Nearly 8 million people are suffering from Chagas disease in the Americas. The etiological agent, Trypanosoma cruzi, is mainly transmitted by triatomine bugs, also known as kissing or vampire bugs, which suck blood and transmit the parasite through their feces. Among these triatomine species, Rhodnius prolixus is considered the main vector, and many studies have focused on characterizing its biology, physiology, ecology and evolution. 

Interestingly, given that Rhodnius species feed almost exclusively on blood, their diet is unbalanced, and the insects can lack nutrients and vitamins that they cannot synthetize themself, such as B-vitamins. In all insects feeding exclusively on blood, symbioses with microbes producing B-vitamins (mainly biotin, riboflavin and folate) have been widely described (see review in Duron and Gottlieb 2020) and are critical for insect development and reproduction. These co-evolved relationships between blood feeders and nutritional symbionts could now be considered to develop new control methods, by targeting the ‘Achille’s heel’ of the symbiotic association (i.e., transfer of nutrient and / or control of nutritional symbiont density). But for this, it is necessary to better characterize the relationships between triatomines and their symbionts. 

R. prolixus is known to be associated with several symbionts. The extracellular gut symbiont Rhodococcus rhodnii, which reaches high bacterial densities and is almost fixed in R. prolixus populations, appears to be a nutritional symbiont under many blood sources. This symbiont can provide B-vitamins such as biotin (B7), niacin (B3), thiamin (B1), pyridoxin (B6) or riboflavin (B2) and can play an important role in the development and the reproduction of R. prolixus (Pachebat et al. (2013) and see review in Salcedo-Porras et al. (2020)). This symbiont is orally acquired through egg smearing, ensuring the fidelity of transmission of the symbiont from mother to offspring. However, as recently highlighted by Tobias et al. (2020) and Gilliland et al. (2022), other gut microbes could also participate to the provision of B-vitamins, and R. rhodnii could additionally provide metabolites (other than B-vitamins) increasing bug fitness. In the study from Filée et al., the authors focused on Wolbachia, an intracellular, maternally inherited bacterium, known to be a nutritional symbiont in other blood-sucking insects such as bedbugs (Nikoh et al. 2014), and its potential role in vitamin provision in triatomine bugs. 

After screening 17 different triatomine species from the 3 phylogenetic groups prolixus, pallescens and pictipes, they first show that Wolbachia symbionts are widely distributed in the different Rhodnius species. Contrary to R. rhodnii that were detected in all samples, Wolbachia prevalence was patchy and rarely fixed. The authors then sequenced, assembled, and compared 13 Wolbachia genomes from the infected Rhodnius species. They showed that all Wolbachia are phylogenetically positioned in the supergroup F that contains wCle (the Wolbachia from bedbugs). In addition, 8 Wolbachia strains (out of 12) encode a biotin operon under strong purifying selection, suggesting the preservation of the biological function and the metabolic potential of Wolbachia to supplement biotin in their Rhodnius host. From the study of insect genomes, the authors also evidenced several horizontal transfers of genes from Wolbachia to Rhodnius genomes, which suggests a complex evolutionary interplay between vampire bugs and their intracellular symbiont. 

This nice piece of work thus provides valuable information to the fields of multiple partners / nutritional symbioses and Wolbachia research. Dual symbioses described in insects feeding on unbalanced diets generally highlight a certain complementarity between symbionts that ensure the whole nutritional complementation. The study presented by Filée et al. leads rather to consider the impact of multiple symbionts with different lifestyles and transmission modes in the provision of a specific nutritional benefit (here, biotin). Because of the low prevalence of Wolbachia in certain species, a “ménage à trois” scenario would rather be replaced by an “open couple”, where the host relationship with new symbiotic partners (more or less stable at the evolutionary timescale) could provide benefits in certain ecological situations. The results also support the potential for Wolbachia to evolve rapidly along a continuum between parasitism and mutualism, by acquiring operons encoding critical pathways of vitamin biosynthesis.

References

Duron O. and Gottlieb Y. (2020) Convergence of Nutritional Symbioses in Obligate Blood Feeders. Trends in Parasitology 36(10):816-825. https://doi.org/10.1016/j.pt.2020.07.007

Filée J., Agésilas-Lequeux K., Lacquehay L., Bérenger J.-M., Dupont L., Mendonça V., Aristeu da Rosa J. and Harry M. (2023) Wolbachia genomics reveals a potential for a nutrition-based symbiosis in blood-sucking Triatomine bugs. bioRxiv, 2022.09.06.506778, ver. 3 peer-reviewed and recommended by Peer Community in Evolutionary Biology. https://doi.org/10.1101/2022.09.06.506778

Gilliland C.A. et al. (2022) Using axenic and gnotobiotic insects to examine the role of different microbes on the development and reproduction of the kissing bug Rhodnius prolixus (Hemiptera: Reduviidae). Molecular Ecology. https://doi.org/10.1111/mec.16800

Nikoh et al. (2014) Evolutionary origin of insect–Wolbachia nutritional mutualism. PNAS. 111(28):10257-10262. https://doi.org/10.1073/pnas.1409284111

Pachebat, J.A. et al. (2013). Draft genome sequence of Rhodococcus rhodnii strain LMG5362, a symbiont of Rhodnius prolixus (Hemiptera, Reduviidae, Triatominae), the principle vector of Trypanosoma cruzi. Genome Announc. 1(3):e00329-13. https://doi.org/10.1128/genomea.00329-13

Salcedo-Porras N., et al. (2020). The role of bacterial symbionts in Triatomines: an evolutionary perspective. Microorganisms. 8:1438. https://doi.org/10.3390%2Fmicroorganisms8091438

Tobias N.J., Eberhard F.E., Guarneri A.A. (2020) Enzymatic biosynthesis of B-complex vitamins is supplied by diverse microbiota in the Rhodnius prolixus anterior midgut following Trypanosoma cruzi infection. Computational and Structural Biotechnology Journal. 3395-3401. https://doi.org/10.1016/j.csbj.2020.10.031 

Viruses establish intimate relationships with the cells they infect. The virocell is a novel entity, different from the original host cell and beyond the mere combination of viral and cellular genetic material. In these close encounters, viral and cellular genomes often hybridise, combine, recombine, merge and excise. Such chemical promiscuity leaves genomics scars that can be passed on to descent, in the form of deletions or duplications and, importantly, insertions and back and forth exchange of genetic material between viruses and their hosts.
In this preprint [1], Di Giovanni and coworkers report the identification of 13 genes present in the extant genomes of members of the Leptopilina wasp genus, bearing sound signatures of having been horizontally acquired from an ancestral virus. Importantly the authors identify Leptopilina boulardi filamentous virus (LbFV) as an extant relative of the ancestral virus that served as donor for the thirteen horizontally transferred genes. While pinpointing genes with a likely possible viral origin in eukaryotic genomes is only relatively rare, identifying an extant viral lineage related to the ancestral virus that continues to infect an extant relative of the ancestral host is remarkable. But the amazing evolutionary history of the Leptopilina hosts and these filamentous viruses goes beyond this shared genes. These wasps are endoparasitoids of Drosophila larvae, the female wasp laying the eggs inside the larvae and simultaneously injecting venom that hinders the immune response. The composition of the venoms is complex, varies between wasp species and also between individuals within a species, but a central component of all these venoms are spiked structures that vary in morphology, symmetry and size, often referred to as virus-like particles (VLPs).
In this preprint, the authors convincingly show that the expression pattern in the Leptopilina wasps of the thirteen genes identified to have been horizontally acquired from the LbFV ancestor coincides with that of the production of VLPs in the female wasp venom gland. Based on this spatio-temporal match, the authors propose that these VLPs have a viral origin. The data presented in this preprint will undoubtedly stimulate further research on the composition, function, origin, evolution and diversity of these VLP structures, which are highly debated (see for instance [2] and [3]).

References

[1] Di Giovanni, D., Lepetit, D., Boulesteix, M., Ravallec, M., & Varaldi, J. (2018). A behavior-manipulating virus relative as a source of adaptive genes for parasitoid wasps. bioRxiv, 342758, ver. 5 peer-reviewed and recommended by PCI Evol Biol. doi: 10.1101/342758
[2] Poirié, M., Colinet, D., & Gatti, J. L. (2014). Insights into function and evolution of parasitoid wasp venoms. Current Opinion in Insect Science, 6, 52-60. doi: 10.1016/j.cois.2014.10.004
[3] Heavner, M. E., Ramroop, J., Gueguen, G., Ramrattan, G., Dolios, G., Scarpati, M., ... & Govind, S. (2017). Novel organelles with elements of bacterial and eukaryotic secretion systems weaponize parasites of Drosophila. Current Biology, 27(18), 2869-2877. doi: 10.1016/j.cub.2017.08.019