An insight into the sialotranscriptome and virome of Amazonian anophelines

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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.

Electronic supplementary material

The online version of this article (10.1186/s12864-019-5545-0) contains supplementary material, which is available to authorized users.

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Most cited references 82

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The dominant Anopheles vectors of human malaria in the Americas: occurrence data, distribution maps and bionomic précis

Marianne Sinka, Yasmin Rubio-Palis, Sylvie Manguin … (2010)

Background An increasing knowledge of the global risk of malaria shows that the nations of the Americas have the lowest levels of Plasmodium falciparum and P. vivax endemicity worldwide, sustained, in part, by substantive integrated vector control. To help maintain and better target these efforts, knowledge of the contemporary distribution of each of the dominant vector species (DVS) of human malaria is needed, alongside a comprehensive understanding of the ecology and behaviour of each species. Results A database of contemporary occurrence data for 41 of the DVS of human malaria was compiled from intensive searches of the formal and informal literature. The results for the nine DVS of the Americas are described in detail here. Nearly 6000 occurrence records were gathered from 25 countries in the region and were complemented by a synthesis of published expert opinion range maps, refined further by a technical advisory group of medical entomologists. A suite of environmental and climate variables of suspected relevance to anopheline ecology were also compiled from open access sources. These three sets of data were then combined to produce predictive species range maps using the Boosted Regression Tree method. The predicted geographic extent for each of the following species (or species complex*) are provided: Anopheles (Nyssorhynchus) albimanus Wiedemann, 1820, An. (Nys.) albitarsis*, An. (Nys.) aquasalis Curry, 1932, An. (Nys.) darlingi Root, 1926, An. (Anopheles) freeborni Aitken, 1939, An. (Nys.) marajoara Galvão & Damasceno, 1942, An. (Nys.) nuneztovari*, An. (Ano.) pseudopunctipennis* and An. (Ano.) quadrimaculatus Say, 1824. A bionomics review summarising ecology and behaviour relevant to the control of each of these species was also compiled. Conclusions The distribution maps and bionomics review should both be considered as a starting point in an ongoing process of (i) describing the distributions of these DVS (since the opportunistic sample of occurrence data assembled can be substantially improved) and (ii) documenting their contemporary bionomics (since intervention and control pressures can act to modify behavioural traits). This is the first in a series of three articles describing the distribution of the 41 global DVS worldwide. The remaining two publications will describe those vectors found in (i) Africa, Europe and the Middle East and (ii) in Asia. All geographic distribution maps are being made available in the public domain according to the open access principles of the Malaria Atlas Project.

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Ecologic observations on anopheline vectors of malaria in the Brazilian Amazon.

V Scarpassa, Marta S. Rafael, Sherry Thatcher … (1998)

Human intervention in the Brazilian Amazon region promotes contacts between humans and vectors that may favor the propagation of anopheline mosquitoes and the spread of malaria in the absence of planning and infrastructure to control this disease. Vector ecology studies were carried out to determine the risk areas. These data should help in designing appropriate malaria control measures. Data from 14 different regions are reported. Vectors are able to adapt to different environments, which made it necessary to study each area. The parameters studied were Anopheles breeding sites, species distribution, incidence, feeding preferences, hours of maximum activity of adult mosquitoes, seasonality, resting places, and the presence of Plasmodium. Species complexes were also studied. Anopheles darlingi may be responsible for maintaining malaria in human populations in this region. A reduction in the population density of A. darlingi in a particular geographic area can sometimes cause the disappearance of malaria. This species feeds at night but has a peak of activity at the beginning of the evening and another at dawn. Other species are mainly crepuscular and all anophelines demonstrated pronounced exophilia. The timing of feeding activities was found to vary in areas altered by human intervention and also depended on the time of the year and climatic conditions. The larvae were more abundant in the rivers with a less acidic pH and rural areas showed the highest larval index.

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A Deep Insight into the Sialotranscriptome of the Gulf Coast Tick, Amblyomma maculatum

Shahid Karim, Parul Singh, Jose Ribeiro (2011)

Background Saliva of blood sucking arthropods contains compounds that antagonize their hosts' hemostasis, which include platelet aggregation, vasoconstriction and blood clotting; saliva of these organisms also has anti-inflammatory and immunomodullatory properties. Perhaps because hosts mount an active immune response against these compounds, the diversity of these compounds is large even among related blood sucking species. Because of these properties, saliva helps blood feeding as well as help the establishment of pathogens that can be transmitted during blood feeding. Methodology/Principal Findings We have obtained 1,626,969 reads by pyrosequencing a salivary gland cDNA library from adult females Amblyomma maculatum ticks at different times of feeding. Assembly of this data produced 72,441 sequences larger than 149 nucleotides from which 15,914 coding sequences were extracted. Of these, 5,353 had >75% coverage to their best match in the non-redundant database from the National Center for Biotechnology information, allowing for the deposition of 4,850 sequences to GenBank. The annotated data sets are available as hyperlinked spreadsheets. Putative secreted proteins were classified in 133 families, most of which have no known function. Conclusions/Significance This data set of proteins constitutes a mining platform for novel pharmacologically active proteins and for uncovering vaccine targets against A. maculatum and the diseases they carry.

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Author and article information

Contributors

Vera Margarete Scarpassa: vera@inpa.gov.br

Humbeto Julio Debat: debat.humberto@inta.gob.ar

Ronildo Baiatone Alencar: alencarronildo@gmail.com

José Ferreira Saraiva: jfsento@gmail.com

Eric Calvo: ecalvo@niaid.nih.gov

Bruno Arcà: bruno.arca@uniroma1.ita

José M. C. Ribeiro: jribeiro@niaid.nih.gov

Journal

Journal ID (nlm-ta): BMC Genomics

Journal ID (iso-abbrev): BMC Genomics

Title: BMC Genomics

Publisher: BioMed Central (London )

ISSN (Electronic): 1471-2164

Publication date (Electronic): 4 March 2019

Publication date PMC-release: 4 March 2019

Publication date Collection: 2019

Volume: 20

Electronic Location Identifier: 166

Affiliations

[1 ]ISNI 0000 0004 0427 0577, GRID grid.419220.c, Laboratório de Genética de Populações e Evolução de Mosquitos Vetores de Malária e Dengue, Coordenação de Biodiversidade, , Instituto Nacional de Pesquisas da Amazônia, ; Manaus, Amazonas Brazil

[2 ]ISNI 0000 0001 2167 7174, GRID grid.419231.c, Instituto de Patología Vegetal, Centro de Investigaciones Agropecuarias, , Instituto Nacional de Tecnología Agropecuaria (IPAVE-CIAP-INTA), ; Córdoba, Argentina

[3 ]GRID grid.7841.a, Department of Public Health and Infectious Diseases, Division of Parasitology, , Sapienza University of Rome, ; Rome, Italy

[4 ]ISNI 0000 0001 2164 9667, GRID grid.419681.3, Laboratory of Malaria and Vector Research, , National Institute of Allergy and Infectious Diseases, ; Bethesda, MD USA

Article

Publisher ID: 5545

DOI: 10.1186/s12864-019-5545-0

PMC ID: 6399984

PubMed ID: 30832587

SO-VID: 54c8455c-5aab-49ba-8456-a3965203a419

License:

Open AccessThis 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.

History

Date received : 4 October 2018

Date accepted : 18 February 2019

Funding

Funded by: Division of Intramural Research, National Institute of Allergy and Infectious Diseases (US)

Award ID: Z01 AI000810-19

Funded by: FundRef http://dx.doi.org/10.13039/501100003407, Ministero dell’Istruzione, dell’Università e della Ricerca;

Award ID: PRIN 2015JXC3JF

Award Recipient : Bruno Arcà

Funded by: FundRef http://dx.doi.org/10.13039/501100004916, Fundação de Amparo à Pesquisa do Estado do Amazonas;

Award ID: 3111/2012-Universal

Award Recipient : Vera Margarete Scarpassa

Custom metadata

ScienceOpen disciplines: Genetics

Keywords: vector biology,mosquitoes,malaria,virus,salivary glands,transcriptome

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ScienceOpen disciplines: Genetics

Keywords: vector biology, mosquitoes, malaria, virus, salivary glands, transcriptome

An insight into the sialotranscriptome and virome of Amazonian anophelines

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Abstract

Background

Results

Conclusions

Electronic supplementary material

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Vector Biology

Most cited references 82

The dominant Anopheles vectors of human malaria in the Americas: occurrence data, distribution maps and bionomic précis

Ecologic observations on anopheline vectors of malaria in the Brazilian Amazon.

A Deep Insight into the Sialotranscriptome of the Gulf Coast Tick, Amblyomma maculatum

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