Hematophagous triatomine bugs feed also on plants and express functional amylase

Abstract

AbstractBACKGROUNDBlood feeding is a secondary adaptation in hematophagous bugs that ancestrally feed on plants. Many vector proteins are devoted to cope with the host’s 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 bugRhodnius prolixusand its related speciesR. robustus(Hemiptera, Reduviidae, Triatominae). Triatominae bugs are vectors ofTrypanosoma cruzi, the causal agent of Chagas’disease. 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 speciesR. robustuscaught on palm trees to detect traces of plant meals. We found plant DNA in over 8 % of theR. robustussamples, mostly the palm treeAttalea speciosa. Moreover, we showed that theR. robustusalpha-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 theRhodniusgenus (Hemiptera, Reduviidae), which are vectors of the Chagas’disease, an important health issue in Latin America. In this study, we evidence for the first time that sylvatic bugsR. robustusalso 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 fromAttaleapalm 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.