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. 2021 Jan 29:10:611113.
doi: 10.3389/fcimb.2020.611113. eCollection 2020.

Comparative Proteomic Analysis of Rhipicephalus sanguineus sensu lato (Acari: Ixodidae) Tropical and Temperate Lineages: Uncovering Differences During Ehrlichia canis Infection

Gustavo Seron Sanches  1   2 , Margarita Villar  3   4 , Joana Couto  1 , Joana Ferrolho  1 , Isabel G Fernández de Mera  3 , Marcos Rogério André  5 , Darci Moraes Barros-Battesti  5 , Rosangela Zacarias Machado  5 , Gervásio Henrique Bechara  2 , Lourdes Mateos-Hernández  3   6 , José de la Fuente  3   7 , Sandra Antunes  1 , Ana Domingos  1
Affiliations

Comparative Proteomic Analysis of Rhipicephalus sanguineus sensu lato (Acari: Ixodidae) Tropical and Temperate Lineages: Uncovering Differences During Ehrlichia canis Infection

Gustavo Seron Sanches et al. Front Cell Infect Microbiol. .

Abstract

The tick vector Rhipicephalus sanguineus is established as a complex of closely related species with high veterinary-medical significance, in which the presence of different genetic, morphological, and biological traits has resulted in the recognition of different lineages within taxa. One of the most striking differences in the "temperate" and "tropical" lineages of R. sanguineus (s.l.) is the vector competence to Ehrlichia canis, suggesting that these ticks tolerate and react differently to pathogen infection. The present study addresses the SG and MG proteome of the R. sanguineus tropical and temperate lineages and compares their proteomic profile during E. canis infection. Batches of nymphs from the two lineages were allowed to feed on naïve and experimentally E. canis infected dogs and after molting, adults were dissected, and salivary glands and midgut tissues separated. Samples were screened for the presence of E. canis before proteomic analyses. The representation of the proteins identified in infected and non-infected tissues of each lineage was compared and gene ontology used for protein classification. Results highlight important differences in those proteomic profiles that added to previous reported genetic, biological, behavioral, and morphological differences, strengthening the hypothesis of the existence of two different species. Comparing infected and non-infected tissues, the results show that, while in midgut tissues the response to E. canis infection is similar in the salivary glands, the two lineages show a different pattern of protein representation. Focusing on the proteins found only in the infected condition, the data suggests that the cement cone produced during tick feeding may be implicated in pathogen infection. This study adds useful information to the debate on the controversial R. sanguineus systematic status, to the discussion related with the different vectorial competence occurring between the two lineages and identifies potential targets for efficient tick and tick-borne disease control.

Keywords: Ehrlichia; Rhipicephalus sanguineus; mialome; proteomics; sialome; ticks; vector competence.

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Conflict of interest statement

The authors declare that the research was conducted in the absence of any commercial or financial relationships that could be construed as a potential conflict of interest.

Figures

Figure 1
Figure 1
Study schema outlining the derivation of the samples, and the experimental groups subjected to the proteomic analysis. ni, non-infected condition; i, infected condition; SG, salivary glands; MG, midgut; G1–G8, experimental groups.
Figure 2
Figure 2
Gene ontology of differentially represented proteins from salivary glands of R. sanguineus tropical lineage vs. R. sanguineus temperate lineage in the non-infection condition. GO terms and its representation of biological process (A), and molecular function (B) were obtained using level 3. Blue bars represent the number of over-represented proteins in the tropical lineage compared to the temperate lineage and red bars represented the number of under-represented proteins in the tropical lineage compared to the temperate lineage (can be interpreted as the number of proteins more represented in the temperate lineage compared to the tropical lineage), with statistical significance (p < 0.05).
Figure 3
Figure 3
Gene ontology of differentially represented proteins from midgut of R. sanguineus tropical lineage vs. R. sanguineus temperate lineage in the non-infection condition. GO terms and its representation of biological process (A), and molecular function (B) obtained using level 3. Blue bars represent the number of over-represented proteins in the tropical lineage compared to the temperate lineage and red bars represented the number of under-represented proteins in the tropical lineage compared to the temperate lineage (can be interpreted as the number of proteins more represented in the temperate lineage compared to the tropical lineage), with statistical significance (p < 0.05).
Figure 4
Figure 4
Gene ontology of differentially represented proteins from salivary glands of R. sanguineus tropical lineage vs. R. sanguineus temperate lineage in the infection condition. GO terms and its representation of biological process (A), and molecular function (B) obtained using level 3. Blue bars represent the number of over-represented proteins in the tropical lineage compared to the temperate lineage and red bars represented the number of under-represented proteins in the tropical lineage compared to the temperate lineage (can be interpreted as the number of proteins more represented in the temperate lineage compared to the tropical lineage), with statistical significance (p < 0.05).
Figure 5
Figure 5
Gene ontology of differentially represented proteins from midgut of R. sanguineus tropical lineage vs. R. sanguineus temperate lineage in the infection condition. GO terms and its representation of biological process (A), and molecular function (B) obtained using level 3. Blue bars represent the number of over-represented proteins in the tropical lineage compared to the temperate lineage and red bars represented the number of under-represented proteins in the tropical lineage compared to the temperate lineage (can be interpreted as the number of proteins more represented in the temperate lineage compared to the tropical lineage), with statistical significance (p < 0.05).
Figure 6
Figure 6
Gene ontology of differentially represented proteins from salivary glands of R. sanguineus tropical lineage vs. R. sanguineus temperate lineage identified only in the infection condition. GO terms and its representation of biological process (A), and molecular function (B) obtained using level 3. Blue bars represent the number of over-represented proteins in the tropical lineage compared to the temperate lineage and red bars represented the number of under-represented proteins in the tropical lineage compared to the temperate lineage (can be interpreted as the number of proteins more represented in the temperate lineage compared to the tropical lineage), with statistical significance (p < 0.05).
Figure 7
Figure 7
Gene ontology of differentially represented proteins from midgut of R. sanguineus tropical lineage vs. R. sanguineus temperate lineage identified only in the infection condition. GO terms and its representation of biological process (A), and molecular function (B) obtained using level 3. Blue bars represent the number of over-represented proteins in the tropical lineage compared to the temperate lineage and red bars represented the number of under-represented proteins in the tropical lineage compared to the temperate lineage (can be interpreted as the number of proteins more represented in the temperate lineage compared to the tropical lineage), with statistical significance (p < 0.05).
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