L, A179L, EP153R) encoding proteins involved in interaction with host cells after infection was high; among them, the AT bias of EP153R was the greatest at 78.3%. A large number of overrepresented codons were identified in EP153R, whereas there were no overrepresented codons with a relative synonymous codon usage (RSCU) value of ≥ 3 in B646L. In most genes, the pattern of selection pressure was similar for each clade, but in EP153R, diverse patterns of selection pressure were captured within the same clade and genotype. As a result of evaluating host adaptation based on the codon adaptation index (CAI), for B646L, E183L, CP204Land A179L, the codon usage patterns in all sequences were more similar to tick than domestic pig or wild boar. However, EP153R showed the lowest average CAI value of 0.52 when selecting tick as a reference set. Conclusions: The genes analysed in this study showed different magnitudes of selection pressure at the clade and genotype levels, which is likely to be related to the function of the encoded proteins and may determine key evolutionary traits of viruses, such as the level of genetic variation and host range. The diversity of codon adaptations at the genetic level in ASFV may account for differences in translational selection in ASFV hosts and provides insight into viral host adaptation and co‑evolution.

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Section: Discussionsupporting

confidence: 91%

The evolutionary and genetic patterns of African swine fever virus

Cho,

Min,

Been

et al. 2023

Preprint

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“…The PR2 diagram illustrates an imbalance in the frequencies of A3, U3, G3 and C3 codons in ASFV, indicating that natural selection plays a significant role in moulding the virus’s codon preferences. Furthermore, analysis using ENC and neutral plots supports the notion that factors beyond mutation pressure contribute to ASFV’s codon usage patterns, aligning with previous research findings [ 53 ]. The neutrality plot analysis also indicated that natural selection and mutation pressure both participate in ASFV CUB.…”

Section: Discussionsupporting

confidence: 86%

Systematic analysis of the codon usage patterns of African swine fever virus genome coding sequences reveals its host adaptation phenotype

Wang,

Chi,

Zhang

et al. 2024

Microbial Genomics

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African swine fever (ASF) is a severe haemorrhagic disease caused by the African swine fever virus (ASFV), transmitted by ticks, resulting in high mortality among domestic pigs and wild boars. The global spread of ASFV poses significant economic threats to the swine industry. This study employs diverse analytical methods to explore ASFV’s evolution and host adaptation, focusing on codon usage patterns and associated factors. Utilizing phylogenetic analysis methods including neighbour-joining and maximum-likelihood, 64 ASFV strains were categorized into four clades. Codon usage bias (CUB) is modest in ASFV coding sequences. This research identifies multiple factors – such as nucleotide composition, mutational pressures, natural selection and geographical diversity – contributing to the formation of CUB in ASFV. Analysis of relative synonymous codon usage reveals CUB variations within clades and among ASFVs and their hosts. Both Codon Adaptation Index and Similarity Index analyses confirm that ASFV strains are highly adapted to soft ticks (Ornithodoros moubata) but less so to domestic pigs, which could be a result of the long-term co-evolution of ASFV with ticks. This study sheds light on the factors influencing ASFV’s codon usage and fitness dynamics, enriching our understanding of its evolution, adaptation and host interactions.

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“…The GC content (35.95%) characterizes ASFV as an AT-rich DNA virus. ASFV's preference for using AT nucleotides over GC nucleotides in all its coding sequences has been observed in a comparative genomics analysis of ASFV (Pu et al, 2023). Other viruses with a similar AT nucleotide composition include Hantaan viruses (Ata et al, 2021), Hepadnaviridae (Deb et al, 2020), Flaviviridae (Yao et al, 2019), lyssaviruses (Zhang et al, 2018), PEDV (Chen et al, 2014), PDCoV (He et al, 2019), and SARS-CoV-2 (Hou, 2020).…”

Section: Discussionmentioning

confidence: 94%

Comprehensive codon usage analysis of the African Swine Fever Virus

Kanyema,

Cheng,

Luo

et al. 2023

Acta Virol.

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The non-uniform usage of synonymous codons occurs in genomes of all organisms, including DNA and RNA viruses. The preferential selection of a codon at the expense of other synonymous codons within the same group is known as Codon Usage Bias. The understanding of this bias assists in unveiling the factors driving molecular evolution, as defined by the selection-mutation-drift theory. According to this model, molecular evolution is predominantly driven by mutation, natural selection, and genetic drift. Nevertheless, elements like nucleotide composition, gene length, and protein secondary structure also contribute to this process. Comprehensive genomic analyses that highlight the codon usage preference of the African Swine Fever Virus (ASFV) are infrequent. ASFV, a hemorrhagic and highly contagious viral disease, almost invariably results in 100% fatality among infected pigs and wild boars. This study, therefore, embarked on a thorough examination of codon usage patterns in ASFV’s complete genomic sequences, an endeavor of great relevance to molecular evolution studies, complex transmission models, and vaccine research. For an exhaustive evaluation of ASFV’s whole-genome codon usage, we used parameters like ENC, RSCU, and CAI. A Principal Component Analysis was carried out to reaffirm the interconnected RSCU lineages based on the continent, and their evolutionary relationships were later elucidated through phylogenetic tree construction. ASFV emerged as a low-biased codon user (ENC = 52.8) that is moderately adapted to its host. Its genome has a high AT composition (64.05%), suggesting the impact of mutational pressure on genomic evolution. However, neutrality plot analysis revealed natural selection’s slight supremacy over mutational pressure. The low codon bias (>45) implies ASFV’s diverse usage of synonymous codons within a given codon family, allowing for effective translation and subsequent successful viral replication cycles. Its moderate adaptation (CAI = 0.56) permits the virus to infect a range of hosts, including reservoirs such as warthogs and bush pigs. To the best of our knowledge, this is the pioneering report providing a comprehensive examination of ASFV’s complete genomic sequences. Consequently, research focusing on viral gene expression and regulation, gene function prediction, parasite-host interaction, immune dysfunction, and drug and vaccine design may find this report to be a valuable resource.

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Nucleotide and codon usage biases involved in the evolution of African swine fever virus: A comparative genomics analysis

Cited by 8 publications

References 139 publications

The evolutionary and genetic patterns of African swine fever virus

The evolutionary and genetic patterns of African swine fever virus

Systematic analysis of the codon usage patterns of African swine fever virus genome coding sequences reveals its host adaptation phenotype

Comprehensive codon usage analysis of the African Swine Fever Virus

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