Hematophagous triatomine bugs feed also on plants and express functional amylase

Abstract

BACKGROUNDBlood feeding is a secondary adaptation in hematophagous bugs that ancestrally feed on plants. Many vector proteins are devoted to cope with the hosts defenses and to process the blood meal. In contrast, one can expect that some digestive enzymes devoted to phytophagous diet were lost during or after this peculiar adaptation. And yet, in many strictly hematophagous arthropods, alpha-amylases genes, coding the enzymes that digest starch from plants, are still present and transcribed, including in the blood-sucking bug Rhodnius prolixus and its related species R. robustus (Hemiptera, Reduviidae, Triatominae). Triatominae bugs are vectors of Trypanosoma cruzi, the causal agent of Chagasdisease. Besides the parasitic human infection by the vector-borne route via an exposition to infected feces, an oral route is documented by the ingestion of contaminated food or juices made from palm fruit trees. METHODOLOGY/PRINCIPAL FINDINGSWe hypothesized that retaining alpha-amylase could be advantageous if the bugs happen to consume occasionally plant tissues. To this end, we surveyed hundreds of gut DNA extracts from the sylvatic species R. robustus caught on palm trees to detect traces of plant meals. We found plant DNA in over 8 % of the R. robustus samples, mostly the palm tree Attalea speciosa. Moreover, we showed that the R. robustus alpha-amylase retained normal amylolytic activity. CONCLUSIONSPreserving alpha-amylase function could be an important way of optimally harness plant substrates, and plant feeding could be a way for bridging the gap between two blood meals. Our data indicate that plants are a common and yet underestimated food source in the wild for Triatomine. Author SummaryAdaptation to a specific diet is often accompanied by metabolic, behavioral, physiological changes and hence by genetic changes like gene family expansion, gene losses or gains. In blood-sucking insects some adaptive features such as salivary components acting against blood clotting are known. However, it is intriguing that a digestive enzyme, alpha-amylase, which digests starch, is conserved in those animals, because blood does not contain starch nor related glucose polymers. This is the case in the blood-sucking bugs of the Rhodnius genus (Hemiptera, Reduviidae), which are vectors of the Chagasdisease, an important health issue in Latin America. In this study, we evidence for the first time that sylvatic bugs R. robustus also consume plant tissues in the wild. We detected by PCR performed on DNA from digestive tract that a significant number of wild-caught individuals harbored plant DNA, especially from Attalea palm trees, on which they used to nest. We showed that the amylase enzyme is normally active on starch. We suggest plant feeding could be a way for bridging the gap between two blood meals but might not be linked to nutritional distress.