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. 2024 Jan 23;12(2):239.
doi: 10.3390/microorganisms12020239.

Untranslated Regions of a Segmented Kindia Tick Virus Genome Are Highly Conserved and Contain Multiple Regulatory Elements for Viral Replication

Anastasia A Tsishevskaya  1   2 , Daria A Alkhireenko  1   3 , Roman B Bayandin  1 , Mikhail Yu Kartashov  1 , Vladimir A Ternovoi  1 , Anastasia V Gladysheva  1
Affiliations

Untranslated Regions of a Segmented Kindia Tick Virus Genome Are Highly Conserved and Contain Multiple Regulatory Elements for Viral Replication

Anastasia A Tsishevskaya et al. Microorganisms. .

Abstract

Novel segmented tick-borne RNA viruses belonging to the group of Jingmenviruses (JMVs) are widespread across Africa, Asia, Europe, and America. In this work, we obtained whole-genome sequences of two Kindia tick virus (KITV) isolates and performed modeling and the functional annotation of the secondary structure of 5' and 3' UTRs from JMV and KITV viruses. UTRs of various KITV segments are characterized by the following points: (1) the polyadenylated 3' UTR; (2) 5' DAR and 3' DAR motifs; (3) a highly conserved 5'-CACAG-3' pentanucleotide; (4) a binding site of the La protein; (5) multiple UAG sites providing interactions with the MSI1 protein; (6) three homologous sequences in the 5' UTR and 3' UTR of segment 2; (7) the segment 2 3' UTR of a KITV/2017/1 isolate, which comprises two consecutive 40 nucleotide repeats forming a Y-3 structure; (8) a 35-nucleotide deletion in the second repeat of the segment 2 3' UTR of KITV/2018/1 and KITV/2018/2 isolates, leading to a modification of the Y-3 structure; (9) two pseudoknots in the segment 2 3' UTR; (10) the 5' UTR and 3' UTR being represented by patterns of conserved motifs; (11) the 5'-CAAGUG-3' sequence occurring in early UTR hairpins. Thus, we identified regulatory elements in the UTRs of KITV, which are characteristic of orthoflaviviruses. This suggests that they hold functional significance for the replication of JMVs and the evolutionary similarity between orthoflaviviruses and segmented flavi-like viruses.

Keywords: Flaviviridae; Jingmenvirus group; Kindia tick virus; RNA structure; flavi-like virus; ixodid ticks; orthoflavivirus; phylogenetics; segmented virus; untranslated region.

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Conflict of interest statement

The authors declare no conflicts of interest.

Figures

Figure 1
Figure 1
Phylogenetic analysis of tick-borne flavi-like viruses with a segmented genome according to the nucleotide sequence ORF of the all segments. (A) Phylogenetic analysis of the ORF nucleotide sequence encoding RNA-dependent RNA polymerase. (B) Phylogenetic analysis of the ORF nucleotide sequence encoding VP1. (C) Phylogenetic analysis of the ORF nucleotide sequence encoding the NS3 viral protein. (D) Phylogenetic analysis of the ORF nucleotide sequence encoding VP2. (E) Phylogenetic analysis of the ORF nucleotide sequence encoding VP3.
Figure 2
Figure 2
Linear models of the secondary structure of 5′ UTR (a) and 3′ UTR (b) of genomic RNA segment 1 of the KITV isolate KITV/2018/1. Functional orthoflavivirus regions are indicated by colored arrows.
Figure 3
Figure 3
Linear models of the secondary structure of 5′ UTR and 3′ UTR of genomic RNA segment 2 of KITV (a). 5′ UTR of the KITV/2018/1 isolate (b). 3′ UTR of the KITV/2018/1 isolate. (c). 3′ UTR of the KITV/2018/2 isolate (d). 3′ UTR of the KITV/2017/1 isolate. The complementary sequences in 5′ and 3′ UTR are highlighted with colored circles. Homologous sequences in 5′ and 3′ UTR are designated as R1, R2, R3.
Figure 4
Figure 4
Linear model of the secondary structure of the 5′ UTR of genomic RNA segment 3 of the KITV/2018/1 isolate. Functional orthoflavivirus regions are indicated by colored arrows.
Figure 5
Figure 5
Linear models of the secondary structure of 5′ UTR (a) and 3′ UTR (b) of genomic RNA segment 4 of the KITV isolate KITV/2018/1. Functional orthoflavivirus regions are indicated by colored arrows.
Figure 6
Figure 6
Conservative motifs in 5′ UTR segmented flavi-like viruses. (a). Nucleotide sequences of motifs and their location in the 5′ UTR of segment 1 of segmented flavi-like viruses. A highly conservative area is highlighted in motif 2. (b). Nucleotide sequences of motifs and their location in the 5′ UTR of segment 2 of segmented flavi-like viruses. A highly conservative area is highlighted in motif 3. (c). Nucleotide sequences of motifs and their location in the 5′ UTR of segment 3 of segmented flavi-like viruses. A highly conservative area is highlighted in motifs 1 and 4. (d). Nucleotide sequences of motifs and their location in the 5′ UTR of segment 4 of segmented flavi-like viruses. A highly conservative area is highlighted in motif 3. The size of the bases correlates with the conservation of their detection among different JMV isolates. Complete date are presented in Figures S8–S11.
Figure 7
Figure 7
Conservative motifs in 3′ UTR segmented flavi-like viruses. (a). Nucleotide sequences of motifs and their location in the 3′ UTR of segment 1 of segmented flavi-like viruses. A highly conservative area is highlighted in motif 4. (b). Nucleotide sequences of motifs and their location in the 3′ UTR of segment 2 of segmented flavi-like viruses. A highly conservative area is highlighted in motif 4. (c). Nucleotide sequences of motifs and their location in the 3′ UTR of segment 4 of segmented flavi-like viruses. A highly conservative area is highlighted in motif 4. The size of the bases correlates with the conservation of their detection among different JMV isolates. Complete date are presented in the Figures S12–S14.
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