Leveraging transcriptome SRAs for virus detection in wild and colony populations of triatomines (Hemiptera: Reduviidae: Triatominae)

doi:10.21203/rs.3.rs-4870255/v1

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Research Article

Leveraging transcriptome SRAs for virus detection in wild and colony populations of triatomines (Hemiptera: Reduviidae: Triatominae)

https://doi.org/10.21203/rs.3.rs-4870255/v1

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published 04 Oct, 2024

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Triatomines are infamous as vectors of the parasite Trypanosoma cruzi, the causative agent of Chagas disease. However, climate-driven range expansion and urbanization adaptation of Triatomine populations coupled with their highly diverse feeding strategies (vertebrate haematophagy, kleptohaematophagy, and coprophagy) and has elevated interest in Triatomines as potential arboviral vectors. Information on the Triatomine virome is highly scant, with prior records including only eight insect-specific viruses: Triatoma virus (TrV) and Rhodnius prolixus viruses 1–7. Here we leverage publicly available transcriptome datasets to assess viral diversity in 122 wild and colony kissing bugs representing eight species from six countries.

In total, six viruses were detected (including Rhodnius prolixus viruses 4–6), and TrV was detected in almost half of all screened Triatomines. TrV is reported in Triatoma brasiliensis and in the genus Mepraia (M. gajardoi, M. spinolai, M. parapatrica) for the first time, and this effort has vastly expanded the publicly available genomic resources of TrV, adding 39 genomes to the single genome currently available on GenBank. Furthermore, two additional viruses—Meccus longipennis virus 1 and Drosophila melanogaster Nora virus—are herein reported from kissing bugs for the first time. Meccus longipennis virus 1 was detected in Triatoma infestans from Argentina, Brazil, Chile, and Peru, and Drosophila melanogaster Nora virus was found in T. infestans from Argentina. Our results illustrate the advantage and utility of low-cost transcriptome data mining for the discovery of known and novel arboviruses in Triatomines, and other potential insect vectors.

Triatomines

pathogens

virus

transcriptome

Triatomines (subfamily Triatominae) are a highly diverse subfamily of hematophagous insects [1], which feed on a variety of vertebrates [2]. The group is particularly important from the perspective of public health, due to its members being the sole vectors of the parasite Trypanosoma cruzi, the causative agent of Chagas disease. With the Triatominae’s largely Neotropical distribution, the majority of Chagas disease cases occur in the Americas, affecting approximately 6 million people and causing an average of 12,000 deaths each year [3].

Central to global efforts to prevent and control Chagas disease has been mitigating vector-borne transmission. To this end, considerable efforts have been made to understand the ecology, life history, physiology, immunology, and evolutionary biology of the Triatominae vectors, using both wild populations and laboratory colonies. In more recent years, studies of Triatominae microbiomes have provided important insights into microbial diversity, immune defense, and vectorial capacity [4–6]. However, few studies have been undertaken to explicitly explore the viral diversity present in this group. Until recently, only a single viral species, Triatoma virus (TrV) (Dicistroviridae: Cripavirus) was identified from Triatominae. Initially discovered in a laboratory colony of T. infestans from Argentina [7, 8], TrV has since been detected by RT-PCR in variety of Triatoma species, as well as Rhodnius prolixus [9]. It has also been found naturally infecting Triatoma breyeri, T. delpontei, T. guasayana, T. infestans, T. platensis, T. sordida, and Psammolestes coreodes [10–13]. TrV infection has been shown to increase insect mortality, reduce productivity, and inhibit molting, all characteristics that can be leveraged for vector population control [14, 15]. More recently, an unclassified unclassified Riboviria group, comprising Rhodnius prolixus viruses 1–7 (RpV1–7), was characterized from a Brazilian laboratory in colony of R. prolixus via de-novo transcriptome assembly [16]. In addition to Dicistroviridae, viruses belonging to diverse families or groups including Iflaviridae and Rhabdoviridae, have been identified in other hemipterans such as aphids (Aphidoidea), leafhoppers (Cicadellidae), psyllids (Psyllidae) and stinkbugs (Pentatomidae) [17].

The current study leverages 122 Triatominae transcriptome datasets available on publicly available repositories such as the Sequence Read Archive (SRA) and the European Nucleotide Archive (ENA) for an exploration of the viromes present in this subfamily. This provides a unique opportunity to expand on the limited molecular resources currently available for TrV and RpV1–7, and potentially characterize other novel and/ or emerging viruses in Triatominae species.

Data downloads and processing

All available Triatominae single and paired-end illumina transcriptome data from the SRA and the ENA repositories were analyzed to identify and characterize viruses present within this subfamily (Table S1). The available transcriptome data totalled 122 samples, comprising 66 laboratory colony samples and 56 wild population samples from six countries (Argentina, Bolivia, Brazil, Chile, French Guiana and Peru). These data were first adaptor trimmed and quality filtered using fastp v0.23.3 (--qualified_quality_phred = 15; --unqualified_percent_limit = 40) [18, 19].

Read taxonomic classification

Kraken2 [20] was used to provide a preliminary taxonomic classification of the cleaned reads. This tools classified reads against the NCBI nt database, with the confidence threshold set to 0.2. Kraken reports were viewed using Pavian [21]. For each sample, reads that were taxonomically classified to viral families were then extracted from the cleaned Illumina® reads using the extract_kraken_reads.py script available from KrakenTools [22]. Those viruses that did not have a NCBI taxonomy assignment at the level of family were extracted at the next highest taxonomic rank.

De novo assembly

The candidate viral target reads from each sample were then used for de novo assembly using Spades v3.15.5 [23], with the metagenomic data (--meta) turned on and making input adjustments for single and paired end reads. The resulting de novo assembled contigs that mapped to target reference genomes using minimap2 [24] and the long assembly preset (-x asm20) were retained for downstream analyses. Contigs with identical overlapping regions were merged in AliView [25].

To explore any additional viral novelty, the full dataset of cleaned reads were also de novo assembled, and the assembled contigs were aligned to the National Center for Biotechnology Information (NCBI) protein non-redundant (nr) database using Diamond v2.1.9 (--long-reads; --evalue 1e-6) [26] and taxonomically classified using Megan v6.24.20 (--minSupport 1; --minPercentIdentity 70; --maxExpected 1.0E-6; --lcaAlgorithm longReads; --lcaCoveragePercent 51; --longReads) [27].

Phylogenetic analysis

Putative Open Reading Frames (ORFs) and amino acid sequences were predicted using ORF finder (https://www.ncbi.nlm.nih.gov/orffinder). ORFs were then aligned by amino acid with congeneric relatives, listed in the International Committee on Taxonomy of Viruses (ICTV) report chapters (https://ictv.global/report), using the muscle algorithm [28] implemented in SeaView v5.0.5 [29]. The removal of spurious and/or poorly aligned regions from the multiple sequence alignment was achieved using trimAl v1.4 [46] using the automated heuristic approach (option-automated1).

To explore phylogenetic relationships between assembled genomes and near relatives, maximum likelihood phylogenetic analysis was performed in IQ-TREE 2 v2.2.0 [30] with 1,000 replicates. Optimal model selection was performed using the -m MFP option, and the models were restricted to those designed for viruses using the -msub viral option. The resulting consensus trees are shown with UFBoot support values, providing less biased values than standard nonparametric bootstrap, with clade support considered at ≥ 95%. Pairwise sequence distances were expressed as p-distances i.e. proportion of different nucleotide sites between two sequences, as calculated in MEGA [31].

Our assembly approach recovered a total of six viruses in the 122 transcriptome datasets, all of which are insect-specific. These included Meccus longipennis virus 1 (MlV1) and Drosophila melanogaster Nora virus (NV)— that have never previously been reported in Triatomine bugs— and the previously reported TrV and Rhodnius prolixus viruses RpV4, RpV5 and RpV6 (Table 1). No additional viral novelty or improved genome assembly was achieved by de novo assembly of the full clean read datasets.

Table 1

Description of viruses detected in transcriptome data from the Sequence Read Archive (SRA) and the European Nucleotide Archive (ENA) used in this study. Species in bold represent new host records. Asterisks (*) represent new country records for wild populations.
Virus	Host species	Wild/laboratory host population country	Laboratory colony SRAs	Wild population SRAs
Triatoma virus	Mepraia gajardoi	Chile	-	3*
	Mepraia spinolai	Chile	-	4*
	Mepraia parapatrica	Chile	-	1*
	Triatoma brasiliensis	Brazil	-	1*
	Triatoma infestans	Argentina	24	-
	Triatoma infestans	Bolivia	4	7*
	Triatoma infestans	Chile	2	-
	Triatoma infestans	Peru	2	-
	Rhodnius neglectus	Brazil	11	-
	Rhodnius prolixus	Brazil	1	-
Meccus longipennis virus 1	Triatoma infestans	Argentina	2	-
	Triatoma infestans	Bolivia	4	7*
	Triatoma infestans	Chile	2	-
	Triatoma infestans	Peru	1	-
D. melanogaster Nora virus	Triatoma infestans	Argentina	2	-
Rhodnius prolixus virus 4	Rhodnius robustus	French Guiana	1	-
Rhodnius prolixus virus 5	Rhodnius robustus	French Guiana	-	1*
Rhodnius prolixus virus 6	Rhodnius neglectus	Brazil	1	-
	Rhodnius robustus	French Guiana	-	1*

Triatoma Virus (TrV)

TrV is highly prevalent, being detected in almost half of all SRA samples analyzed (49.2%, 60/122). Most of the TrV positives came from laboratory colonies (73.3%, 44/60) and from T. infestans hosts (65%, 39/60). However, TrV was also detected in T. brasiliensis, R. prolixus, R. neglectus, and three Mepraia species – M. gajardoi, M. spinolai, M. parapatrica (Table 1).

A total of 40 complete (8,941–9,010 base pairs) or near complete (8,691 bp) TrV genomes were recovered from the data. Characteristic motifs conserved in TrV and the insect picorna-like viruses were recovered in the RNA helicase (GX₄GK), cysteine protease (GXCG) and RdRp (LKDE, SGX₃TX₃N and YGDD) regions. The TrV genome and all known Dicistroviridae genomes comprise two non-overlapping ORFs (nonstructural protein and capsid protein) and 20 of the 40 assembled genomes had the same genetic architecture (GenBank Acc. BK067781, BK068012–030; Fig. 1A). However, the remaining 20 genomes had a single stop codon present at the beginning of where ORF1 (nonstructural protein) should be found. Ten of these genomes contained the TAG stop codon at base position 37 of the ORF1 nonstructural protein (relative to the TrV reference genome; Fig. 1B), while the remaining 10 genomes contained the TAA stop codon at base position 55 of the ORF1 nonstructural protein (Fig. 1C).

Phylogenetic analysis of translated sequences at the ORF1, encoding for nonstructural proteins (Fig. 2), showed all sequences formed a strongly supported clade (UFBoot support: 100%) that included the only TrV genome publicly available (ORF1, GenBank: AAF00472). This TrV clade was found as a sister (UFBoot support: 96%) to a Black queen cell virus and Himetobi P virus clade (UFBoot support: 100%).

Phylogenetic analysis of translated sequences at ORF2, encoding for the capsid protein, showed all sequences clusters tightly (UFBoot support: 100%) with the TrV reference genome (GenBank: AAF00473; Figure S1). Genome assemblies have percentage differences with the TrV reference genome of between 1.88–5.01% (p-distance). Pairwise sequence differences within the TrV clades were in the range 0–5.49% (p-distance).

Meccus longipennis virus 1 (MlV1)

MlV1 was detected in 16 from a total of 122 SRA samples. All positives were detected from T. infestans hosts with 9 and 7 positives detected from laboratory colony and wild population samples, respectively. A total of 16 complete (10,452–10,524 bp) or near complete (10,291–10,421 bp) MlV1 genomes were recovered from the data (GenBank Acc. BK068121–136).

Only a single ORF, encoding a polyprotein, is present in MIV1 (GenBank: OQ384707). Phylogenetic analysis of the single Iflaviridae polyprotein (Fig. 3), showed all sequences clusters tightly (UFBoot support: 100%) with the only MlV1 genome publicly available (Polyprotein, GenBank: OQ384707). This MlV1 clade was found as a sister (UFBoot support: 96%) to a clade containing Euscelidius variegatus virus 1, Graminella nigrifrons virus 1 and Psammotettix alienus iflavirus 1 (UFBoot support: 100%). Assembled genomes have percentage differences with the MlV1 reference genome of between 2.30–2.90% (p-distance). Percentage differences within the MlV1 clades were in the range 0–2.90% (p-distance).

Drosophila melanogaster Nora virus (NV)

Drosophila melanogaster Nora virus (NV) sequences were found in a T. infestans laboratory colony from Argentina. An NV sequence (517 bp) from SRR21627160 aligned to the third protein (VP4C) of the VP4 capsid protein gene and the non-coding 3´ end of the NV reference genome (Fig. 4; GenBank: NC_007919), with which it had a percentage difference of 2.52% (p-distance). Another NV sequence (1,803 bp) from SRR21627167 aligned to the 3´ end of the VP2 gene of the NV reference genome, with which it had a percentage difference of 2.83% (p-distance).

Rhodnius prolixus viruses 4–6

Three RpVs taxa were detected among 3 SRA samples corresponding to RpV4, RpV5, and RpV6. A sequence of RpV4 (789 bp) was recovered in a R. robustus laboratory colony pool sample from French Guiana (ERR1315268). This sequence aligned at the 3´ end of the RNA-dependent RNA polymerase (RdRp) gene of the RpV4 reference genome (Fig. 5; GenBank: MZ328307), with which it had a percentage difference of 4.06% (p-distance). A sequence of RpV6 (522 bp) was recovered in a R. neglectus laboratory colony pool sample from Brazil (SRR15602393). This sequence aligned at the 3´ end of ORF1 and the 5´ end of the RdRp gene of the RpV6 reference genome (Fig. 5; GenBank: MZ328309), with which it had a percentage difference of 11.1% (p-distance). Sequences from RpV5 (1,224 bp) and RpV6 (982 bp) were recovered in a wild R. neglectus individual from French Guiana (ERR1315270). The former aligned with the majority of ORF1 and the 5´ end of the RdRp gene of the RpV5 genome (Fig. 5; GenBank: MZ328308), with which it had a percentage difference of 0.25% (p-distance). The latter aligned at the 3´ end of ORF1 and the 5´ end of the RdRp gene of the RpV6 reference genome (GenBank: MZ328309), with which it had a percentage difference of 0.41% (p-distance).

The central importance of Triatominae in the transmission of Chagas disease has driven the need for phylogenetic studies to better characterize and incriminate Triatominae species, and the establishment of laboratory colonies to undertake in vivo experiments addressing questions on vector biology, vector-parasite interactions, insecticide susceptibility, among others. Despite the generation of considerable molecular resources for Triatominae, such as genome and genome expression data, the virome infecting Triatominae remains poorly known. The first virus discovered in Triatominae was the TrV, isolated from wild and laboratory populations of T. infestans from Argentina in 1987 [7, 8] but it was not until 2000 that the first TrV genome (GenBank: NC_003783) became publicly available [32]. Only recently, a further seven viruses belonging to the families Iflaviridae, Permutotetraviridae and Solemoviridae (RpV1–7; GenBank: MZ328304–310) have been detected in laboratory colonies of R. prolixus from Brazil [16]. One other virus—MlV1, belonging to the family Iflaviridae—has been identified in Meccus longipennis from Mexico (GenBank: OQ384707). Crucially, only a single reference genome exists for each virus species so far detected in Triatominae. In this study, we sought to assess the utility of publicly available transcriptome data available through the SRA and ENA repositories for better characterizing Triatominae viromes, assembling additional and novel virus genomes and establishing new virus records for a variety of species and genera in Triatominae.

The TrV was the most prevalent virus detected among samples, species and genera. Previously, this virus was detected in a variety of Triatoma species as well as P. coreodes and R. prolixus. To our knowledge, this study reports the first records of TrV in T. brasiliensis and in the genus Mepraia (M. gajardoi, M. spinolai, M. parapatrica). We have expanded the publicly available genomic resources of TrV, adding 39 genomes to the single genome currently available on GenBank. No clear geographic partitioning of genetic variation between laboratory and wild host populations was apparent. The TrV has previously been detected in several Triatoma species in Argentina, with positivity rates of approximately 10% [11, 13, 14], whereas positivity rates among laboratory Triatominae have been reported to be considerably higher, in some cases up to 100% [14]. This has been attributed to high host densities and the increased likelihood of cannibalism, coprophagy, kleptohaemophagy, and fecal-oral transmission [14, 33]. However, in the current study, we assembled partial and whole TrV genomes from almost 50% of Mepraia individuals (8/18) collected from Chile as part phylogenomic study of the genus [34], and from 100% of seven T. infestans individuals collected from Bolivia as part of a study to establish expression profiles for the species [35]. Far fewer TrV positives (1 of 29) were detected among individuals taken from a wild population of T. brasiliensis from the city of Caicó, Brazil as part of an effort to establish a reference transcriptome and expression profiles for this species [36, 37]. While TrV seropositivity has been found among human populations in Argentina, Bolivia, and Mexico [38], to date the virus has only detected among wild Triatominae populations in Argentina. To our knowledge, our study reports the first cases of TrV detected among wild populations in Bolivia, Brazil, and Chile. Taken as a whole, the TrV appears to have a continental distribution and considerable differences in prevalence among wild Triatominae, with some populations reaching the levels of prevalence found in laboratory populations. Due to the virus’ horizontal mode of transmission and high pathogenicity, it has been considered a potential agent for the control of Triatominae vectors [14]. The considerable variation in prevalence observed in wild populations may influence host exposure, susceptibility, and immune response, which have important implications for the efficacy of vector control measures using this agent. The impact of the TrV genomes with ORF1 stop codons, and whether they can be rescued with functional virus proteins in the infected cells, needs further elucidation. The genomic variation extant in endemic and introduced TrV may also have an important influence the efficacy of such control interventions. Our contributions to expanding the public genomic resources of this virus serves as an important baseline to further characterize genomic and geographic variation in TrV.

The next most prevalent virus among Triatominae hosts was MlV1. This virus is very poorly known and first characterized in 2023 from wild caught individuals of M. longipennis from the state of Chihuahua, Mexico. The MlV1 genomes assembled in the current study came from wild and laboratory populations, and the genetic variation and phylogenetic position is consistent with a single taxonomic clade. It is found in a sister relationship with a clade of other Hemiptera-specific viruses (Euscelidius variegatus virus 1, Psammotettix alienus iflavirus 1 and Graminella nigrifrons virus 1), which may represent host-based evolutionary relationships. Our findings present the first records of this virus both in laboratory populations, and from wild populations in South America.

The Drosophila melanogaster NV was detected in two individuals from a laboratory colony in Argentina. This virus was first characterized in a laboratory colony of Drosophila melanogaster in Sweden in 2006. Since then, the virus has been detected in species from a total of five insect Orders (Diptera, Coleoptera, Hymenoptera, Lepidoptera and Orthoptera) [39]. Our findings record Drosophila melanogaster NV in a species of Hemiptera (T. infestans) for the first time. Although the assemblies recovered in the current study display very low levels of sequence differences with the NV references available on GenBank, our assemblies are partial, representing less than 20% of the viral genome, and so we are unable to fully characterize the extent of differentiation between the virus found in the Argentinian colony from the Drosophila melanogaster NV references. However, our findings present a primer for further work on the detection and characterization of Drosophila melanogaster NV in Triatominae and its potential circulation among species across the Order.

The final group of viruses detected in this study were only recently characterized from a R. prolixus laboratory colony from Brazil [16]. Here we detected signatures for three of the seven originally characterized viruses in individuals of R. robustus and R. neglectus. These three viruses belong to the families Permutotetraviridae (RpV4) and Solemoviridae (RpV5, RpV6) and are the first reports of such detections outside of Brazil. We also report the first records of the Solemoviridae viruses detected in a wild Triatominae (R. robustus) population, which were collected in French Guiana as part of a study of chemosensory genes in Chagas disease vectors [40]. Whereas the study that originally characterized the R. prolixus viruses found that the persistence of these viruses in laboratory colonies was at least partly explained by the vertical modes of transmission [16], the modes of transmission in wild populations is unknown. Our findings indicate the circulation of R. prolixus viruses in wild populations of other Rhodnius species and the need for further exploration of these viruses, their transmission routes and pathogenic potential across the genus.

Understanding the relationship between insect-specific viruses and their Triatomine hosts may unlock novel population suppression mechanisms that can be leveraged in the fight against the silent expansion of the neglected, but deadly Chagas disease in the New World. All six of the viruses detected in the current study are now reported in well-established laboratory colonies of Triatominae (this study and Brito et al. [16]). The hidden presence of such insect viruses in vector colonies can have important impacts on the quality and reproducibility of downstream experimental studies of virology, immunology, and metabolism, where coinfections can inhibit the replication of a pathogen and alter vector competence, alter virus virulence and infection severity, and modify immune responses to primary and secondary infections [41–44]. Thorough screening of laboratory colonies using agnostic sequencing approaches enables detection and characterization of potentially hidden and novel virus infections and control for such variables that may impact experimental outcomes. Our study also underlines the importance of further virome studies in wild Triatominae populations. There is currently a dearth of publicly transcriptome data to enable mining of novel and diverse viruses from the wild. Despite minimal available data, our study has provided new virus records for each wild origin dataset analyzed, showing the values of reinterrogating publicly available transcriptome data for pathogen discovery. Consequently, we recognize continued agnostic sequencing approaches as highly valuable for establishing baselines for novel and emerging virus prevalence, diversity, and dynamics among Chagas disease vectors and essential for possible novel virus isolation and pathogenicity analysis.

The authors declare that the research was conducted in the absence of any commercial or financial relationships that could be construed as a potential conflict of interest.

Disclaimer

The authors declare that the research was conducted in the absence of any commercial or financial relationships that could be construed as a potential conflict of interest. The funders of the research had no influence on results presented. The opinions or assertions contained herein are the private views of the authors, and are not to be construed as official, or as reflecting true views of the Department of the Army, Navy, or the Department of Defense. Material contained within this publication has been reviewed by the Walter Reed Army Institute of Research. There is no objection to its presentation and/or publication. Any use of trade, firm, or product names is for descriptive purposes only and does not imply endorsement by the U.S. Government.

Author Contributions

All authors contributed to the study conception and design. Analyses were performed by BPB, JO and KE. The first draft of the manuscript was written by BPB and JO and all authors commented on previous versions of the manuscript. All authors read and approved the final manuscript.

Acknowledgments

This study was conducted at the Walter Reed Biosystematics Unit (WRBU) of the Walter Reed Army Institute of Research (WRAIR), housed within the Smithsonian Institution Museum Support Center, with institutional support from both parties. Data analysis were conducted in and with the support of the Laboratories of Analytical Biology (https://ror.org/05b8c0r92) of the National Museum of Natural History. This study was financially supported by the Armed Forces Health Surveillance Division—Global Emerging Infections Surveillance (AFHSD-GEIS) award P0053_24_WR and the Military Infectious Diseases Research Program (MIDRP) award MI240083. A one-year travelling research fellowship for JO was funded by Fundação de Amparo à Pesquisa do Estado de São Paulo (FAPESP process 2022/01894-4). This manuscript was prepared whilst BPB and KE held a National Research Council (NRC) Research Associateship Awards at the Walter Reed Biosystematics Unit (WRBU), through the Walter Reed Army Institute of Research (WRAIR), Silver Spring, MD.

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Leveraging transcriptome SRAs for virus detection in wild and colony populations of triatomines (Hemiptera: Reduviidae: Triatominae)

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