An Insight into the Sialotranscriptome of the Cat Flea, Ctenocephalides felis

José M C Ribeiro,Patricia H Alvarenga,Ivo M B Francischetti,Kevin R Macaluso,Dongying Ma,Van M Pham,Teresa C F Assumpção,John F Andersen,Bradley S Schneider

doi:10.1371/journal.pone.0044612

José M C Ribeiro, Patricia H Alvarenga + Show 7 more

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https://doi.org/10.1371/journal.pone.0044612

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Abstract

BackgroundSaliva of hematophagous arthropods contains a diverse mixture of compounds that counteracts host hemostasis. Immunomodulatory and antiinflammatory components are also found in these organisms' saliva. Blood feeding evolved at least ten times within arthropods, providing a scenario of convergent evolution for the solution of the salivary potion. Perhaps because of immune pressure from hosts, the salivary proteins of related organisms have considerable divergence, and new protein families are often found within different genera of the same family or even among subgenera. Fleas radiated with their vertebrate hosts, including within the mammal expansion initiated 65 million years ago. Currently, only one flea species–the rat flea Xenopsylla cheopis–has been investigated by means of salivary transcriptome analysis to reveal salivary constituents, or sialome. We present the analysis of the sialome of cat flea Ctenocephaides felis.Methodology and Critical FindingsA salivary gland cDNA library from adult fleas was randomly sequenced, assembled, and annotated. Sialomes of cat and rat fleas have in common the enzyme families of phosphatases (inactive), CD-39-type apyrase, adenosine deaminases, and esterases. Antigen-5 members are also common to both sialomes, as are defensins. FS-I/Cys7 and the 8-Cys families of peptides are also shared by both fleas and are unique to these organisms. The Gly-His-rich peptide similar to holotricin was found only in the cat flea, as were the abundantly expressed Cys-less peptide and a novel short peptide family.Conclusions/SignificanceFleas, in contrast to bloodsucking Nematocera (mosquitoes, sand flies, and black flies), appear to concentrate a good portion of their sialome in small polypeptides, none of which have a known function but could act as inhibitors of hemostasis or inflammation. They are also unique in expansion of a phosphatase family that appears to be deficient of enzyme activity and has an unknown function.

Highlights

Saliva of blood-feeding animals contains a mixture of compounds that prevent their host’s physiologic defences against blood loss, or hemostasis, which is a complex response based on the functional triad of platelet aggregation, vasoconstriction, and blood clotting
In the past 10 years, molecular biology advances allowed the description of organ-specific transcriptomes, obtained from the random DNA sequencing of clones derived from reverse transcription of organ-specific mRNA
This transcriptome Expressed sequence tags (EST) and contig distribution contrasts with that found for the rat flea sialotranscriptome [9], where 75% of the ESTs were classified as belonging to the S class, nearly 3 times the value found here

Summary

Introduction

Saliva of blood-feeding animals contains a mixture of compounds that prevent their host’s physiologic defences against blood loss, or hemostasis, which is a complex response based on the functional triad of platelet aggregation, vasoconstriction, and blood clotting. The sialotranscriptome of X. cheopis identified an expanded phosphatase family of proteins (without a known function) as well as other enzymes including a CD-39 type of apyrase and an esterase; mucins, antimicrobial peptides, and members of the antigen 5 family were described.

Results

Conclusion