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Downloaded from Vector Base) [101] Were Added Was Performed Using the Oligo-Dt Beads Provided in the to the Last Assembly Stage Scarpassa et al. BMC Genomics (2019) 20:166 https://doi.org/10.1186/s12864-019-5545-0 RESEARCH ARTICLE Open Access An insight into the sialotranscriptome and virome of Amazonian anophelines Vera Margarete Scarpassa1, Humbeto Julio Debat2, Ronildo Baiatone Alencar1, José Ferreira Saraiva1, Eric Calvo4, Bruno Arcà3 and José M. C. Ribeiro4* Abstract Background: Saliva of mosquitoes contains anti-platelet, anti-clotting, vasodilatory, anti-complement and anti- inflammatory substances that help the blood feeding process. The salivary polypeptides are at a fast pace of evolution possibly due to their relative lack of structural constraint and possibly also by positive selection on their genes leading to evasion of host immune pressure. Results: In this study, we used deep mRNA sequence to uncover for the first time the sialomes of four Amazonian anophelines species (Anopheles braziliensis, A. marajorara, A. nuneztovari and A. triannulatus) and extend the knowledge of the A. darlingi sialome. Two libraries were generated from A. darlingi mosquitoes, sampled from two localities separated ~ 1100 km apart. A total of 60,016 sequences were submitted to GenBank, which will help discovery of novel pharmacologically active polypeptides and the design of specific immunological markers of mosquito exposure. Additionally, in these analyses we identified and characterized novel phasmaviruses and anpheviruses associated to the sialomes of A. triannulatus, A. marajorara and A. darlingi species. Conclusions: Besides their pharmacological properties, which may be exploited for the development of new drugs (e.g. anti-thrombotics), salivary proteins of blood feeding arthropods may be turned into tools to prevent and/or better control vector borne diseases; for example, through the development of vaccines or biomarkers to evaluate human exposure to vector bites. The sialotranscriptome study reported here provided novel data on four New World anopheline species and allowed to extend our knowledge on the salivary repertoire of A. darlingi. Additionally, we discovered novel viruses following analysis of the transcriptomes, a procedure that should become standard within future RNAseq studies. Keywords: Vector biology, Mosquitoes, Malaria, Virus, Salivary glands, Transcriptome Background host blood for the production and development of their Anopheline mosquitoes (Diptera: Culicidae: Anopheli- eggs [2]. While feeding blood, they can transmit patho- nae) of the Anopheles Meigen, 1818 genus are important gens to their hosts. in public health because they are vectors of human Currently, the Anopheles genus includes 465 formally malaria parasites in addition to arboviruses. In Brazil recognized species, which are subdivided into seven sub- they are popularly known as “muriçoca”, “mosquito genera: Anopheles (cosmopolitan, 182 species), Baimaia prego”, “suvela”, “pernilongo”, and “carapanã” [1]. Their (Oriental, one species), Cellia (Old World, 220 species), development comprise the stages of egg, larvae (four Kerteszia (Neotropical, 12 species), Lophopodomyia instars), and pupae, which are aquatic, while the adult (Neotropical, six species), Nyssorhynchus (Neotropical, stage is terrestrial. Both male and female adults feed on 39 species), and Stethomyia (Neotropical, five species) carbohydrates from flowers and fruits; however, only [3]. Worldwide, the primary vectors of human malaria females are hematophagous, using the proteins found in parasites belong to the subgenera Anopheles, Cellia, Kerteszia and Nyssorhynchus. * Correspondence: [email protected] In the Americas, the dominant vector species belong 4Laboratory of Malaria and Vector Research, National Institute of Allergy and Infectious Diseases, Bethesda, MD, USA to the Anopheles (three species) and Nyssorhynchus (six Full list of author information is available at the end of the article species) subgenera [4]. Among species of the subgenus © The Author(s). 2019 Open Access This article is distributed under the terms of the Creative Commons Attribution 4.0 International License (http://creativecommons.org/licenses/by/4.0/), which permits unrestricted use, distribution, and reproduction in any medium, provided you give appropriate credit to the original author(s) and the source, provide a link to the Creative Commons license, and indicate if changes were made. The Creative Commons Public Domain Dedication waiver (http://creativecommons.org/publicdomain/zero/1.0/) applies to the data made available in this article, unless otherwise stated. Scarpassa et al. BMC Genomics (2019) 20:166 Page 2 of 13 Nyssorhynchus, Anopheles darlingi is the primary vector been reported with human malaria parasites in different in Brazil, particularly in the Brazilian Amazon, and in regions of Brazil [7, 11, 18], as well as Peru and other countries in South America [4, 5]. The remaining Venezuela [19, 20]; however, due to its behavior and dominant vector species are A. albimanus, a member of habitat it has been recognized as a secondary vector. the A. albitarsis complex, A. marajoara, A. aquasalis, Currently, Anopheles nuneztovari is recognized as a and A. nuneztovari [4]. Other species of the Nyssor- species complex, where A. nuneztovari s.s. is incrimi- hynchus subgenus may be secondary local vectors or nated as an important human malaria vector in were found naturally infected with malaria parasite, such Colombia and Venezuela, showing endo and exophagic as A. benarrochi, A. rangeli, A. oswaldoi s.l., A. strodei, behaviors, and elevated levels of anthropophily and in- A. rondoni, A. trinkae, A. braziliensis, A. triannulatus, fection rate [21, 22]. On the other hand, the Brazilian and A. mattogrossensis [6, 7]. populations of A. nuneztovari s.l. are predominantly Anopheles darlingi is one of the most anthropophilic zoophagic; however, this species has been reported to be and efficient malaria vector in the Neotropical region, infected with Plasmodium spp. in five states of the Bra- particularly in the Brazilian Amazon region [5, 8]. It is zilian Amazon region [6, 7, 23], and it was incriminated mainly a riverine mosquito, amply distributed in the as a local vector in the state of Amapá, Brazil [11]. Based rainforest but also it is found in other regions from on recent studies, A. nuneztovari s.l. may consist of two Brazil, with exception of the dry areas of northeastern or more species within the Brazilian Amazon [24, 25], region. Anopheles darlingi also efficiently adapts in areas likely with different susceptibility to malaria parasites. of deforestation and altered environments, favoring its From the five species mentioned above, only A. dar- abundance and expansion and consequently triggering lingi has been studied under genomic and proteomic malaria outbreaks. Adults of this species bite throughout approaches, including transcriptome salivary gland ana- the night [7, 8], however, often two biting peaks have lyses [26, 27]. In this study, we present next generation been observed, one at sunset and the other at dawn. sequencing and sialotranscriptome approaches to inves- Specimens of A. darlingi have been captured in both tigate the salivary protein composition of five anopheline indoor and outdoor environments, with predominance species from the Brazilian Amazon region, which include for the later [8]. two samples of A. darlingi, an important malaria vector Anopheles marajoara is a member of the A. albitarsis in this region, Anopheles marajoara, an important local complex. In the past, it was believed that A. marajoara malaria vector, and Anopheles nuneztovari, Anopheles was a secondary or local vector of minor importance. triannulatus, and Anopheles braziliensis, secondary mal- However, studies conducted in peri-urban areas of the aria vectors. Additionally, we discuss the evolutionary city of Macapá, in the state of Amapá, Brazil, demon- aspects of these secreted salivary compounds with other strated that it can be a significant regional vector [9–11] anopheline salivary protein previously studied. These as well as in Boa Vista, in the state of Roraima [12]. Sup- protein sequences may help identification by mass porting these findings, in the District of Coração, state spectrometry of polypeptides of pharmacological inter- of Amapá, A. marajoara was the most frequent species, est, or to help in the design of immunological markers together with A. darlingi and A. braziliensis, showing of vector exposure. anthropophilic behavior and being captured in both The Anopheles virus landscape has been scarcely stud- indoor and outdoor environments [13, 14]. ied. The O’nyong-nyong arbovirus is the only Anopheles Previous studies have reported A. braziliensis as a zoo- vectored virus yet reported, and the insect specific vi- philic species with little or no importance in malaria ruses of most Anophelines have been barely explored transmission [1, 15] or as a secondary vector [5]. It has, [28]. Here, by assessing mosquito sialotranscriptome however, been found infected with human malaria data, we were able to identify and characterize three parasites in the states of Amazonas [8, 16], Amapá [9], novel viruses associated to A. triannulatus, A. mara- Rondônia [17], and Roraima [12]. Curiously, in the Dis- joara, and A. darlingi species. The detected viruses trict of Coração, state of Amapá, A. braziliensis was one correspond to emergent clades of insect-specific viruses, of the three most abundant and anthropophilic species. predominantly hosted by mosquitoes. It was captured in both indoor and outdoor environ- ments, although
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