Anopheline salivary protein genes and gene families: an evolutionary overview after the whole genome sequence of sixteen Anopheles species

Bruno Arcà,Fabrizio Lombardo,Claudio J Struchiner,José M C Ribeiro

doi:10.1186/s12864-017-3579-8

Abstract

BackgroundMosquito saliva is a complex cocktail whose pharmacological properties play an essential role in blood feeding by counteracting host physiological response to tissue injury. Moreover, vector borne pathogens are transmitted to vertebrates and exposed to their immune system in the context of mosquito saliva which, in virtue of its immunomodulatory properties, can modify the local environment at the feeding site and eventually affect pathogen transmission. In addition, the host antibody response to salivary proteins may be used to assess human exposure to mosquito vectors. Even though the role of quite a few mosquito salivary proteins has been clarified in the last decade, we still completely ignore the physiological role of many of them as well as the extent of their involvement in the complex interactions taking place between the mosquito vectors, the pathogens they transmit and the vertebrate host. The recent release of the genomes of 16 Anopheles species offered the opportunity to get insights into function and evolution of salivary protein families in anopheline mosquitoes.ResultsOrthologues of fifty three Anopheles gambiae salivary proteins were retrieved and annotated from 18 additional anopheline species belonging to the three subgenera Cellia, Anopheles, and Nyssorhynchus. Our analysis included 824 full-length salivary proteins from 24 different families and allowed the identification of 79 novel salivary genes and re-annotation of 379 wrong predictions. The comparative, structural and phylogenetic analyses yielded an unprecedented view of the anopheline salivary repertoires and of their evolution over 100 million years of anopheline radiation shedding light on mechanisms and evolutionary forces that contributed shaping the anopheline sialomes.ConclusionsWe provide here a comprehensive description, classification and evolutionary overview of the main anopheline salivary protein families and identify two novel candidate markers of human exposure to malaria vectors worldwide. This anopheline sialome catalogue, which is easily accessible as hyperlinked spreadsheet, is expected to be useful to the vector biology community and to improve the capacity to gain a deeper understanding of mosquito salivary proteins facilitating their possible exploitation for epidemiological and/or pathogen-vector-host interaction studies.

Highlights

Mosquito saliva is a complex cocktail whose pharmacological properties play an essential role in blood feeding by counteracting host physiological response to tissue injury
SG2-like has been sometime indicated as SG2a or SG2A, which created some confusion; following the physical order in the cluster we propose here to name AGAP006505 as gSG2a and indicate AGAP006504 as gSG2b or gSG2-like. gSG2 and gSG2b were found expressed in both male and female salivary glands [20, 35, 36, 46] and orthologues were identified in sialotranscriptomes of An. stephensi [23], An. funestus [19] and An. darlingi [21]. gSG2a most likely originated by gene duplication from gSG2b but was neither found during salivary transcriptome analyses nor differentially expressed in salivary glands [46] and for this reason will not be considered here
The anopheline species analyzed here span approximately 100 million years of evolution and the analysis of their salivary repertoires helped shedding some light on the main mechanisms driving the evolution of salivary proteins in anophelines and, more generally, in blood feeding arthropods

Summary

Introduction

Mosquito saliva is a complex cocktail whose pharmacological properties play an essential role in blood feeding by counteracting host physiological response to tissue injury. Vector borne pathogens are transmitted to vertebrates and exposed to their immune system in the context of mosquito saliva which, in virtue of its immunomodulatory properties, can modify the local environment at the feeding site and eventually affect pathogen transmission. Pathogens are deposited into the skin and exposed to the vertebrate host immune system in the context of arthropod saliva These vector salivary components can modify the feeding site and may affect the transmission of pathogens as diverse as arboviruses, bacteria and protozoan parasites [7,8,9,10,11,12], pointing out the possible exploitation of vector salivary proteins as potential vaccine targets [13,14,15,16]. Inoculation of arthropod salivary proteins triggers in vertebrate hosts an antibody response which can be used as a biomarker of host exposure to vector bites and may represent a useful tool for epidemiological studies and evaluation of efficacy of vector control interventions [7, 17]

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Conclusion