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, 12 (2)

Entomological Assessment of the Status and Risk of Mosquito-borne Arboviral Transmission in Ghana

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Entomological Assessment of the Status and Risk of Mosquito-borne Arboviral Transmission in Ghana

Michael Amoa-Bosompem et al. Viruses.

Abstract

Entomological surveillance is one of the tools used in monitoring and controlling vector-borne diseases. However, the use of entomological surveillance for arboviral infection vector control is often dependent on finding infected individuals. Although this method may suffice in highly endemic areas, it is not as effective in controlling the spread of diseases in low endemic and non-endemic areas. In this study, we examined the efficiency of using entomological markers to assess the status and risk of arbovirus infection in Ghana, which is considered a non-endemic country, by combining mosquito surveillance with virus isolation and detection. This study reports the presence of cryptic species of mosquitoes in Ghana, demonstrating the need to combine morphological identification and molecular techniques in mosquito surveillance. Furthermore, although no medically important viruses were detected, the importance of insect-specific viruses in understanding virus evolution and arbovirus transmission is discussed. This study reports the first mutualistic relationship between dengue virus and the double-stranded RNA Aedes aegypti totivirus. Finally, this study discusses the complexity of the virome of Aedes and Culex mosquitoes and its implication for arbovirus transmission.

Keywords: Aedes aegypti; Culex spp.; Ghana; cryptic species; dengue virus; insect-specific virus; mosquito virome; totivirus; virus-virus interaction.

Conflict of interest statement

The authors declare no conflict of interest.

Figures

Figure 1
Figure 1
Map of mosquito collection sites. (A) Map of Africa showing the location of Ghana (shaded region). (B) Map of Ghana showing the collection sites. The collection sites can be divided into 6 Regions (and 5 vegetations); Greater Accra Region (Coastal Savannah); Accra, Volta Region (Forest); Hohoe, Ashanti Region (Forest); Manso Nkwanta, Western Region (Wet Evergreen); Dixcove, Savannah Region (Guinea Savannah); Damongo, Larabanga and Mole National Park and Upper West Region (Guinea Savannah); Jirapa.
Figure 2
Figure 2
Relative abundance of mosquito species in the collection sites. A total of 13 different species of mosquitoes were detected across 6 regions. Aedes (Stg.) aegypti was the most widely distributed mosquito species across the collection sites. Aedes (Stg.) lilii and Aedes (Adm.) hirsutus were detected for the first time in Ghana.
Figure 3
Figure 3
Phylogenetic tree of Phasi Charoen-like Phasivirus (PCLV). Maximum likelihood tree of PCLV constructed with conserved amino acid domains in the RNA-dependent RNA polymerase (RdRp) extracted using MAFFT 7 online version [27] and the Gblocks program [28]. Bootstrap support, from 1000 bootstrap replicates, are indicated by values on the branches. The GenBank accession number of the RdRp, L segment, sequence used is LC498491.
Figure 4
Figure 4
Phylogenetic analysis of Culex flavivirus (CxFV) and cell-fusing agent virus (CFAV). MAFFT 7 online version [27] and the Gblocks program [28] were combined to extract the conserved amino acid domains in CxFV and CFAV genome sequences with Genbank accession numbers LC504568 and LC496857, respectively. The conserved domains were subsequently used in constructing a maximum likelihood phylogenetic tree, with 1000 boostraps, to determine the relationship between CxFV detected in Ghana and other known CxFV and the cell fusing agent virus clade (A). The partial nucleotide sequence of NS5 domains of CFAV (Genbank accession number LC496857) was used in determining the phylogenetic position of CFAV from Ghana in relation to previously reported CFAV strains (B). Bootstrap support, from 1000 bootstrap replicates, are indicated by values on the branches.
Figure 5
Figure 5
Genetic characterization of Odorna virus (OdV) and Cavally virus (CAVV). (A) Genome structure showing ribosomal frameshift (RFS) in the genome. (B) The maximum likelihood tree of OdV and CAVV were constructed with conserved amino acid domains in genome sequences, with Genbank accession numbers LC497422 and LC497421, respectively, extracted using MAFFT 7 online version [27] and the Gblocks program [28]. The genetic relationship between OdV, CAVV, and previously reported alphamesoniviruses were shown on the maximum likelihood tree with bootstrap support from 1000 bootstrap replicates indicated by values on branches.
Figure 6
Figure 6
Genetic characterization of West Accra virus (WAV) and Goutanap virus. (A) Genome structure of WAV showing the representation of the capsid protein on a PAGE gel. (B) Growth rate of WAV in C6/36 cells. (C) Phylogenetic relationship between WAV, Nelorpivirus, and Goutanap virus (GoNV), Sandewavirus. The maximum likelihood tree of WAV and GoNV was constructed with conserved amino acid domains in genome sequences with Genbank accession numbers LC496489 and LC504569, respectively. The conserved domains were extracted using MAFFT 7 online version [27] and the Gblocks program [28]. The bootstrap support, from 1000 bootstrap replicates, are indicated by values on the branches.
Figure 7
Figure 7
Genetic characterization of Tesano Aedes virus (TeAV). (A) Genome structure showing VPg and internal ribosome entry site (IRES) at the 5′ terminal and a poly-A tail at the 3′ terminal. (B) Genetic relationship between TeAV and other viruses of the family Iflaviridae. The maximum likelihood tree was constructed using the complete amino acid domain of the genome sequence with Genbank accession number LC496784. The amino acid domain was aligned using the MAFFT 7 online version [27]. Bootstrap support values from 1000 bootstrap replicates are indicated on the branches.
Figure 8
Figure 8
Genetic characterization of Culex permutotetra-like virus (CxPTV). (A) Genome structure showing hypothetical protein 2 as possibly coding for the capsid protein. (B) Evolutionary history of CxPTV. The maximum likelihood tree was constructed using the complete amino acid domain of the genome sequence with Genbank accession number LC505019. The amino acid domain was aligned using the MAFFT 7 online version [27]. Bootstrap support values from 1000 bootstrap replicates are indicated on the branches. (C) Gel representation of CxPTV protein.
Figure 9
Figure 9
Genetic characterization of Korle-bu Aedes virus (KoBV). (A) KoBV genome showing the predicted stop codon read through. (B) Evolutionary history of KoBV. Maximum likelihood tree constructed with the conserved amino acid domain of the genome sequence with Genbank accession number LC496785. The conserved domains were extracted using MAFFT 7 online version [27] and the Gblocks program [28]. Bootstrap support values from 1000 bootstrap replicates are indicated on the branches.
Figure 10
Figure 10
Genetic characterization of Mole Culex virus (MoCV). (A) Genome structure of MoCV showing 4 segments and an RFS in segments 3 and 4. (B) and (C) Phylogenetic analysis using the conserved non-structural (NS) domains. Maximum likelihood trees constructed using the NS3 and NS5 amino acid domains of genome sequences with Genbank accession numbers LC505052 and LC505053, respectively. The amino acid domain was aligned using the MAFFT 7 online version [27]. Bootstrap support values from 1000 bootstrap replicates are indicated on the branches.
Figure 11
Figure 11
Phylogenetic analysis of Aedes Aegypti virga-like virus (AaVV). Maximum likelihood tree constructed with the complete amino acid domain of the genome sequence with Genbank accession number LC496783. The amino acid domain was aligned using the MAFFT 7 online version [27]. Bootstrap support values from 1000 bootstrap replicates are indicated on the branches.
Figure 12
Figure 12
Phylogenetic analysis of Aedes pseudoscutellaris reovirus (APRV). Maximum likelihood tree of APRV constructed with conserved amino acid domains in the RdRp (VP2) extracted using MAFFT 7 online version [27] and the Gblocks program [28]. Bootstrap support values from 1000 bootstrap replicates are indicated on the branches. The GenBank accession number of the RdRp (L segment) sequence used is LC496849.
Figure 13
Figure 13
Genomic characterization of Aedes aegypti totivirus (AaTV). (A) Genome organization of AaTV. (B) Phylogenetic analysis of AaTV. Maximum likelihood tree of AaTV constructed with the conserved amino acid domain of the genome sequence with Genbank accession number LC496074. The conserved domains were extracted using MAFFT 7 online version [27] and the Gblocks program [28]. Bootstrap support values from 1000 bootstrap replicates are indicated on the branches.
Figure 14
Figure 14
Effect of AaTV infection in C6/36 cells on DENV growth. (A) DENV-1 growth curve [multiplicity of infection (MOI) = 0.01] (B) DENV-1 growth curve (MOI = 1). Controls were DENV infection on naïve C6/36 cells. Statistical significance was done by the t-test * = p ≤ 0.05, ** = p ≤ 0.01.

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