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. 2012;7(9):e44612.
doi: 10.1371/journal.pone.0044612. Epub 2012 Sep 25.

An insight into the sialotranscriptome of the cat flea, Ctenocephalides felis

José M C Ribeiro  1 , Teresa C F Assumpção, Dongying Ma, Patricia H Alvarenga, Van M Pham, John F Andersen, Ivo M B Francischetti, Kevin R Macaluso
Affiliations

An insight into the sialotranscriptome of the cat flea, Ctenocephalides felis

José M C Ribeiro et al. PLoS One. 2012.

Abstract

Background: Saliva 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 findings: A 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/significance: Fleas, 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.

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Conflict of interest statement

Competing Interests: The authors have declared that no competing interests exist.

Figures

Figure 1
Figure 1. Cat flea sialotranscriptome.
Distribution of assembled contigs (A) and number of expressed sequence tags (ESTs) (B) in the sialotranscriptome of the cat flea, Ctenocephalides felis.
Figure 2
Figure 2. Phylogram of the flea salivary phosphatase family with one sequence from Bombus terrestris as an outgroup.
The sequences were aligned by ClustalW. The Ctenocephalides felis sequences are recognized by starting with Cf- and are followed by the number of the contig from which they derived. The other sequences were obtained from GenBank and are recognized by the first three letters of their genus name, followed by the first three letters of the species name, followed by the NCBI accession number. The numbers at the nodes represent the percent bootstrap support (10,000 iterations) for the neighbor-joining algorithm, using pairwise deletion and gamma distribution of the amino acid substitutions. The bar at the bottom indicates the amino acid substitution rate per site. The Roman numerals indicate tree locations for the cat flea sequences that are distant enough to be from different genes. Clade II may have two genes, for a total of four possible genes.
Figure 3
Figure 3. The FS-H/FS-I/7-Cys family of flea salivary peptides.
(A) ClustalW alignment indicating the cysteine residues in black background, the identical Tyr in yellow background, and the conserved amino acids in blue background. The numbers above the sequence indicate the six conserved cysteines. The signal peptide region is not shown. (B) Bootstrapped phylogram of the sequences based on the alignment in (A) after 1,000 iterations. The numbers at the nodes indicate the percent bootstrap support, and the bar at the bottom the amino acid divergence per site. Sequences identified in this work are named Cf- followed by the number of the originating contig from File S1. Sequences derived from GenBank are recognized by the first three letters of their genus name, followed by the first three letters of the species name, followed by the gi| accession number. The cat flea proteins giving the name of the family are indicated by FS-H and FS-I following their accession numbers.
Figure 4
Figure 4. The deorphanized 8-Cys family of flea salivary peptides.
(A) ClustalW alignment indicating the cysteine residues in black background, the identical Gly as well as the conserved Phe and Tyr in yellow background, and remaining conserved amino acids in blue background. The numbers above the sequence indicate the eight conserved cysteines. The signal peptide region is not shown. The sequences identified in this work are named Cf- followed by the number of the originating contig from File S1. The sequences derived from GenBank are recognized by the first three letters of their genus name, followed by the first three letters of the species name, followed by the gi| accession number.
Figure 5
Figure 5. The cat flea Cys-less peptide family.
ClustalW alignment showing the non-conserved residues in black background and the signal peptide in yellow background. Positively charged amino acids on the mature peptide are shown in blue color; acidic residues are shown in red. The GGGGGA motif is shown in green background. The conserved prolines flanking the glycine-rich motif are shown in pink background.
Figure 6
Figure 6. The short flea salivary peptide.
ClustalW alignment indicating the cysteine residues in black background, the identical amino acids in yellow background, and the conserved amino acids in blue background. The signal peptide region is not shown. The sequences identified in this work are named Cf- followed by the number of the originating contig from File S1. The sequences derived from GenBank are recognized by the first three letters of their genus name, followed by the first three letters of the species name, followed by the gi| accession number.
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