An Integrative Sialomic Analysis Reveals Molecules From Triatoma sordida (Hemiptera: Reduviidae)

Abstract

Triatomines have evolved salivary glands that produce versatile molecules with various biological functions, including those leading their interactions with vertebrate hosts’ hemostatic and immunological systems. Here, using high-throughput transcriptomics and proteomics, we report the first sialome study on the synanthropic triatomine Triatoma sordida. As a result, 57,645,372 reads were assembled into 26,670 coding sequences (CDS). From these, a total of 16,683 were successfully annotated. The sialotranscriptomic profile shows Lipocalin as the most abundant protein family within putative secreted transcripts. Trialysins and Kazal-type protease inhibitors have high transcript levels followed by ubiquitous protein families and enzyme classes. Interestingly, abundant trialysin and Kazal-type members are highlighted in this triatomine sialotranscriptome. Furthermore, we identified 132 proteins in T. sordida salivary gland soluble extract through LC-MS/MS spectrometry. Lipocalins, Hemiptera specific families, CRISP/Antigen-5 and Kazal-type protein inhibitors proteins were identified. Our study provides a comprehensive description of the transcript and protein compositions of the salivary glands of T. sordida. It significantly enhances the information in the Triatominae sialome databanks reported so far, improving the understanding of the vector’s biology, the hematophagous behaviour, and the Triatominae subfamily’s evolution.

The biotechnological potential of proteases from hematophagous arthropod vectors

“…During the bite, the host suffers tissue and vascular injuries, which trigger a series of interrelated mechanisms, such as hemostasis, inflammation, and immune responses ( Ribeiro, 1987 ; Ribeiro, 1995 ). Large-scale sialotranscriptomic (salivary glands transcriptome) and sialoproteomic (salivary glands proteome) analyses have been reported for various blood-feeding arthropods ( Andersen et al., 2007 ; Arcà et al., 2007 ; Calvo et al., 2007 ; Assumpcao et al., 2008 ; Chmelar et al., 2008 ; Andersen et al., 2009 ; Alves-Silva et al., 2010 ; Schwarz et al., 2014 ; Santiago et al., 2016 ; Santiago et al., 2018 ; Praça et al., 2021 ) disclosing the saliva of hematophagous is indeed a potent pharmacologically active fluid capable of counteracting the hemostatic, inflammatory, and immune responses of the vertebrate host ( Ribeiro, 1987 ; Ribeiro, 1995 ). The comprehensive mapping of already reported sialomes (salivary glands transcriptomic and proteomic analyses) revealed different protease families are produced by salivary glands cells ( Andersen et al., 2007 ; Arcà et al., 2007 ; Calvo et al., 2007 ; Assumpcao et al., 2008 ; Chmelar et al., 2008 ; Andersen et al., 2009 ; Alves-Silva et al., 2010 ; Schwarz et al., 2014 ; Santiago et al., 2016 ; Santiago et al., 2018 ; Praça et al., 2021 ).…”

Bacteriolytic activity in saliva of the hematophagous Triatoma infestans (Reduviidae) and novel characterization and expression site of a third lysozyme

“…In the salivary glands of triatomines, several genes encoding antimicrobial peptides of different masses are expressed: defensins (4 kDa), pacifastin-like protease inhibitors (4 kDa), short-trialysins (6.1 kDa), diptericin (9 kDa), prolixicin (11 kDa), histones (13, 15 kDa), triatox (14.8 kDa), lysozymes (15 kDa), hemolysin-like proteins (16 kDa), attacins (20 kDa), and trialysins (22 kDa) (Assumpção et al, 2012;Flores-Villegas et al, 2015;Praça et al, 2022;Ribeiro et al, 2012Ribeiro et al, , 2014Salcedo-Porras & Lowenberger, 2019, 2021Santiago et al, 2020).…”

“…In the salivary glands of triatomines, several genes encoding antimicrobial peptides of different masses are expressed: defensins (4 kDa), pacifastin‐like protease inhibitors (4 kDa), short‐trialysins (6.1 kDa), diptericin (9 kDa), prolixicin (11 kDa), histones (13, 15 kDa), triatox (14.8 kDa), lysozymes (15 kDa), hemolysin‐like proteins (16 kDa), attacins (20 kDa), and trialysins (22 kDa) (Assumpção et al, 2012; Flores‐Villegas et al, 2015; Praça et al, 2022; Ribeiro et al, 2012, 2014; Salcedo‐Porras & Lowenberger, 2019, 2021; Santiago et al, 2020). So far in the saliva of different species of triatomines only one attacin, one prolixicin, one triatox, and one diptericin, but up to eight defensins, eight trialysins, and five lysozymes have been found (reviewed by Salcedo‐Porras & Lowenberger, 2019).…”