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. 2020 Apr 14;12(4):440.
doi: 10.3390/v12040440.

Identification and RNAi Profile of a Novel Iflavirus Infecting Senegalese Aedes vexans arabiensis Mosquitoes

Rhys Parry  1 , Fanny Naccache  2   3 , El Hadji Ndiaye  4 , Gamou Fall  5 , Ilaria Castelli  6 , Renke Lühken  7   8 , Jolyon Medlock  9   10 , Benjamin Cull  10 , Jenny C Hesson  11 , Fabrizio Montarsi  12 , Anna-Bella Failloux  6 , Alain Kohl  13 , Esther Schnettler  7   8   14 , Mawlouth Diallo  4 , Sassan Asgari  1 , Isabelle Dietrich  15 , Stefanie C Becker  2   3
Affiliations

Identification and RNAi Profile of a Novel Iflavirus Infecting Senegalese Aedes vexans arabiensis Mosquitoes

Rhys Parry et al. Viruses. .

Abstract

The inland floodwater mosquito Aedes vexans (Meigen, 1830) is a competent vector of numerous arthropod-borne viruses such as Rift Valley fever virus (Phenuiviridae) and Zika virus (Flaviviridae). Aedes vexans spp. have widespread Afrotropical distribution and are common European cosmopolitan mosquitoes. We examined the virome of Ae. vexans arabiensis samples from Barkédji village, Senegal, with small RNA sequencing, bioinformatic analysis, and RT-PCR screening. We identified a novel 9494 nt iflavirus (Picornaviridae) designated here as Aedes vexans iflavirus (AvIFV). Annotation of the AvIFV genome reveals a 2782 amino acid polyprotein with iflavirus protein domain architecture and typical iflavirus 5' internal ribosomal entry site and 3' poly-A tail. Aedes vexans iflavirus is most closely related to a partial virus sequence from Venturia canescens (a parasitoid wasp) with 56.77% pairwise amino acid identity. Analysis of AvIFV-derived small RNAs suggests that AvIFV is targeted by the exogenous RNA interference pathway but not the PIWI-interacting RNA response, as ~60% of AvIFV reads corresponded to 21 nt Dicer-2 virus-derived small RNAs and the 24-29 nt AvIFV read population did not exhibit a "ping-pong" signature. The RT-PCR screens of archival and current (circa 2011-2020) Ae. vexans arabiensis laboratory samples and wild-caught mosquitoes from Barkédji suggest that AvIFV is ubiquitous in these mosquitoes. Further, we screened wild-caught European Ae. vexans samples from Germany, the United Kingdom, Italy, and Sweden, all of which tested negative for AvIFV RNA. This report provides insight into the diversity of commensal Aedes viruses and the host RNAi response towards iflaviruses.

Keywords: Aedes vexans; RNAi; iflavirus; virus discovery.

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Conflict of interest statement

The authors declare no conflict of interest. The funders had no role in the design of the study; in the collection, analyses, or interpretation of data; in the writing of the manuscript, or in the decision to publish the results.

Figures

Figure 1
Figure 1
Genome organization of Aedes vexans iflavirus (AvIFV) and mapping coverage. (A) Genome organization schematic of AvIFV with dotted lines indicating conserved 3C-protease cleavage sites inferred by amino acid alignment and conserved protease consensus sites. The VP1 region corresponds to a calicivirus coat domain (PF00915), and VP3 corresponds to Cricket paralysis virus capsid (PF08762) domain. HEL corresponds to predicted RNA helicase domain (PF00910), 3C-Pro corresponds to 3C/3C-like protease domain, and RdRP corresponds to the RNA-dependent RNA polymerase domain (PF00680). Diagonal striped lines indicate predicted transmembrane domains. internal ribosome entry site (IRES) of 5’UTR (Figure S2). (B) Mapping coverage of AvIFV genome 18–44 nt trimmed reads re-mapped to both genome and anti-genome orientation of the AvIFV genome.
Figure 2
Figure 2
Maximum clade credibility tree of AvIFV within the Picornavirales order. Phylogenetic inferences were calculated using Bayesian evolutionary analysis sampling trees (BEAST v2.5.1) with polyprotein alignments using the Whelan and Goldman protein substitution model with a chain length of 10 × 106. A black arrowhead indicates AvIFV and Genbank accession number is in parentheses. Putative viruses identified in the Transcriptome Shotgun Assembly are labelled in blue. The tree is rooted arbitrarily on the Picornaviridae outgroup. Branch length indicates the number of substitutions per site.
Figure 3
Figure 3
Virus-derived small RNAs derived from AvIFV replication in adult Ae. vexans arabiensis mosquitoes. (A) Profile of nucleotide lengths of virus-derived small RNAs mapped to the AvlFV genome. (B) Profile of 21 nt virus-derived short interfering RNAs and (C) virus-derived piRNA reads (24–29 nt) mapped to the AvIFV genome (blue) and anti-genome (red). (D) AvIFV does not produce vpiRNAs with the characteristic piRNA signature (adenine at position 10, A10, for sense RNA; upper panel and Uridine at position 1, U1 for antisense RNA; lower panel).
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