Abstract
Sand fly salivary proteins that produce a specific antibody response in humans and animal reservoirs have been shown to be promising biomarkers of sand fly exposure. Furthermore, immunity to sand fly salivary proteins were shown to protect rodents and non-human primates against Leishmania infection. We are missing critical information regarding the divergence amongst sand fly salivary proteins from different sand fly vectors, a knowledge that will support the search of broad or specific salivary biomarkers of vector exposure and those for vaccines components against leishmaniasis. Here, we compare the molecular evolution of the salivary protein families in New World and Old World sand flies from 14 different sand fly vectors. We found that the protein families unique to OW sand flies are more conserved than those unique to NW sand flies regarding both sequence polymorphisms and copy number variation. In addition, the protein families unique to OW sand flies do not display as many conserved cysteine residues as the one unique to the NW group (28.5% in OW vs. 62.5% in NW). Moreover, the expression of specific protein families is restricted to the salivary glands of unique sand fly taxon. For instance, the ParSP15 family is unique to the Larroussius subgenus whereas phospholipase A2 is only expressed in member of Larroussius and Adlerius subgenera. The SP2.5-like family is only expressed in members of the Phlebotomus and Paraphlebotomus subgenera. The sequences shared between OW and NW sand flies have diverged at similar rates (38.7 and 45.3% amino acid divergence, respectively), yet differences in gene copy number were evident across protein families and sand fly species. Overall, this comparative analysis sheds light on the different modes of sand fly salivary protein family divergence. Also, it informs which protein families are unique and conserved within taxon for the choice of taxon-specific biomarkers of vector exposure, as well as those families more conserved across taxa to be used as pan-specific vaccines for leishmaniasis.
Highlights
Vector borne diseases represent almost half of the neglected tropical infectious diseases
We focused on the evolutionary analysis of protein families unique to Old World (OW) sand flies comparing that with the protein families shared between OW and New World (NW) sand flies as well as those unique to NW sand flies
From 14 sand fly salivary gland transcriptomes we compiled the sand fly salivary proteins unique to either NW or OW sand flies as well as protein families common to all sand fly species and developed an updated catalog for all the analyzed sand fly salivary proteins (Table 1). With this extensive catalog of sand fly salivary proteins we identified 12 protein families shared between OW and NW sand flies, lufaxin, apyrase, yellow-related protein, silk-related protein or PpSP32, endonuclease, hyaluronidase, adenosine deaminase, small odorant binding-like proteins, D7 family of proteins, antigen-5 related protein, ParSP17 (39 kDa protein of unkown function), ParSP80 (16 kDa protein of unkown function) (Figure 1 and Supplementary Figures 4–15), seven protein families unique to OW sand flies, pyrophosphatase, phospholipase A2, ParSp15 (5 kDa protein of unknown function), ParSP25 (32 kDa protein of unknown function), SP16
Summary
Vector borne diseases represent almost half of the neglected tropical infectious diseases. Blood sucking arthropods secrete a plethora of bioactive compounds in their saliva to counteract the mammalian host hemostatic system in order to get a successful blood meal. Salivary antihemostatic components such as anticoagulants (Chagas et al, 2014), vasodilators (Ribeiro et al, 1989; Lerner et al, 1991; Champagne and Ribeiro, 1994), and inhibitors of platelet aggregation (Calvo et al, 2007, 2011; Assumpcao et al, 2013) have been described and some of these proteins characterized at the molecular level (Coutinho-Abreu et al, 2015). Immunity to specific sand fly salivary proteins was shown to protect rodents and non-human primates against leishmaniasis (Kamhawi et al, 2000; Gomes et al, 2008; Collin et al, 2009; Oliveira et al, 2015)
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