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Filee, J.

Publications and source records attributed to Filee, J..

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Hematophagous triatomine bugs feed also on plants and express functional amylase

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.

ecology↗

The genome of the bee louse fly reveals deep convergences in the evolution of social inquilinism

The nests of social insects often harbor a rich fauna of intruders known as inquilines.1 Social inquilines are usually closely-related to their host due to potential genetic predispositions,2,3 but how phylogenetically distant non-social inquilines adapt to their hosts remains unclear. Here, we analyzed the genome of the wingless and blind bee louse fly Braula coeca, an inquiline kleptoparasite of the Western honey bee Apis mellifera.4,5 Using large phylogenomic data, we confirmed recent accounts that the bee louse fly is an aberrant drosophilid,6,7 and showed that it had likely evolved from a sap-breeder ancestor associated with honeydew and scale insects wax. Unlike many parasites, such as the human louse, the bee louse fly genome did not show significant erosion or strict reliance on an endosymbiont, likely due to a relatively recent age of inquilinism. However, a striking parallel evolution in a set of gene families was observed between the honey bee and the bee louse fly. Convergences included genes potentially involved in metabolism and immunity and the loss of nearly all bitter-tasting gustatory receptors in agreement with life in a protective nest and a major diet of honey, pollen, and beeswax. Vision-related and odorant receptor genes also exhibited rapid losses. Only genes whose orthologs in the closely related Drosophila melanogaster respond to honey bee pheromones components or floral aroma were retained, whereas the losses included orthologous receptors responsive to the anti-ovarian honey bee queen pheromones. These results indicate that deep genomic convergences can underlie major morphological and neuroethological transitions during the evolution of inquilinism between non-social parasites and their social hosts.

evolutionary biology↗

Wolbachia genomics support a tripartite nutritional symbiosis in blood-sucking Triatomine bugs

The nutritional symbiosis promoted by bacteria is a key determinant for adaptation and evolution of many insect lineages. A complex form of nutritional mutualism that arose in blood-sucking insects critically depends on diverse bacterial symbionts that supplement the diet of their nutrient-poor hosts with B vitamins. For instance, the triatomine bug Rhodnius prolixus, one of the main vectors of the Chagas disease in humans, is known to maintain a nutritional symbiosis with the gut symbionts Rhodococcus rhodnii. In this study, we show that Wolbachia symbionts are also widely distributed in the Rhodnius genus. We have screened a large set of Rhodnius blood-sucking bugs samples belonging to 17 different species and to the three phylogenetic groups, prolixus, pallescens and pictipes. We assembled 13 genomes of Wolbachia infecting eight Rhodnius species from prolixus and pictipes groups. We demonstrate that these Wolbachia belong to supergroup F and are closely related to Wolbachia infecting the bedbug Cimex lectularius (wCle). Although bedbugs and triatomines are very distantly related hemipteran bugs, the genomes of their respective Wolbachia were highly similar, suggesting recent horizontal host switches. We also show that Rhodnius Wolbachia genomes infecting the prolixus group encode intact biotin operon, the hallmark of nutritional symbiosis in bedbugs. This operon is lacking from all the other Wolbachia infecting R. pictipes. Finally, host genome analyses provide evidence of massive Wolbachia-to-Rhodnius gene transfers in almost samples, providing footprints of past infections that support a widespread and probably ancient symbiotic association between Wolbachia and triatomine bugs. Our results suggest that both Wolbachia and R. rhodnii gut symbionts and their Rhodnius host maintain a highly prevalent symbiotic relationship, in which the vertically-inherited Wolbachia has the metabolic potantial to ensure or complement, the nutritional mutualism provided by the gut symbionts. Specific loss of the biotin operon in some symbiont genomes suggests that the boundaries between obligatory mutualism, facultative mutualism and parasitism in Wolbachia are transient and fluid, supporting a dynamic process of transition and reversion from one state to another.

evolutionary biology↗

Bacterial origin of thymidylate and folate metabolism in Asgard Archaea

Little is known about the evolution and biosynthetic function of DNA precursor and the folate metabolism in the Asgard group of archaea. As Asgard occupy a key position in the archaeal and eukaryotic phylogenetic trees, we have exploited very recently emerged genome and metagenome sequence information to investigate these central metabolic pathways. Our genome-wide analyses revealed that the recently cultured Asgard archaeon Candidatus Prometheoarchaeum syntrophicum strain MK-D1 (Psyn) contains a complete folate-dependent network for the biosynthesis of DNA/RNA precursors, amino acids and syntrophic amino acid utilization. Altogether our experimental and computational data suggest that phylogenetic incongruences of functional folate-dependent enzymes from Asgard archaea reflect their persistent horizontal transmission from various bacterial groups, which has rewired the key metabolic reactions in an important and recently identified archaeal phylogenetic group. We also experimentally validated the functionality of the lateral gene transfer of Psyn thymidylate synthase ThyX. This enzyme uses bacterial-like folates efficiently and is inhibited by mycobacterial ThyX inhibitors. Our data raise the possibility that the thymidylate metabolism, required for de novo DNA synthesis, originated in bacteria and has been independently transferred to archaea and eukaryotes. In conclusion, our study has revealed that recent prevalent lateral gene transfer has markedly shaped the evolution of Asgard archaea by allowing them to adapt to specific ecological niches.

microbiology↗

The natural history of the black soldier fly, Hermetia illucens: insights from complete mitochondrial genome sequences

The Black Soldier Fly (BSF) Hermetia illucens is a cosmopolitan fly heavily used by industrial companies to reduce biowaste and produce protein and fat for poultry and aquaculture feed. However, the natural history and the genetic diversity of the BSF is poorly known. In this study, we analysed 677 CO1 sequences derived from samples found all over the five continents leading us to the discovery of 52 haplotypes including 10 major haplotypes. We refined the definition of these haplotypes by sequencing 59 mitochondrial genomes. We could derive an estimate of the separation events of the different haplotypes at more than two million years for the oldest branches. This worldwide cryptic genetic and genomic diversity is mirrored at local scale in France in which we found five major haplotypes sometimes in sympatry. Our data resolve the phylogenetic relationships between the major lineages and give insights into the dispersal and the numbers of BSF neo-introduction at global and local scales. Our results indicate that the genetic and genomic diversity of commercial BSF stock is very low and these brood stock participated in the dissemination of the BSF in the wild. Taken together these results call for a better understanding of the genomic diversity of the BSF to unravel possible specific adaptations of the different lineages for industrial needs and to initiate the selection process.

evolutionary biology↗