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The nutritional physiology of parasites is often overlooked although it is at the basis of host-parasite interactions. In the case of Varroa destructor , one of the major pests of the Western honey bee Apis mellifera , the nature of molecules and tissues ingested by the parasite is still not completely understood. Here, the V . destructor feeding biology was explored through artificial feeding, dissection of the mite’s gut and proteomic analyses. More specifically, the proteome of guts extracted from starved mites and honey bee-fed mites was compared to highlight both the parasite proteins likely involved in food processing and the honey bee proteins actually ingested by the mite. We could identify 25 V . destructor candidate proteins likely involved in the parasite digestion. As the host developmental stages infested by the mite are diverse, we also focused on the identity and on the origin of honey bee proteins ingested by the mite when it feeds on larvae, pupae or adults. We highlighted profiles of consumed honey bee proteins and their variations throughout the V . destructor life cycle. These variations matched the ones observed in the honey bee hemolymph, showing that this tissue is an important part of the mite’s diet. Based on the variations of abundance of the most consumed honey bee proteins and on their functions, the potential implication of these key candidate nutrients in V . destructor reproduction is also discussed.

Spiroplasma poulsonii is a maternally transmitted bacterial endosymbiont that is naturally associated with Drosophila melanogaster. S. poulsonii resides extracellularly in the hemolymph, where it must acquire metabolites to sustain proliferation. In this study, we find that Spiroplasma proliferation specifically depletes host hemolymph diacylglyceride, the major lipid class transported by the lipoprotein, Lpp. RNAi-mediated knockdown of Lpp expression, which reduces the amount of circulating lipids, inhibits Spiroplasma proliferation demonstrating that bacterial proliferation requires hemolymph-lipids. Altogether, our study shows that an insect endosymbiont acquires specific lipidic metabolites from the transport lipoproteins in the hemolymph of its host. In addition, we show that the proliferation of this endosymbiont is limited by the availability of hemolymph lipids. This feature could limit endosymbiont over-proliferation under conditions of host nutrient limitation as lipid availability is strongly influenced by the nutritional state. All animals host a large number of harmless microbes. Often the two partners involved in these interactions will depend on each other to thrive: microbes support important host functions and in return the host provides a safe place to live and a continuous supply of food. Many microbes that are intimately associated with animals have lost the ability to gain nutrients from sources other than their host and are unable to survive on their own. However, in many cases, the source and the type of nutrients provided to the microbes are unknown. One of the most common microbial species found in insects is Spiroplasma. This microbe lives in very large numbers in the fluid that fills the body cavities of insects, called the hemolymph. The microbes are transmitted from mother to offspring, and in some circumstances can provide benefits to the insects; for instance, Spiroplasma-infested flies appear to be protected against infection by some parasites. Unfortunately, as it is difficult to study insect–microbe relationships, little else is known about the physiological interactions between these two species. Herren et al. studied the association between Spiroplasma and the fly Drosophila melanogaster. Under normal conditions, Spiroplasma only reduces the life span of the infested fly. This indicates that Spiroplasma has a low impact on the general fitness of its host, only negatively affecting the survival and egg laying ability of old flies. When flies had limited access to nutrients, the number of Spiroplasma they carried was reduced, without the flies losing fitness. This suggests that Spiroplasma growth is dependent on something in the flies' diet. To understand which nutrients are important for the growth of Spiroplasma in Drosophila, Herren et al. analyzed the hemolymph of flies and found that there are fewer fatty-molecules, called lipids, when nutrients are limited. Healthy flies carrying Spiroplasma also have fewer lipids in their hemolymph, suggesting that these are what Spiroplasma feed on. Indeed, inactivating a protein required by the fly to transport lipids to the hemolymph reduced the growth of Spiroplasma in these flies. Herren et al. concluded that the growth of Spiroplasma inside its host is limited by the availability of lipids in the hemolymph. Since this is dependent on diet, the dependence on lipids couples the growth of Spiroplasma to the nutritional state of its host. Herren et al. speculate that this mechanism reduces the fitness cost of harboring the microbes and prevents the damaging consequence of an uncontrolled proliferation of the microbes. Moreover, Spiroplasma's preference for lipids may explain why it helps to protect flies against parasitic infection, as many parasites also rely on lipids for their growth. Herren et al. suggest this strategy could also be used in other animal–microbe associations.

Pressures on honey bee health have substantially increased both colony mortality and beekeepers' costs for hive management across Europe. Although technological advances could offer cost-effective solutions to these challenges, there is little research into the incentives and barriers to technological adoption by beekeepers in Europe. Our study is the first to investigate beekeepers' willingness to adopt the Bee Health Card, a molecular diagnostic tool developed within the PoshBee EU project which can rapidly assess bee health by monitoring molecular changes in bees. The Bee Health Card, based on MALDI BeeTyping®, is currently on level six of the Technology Readiness Level scale, meaning that the technology has been demonstrated in relevant environments. Using an on-line survey from seven European countries, we show that beekeepers recognise the potential for the tool to improve colony health, and that targeted economic incentives, such as subsidises, may help reduce cost being a barrier to the adoption and frequent use of the tool. Based on the description of the tool, 43% of beekeepers appear to be moderately confident in the effectiveness of the Bee Health Card. This confidence could increase if the tool was easy to use and not time consuming, and a higher confidence could also contribute to raising the probability of accepting extra costs linked to it. We estimate that, in the worst-case scenario, the cost per single use of the Bee Health Card should be between €47-90 across a range of European countries, depending on the labour and postage costs. However, the monetary benefits in terms of honey production could exceed this. In order to successfully tackle colony health issues, it is recommended using the BHC five times per year, from the end to the beginning of winter. Finally, we discuss the knowledge needs for assessing beekeeper health tools in future research.

Pressures on honey bee health have substantially increased both colony mortality and beekeepers’ costs for hive management across Europe. Although technological advances could offer cost-effective solutions to these challenges, there is little research into the incentives and barriers to technological adoption by beekeepers in Europe. Our study is the first to investigate beekeepers’ willingness to adopt the Bee Health Card, a molecular diagnostic tool developed within the PoshBee EU project which can rapidly assess bee health by monitoring molecular changes in bees. The Bee Health Card, based on MALDI BeeTyping®, is currently on level six of the Technology Readiness Level scale, meaning that the technology has been demonstrated in relevant environments. Using an on-line survey from seven European countries, we show that beekeepers recognise the potential for the tool to improve colony health, and that targeted economic incentives, such as subsidises, may help reduce cost being a barrier to the adoption and frequent use of the tool. Based on the description of the tool, 43% of beekeepers appear to be moderately confident in the effectiveness of the Bee Health Card. This confidence could increase if the tool was easy to use and not time consuming, and a higher confidence could also contribute to raising the probability of accepting extra costs linked to it. We estimate that, in the worst-case scenario, the cost per single use of the Bee Health Card should be between €47–90 across a range of European countries, depending on the labour and postage costs. However, the monetary benefits in terms of honey production could exceed this. In order to successfully tackle colony health issues, it is recommended using the BHC five times per year, from the end to the beginning of winter. Finally, we discuss the knowledge needs for assessing beekeeper health tools in future research.

In a number of species, individuals exposed to pathogens can mount an immune response and transmit this immunological experience to their offspring, thereby protecting them against persistent threats. Such vertical transfer of immunity, named trans-generational immune priming (TGIP), has been described in both vertebrates and invertebrates. Although increasingly studied during the last decade, the mechanisms underlying TGIP in invertebrates are still elusive, especially those protecting the earliest offspring life stage, i.e. the embryo developing in the egg. In the present study, we combined different proteomic and transcriptomic approaches to determine whether mothers transfer a \"signal\" (such as fragments of infecting bacteria), mRNA and/or protein/peptide effectors to protect their eggs against two natural bacterial pathogens, namely the Gram-positive Bacillus thuringiensis and the Gram-negative Serratia entomophila. By taking the mealworm beetle Tenebrio molitor as a biological model, our results suggest that eggs are mainly protected by an active direct transfer of a restricted number of immune proteins and of antimicrobial peptides. In contrast, the present data do not support the involvement of mRNA transfer while the transmission of a \"signal\", if it happens, is marginal and only occurs within 24h after maternal exposure to bacteria. This work exemplifies how combining global approaches helps to disentangle the different scenarios of a complex trait, providing a comprehensive characterization of TGIP mechanisms in T. molitor. It also paves the way for future alike studies focusing on TGIP in a wide range of invertebrates and vertebrates to identify additional candidates that could be specific to TGIP and to investigate whether the TGIP mechanisms found herein are specific or common to all insect species.

The adult medicinal leech central nervous system (CNS) is capable of regenerating specific synaptic circuitry after a mechanical lesion, displaying evidence of anatomical repair within a few days and functional recovery within a few weeks. In the present work, spatiotemporal changes in molecular distributions during this phenomenon are explored. Moreover, the hypothesis that neural regeneration involves some molecular factors initially employed during embryonic neural development is tested. Imaging mass spectrometry coupled to peptidomic and lipidomic methodologies allowed the selection of molecules whose spatiotemporal pattern of expression was of potential interest. The identification of peptides was aided by comparing MS/MS spectra obtained for the peptidome extracted from embryonic and adult tissues to leech transcriptome and genome databases. Through the parallel use of a classical lipidomic approach and secondary ion mass spectrometry, specific lipids, including cannabinoids, gangliosides and several other types, were detected in adult ganglia following mechanical damage to connected nerves. These observations motivated a search for possible effects of cannabinoids on neurite outgrowth. Exposing nervous tissues to Transient Receptor Potential Vanilloid (TRPV) receptor agonists resulted in enhanced neurite outgrowth from a cut nerve, while exposure to antagonists blocked such outgrowth. The experiments on the regenerating adult leech CNS reported here provide direct evidence of increased titers of proteins that are thought to play important roles in early stages of neural development. Our data further suggest that endocannabinoids also play key roles in CNS regeneration, mediated through the activation of leech TRPVs, as a thorough search of leech genome databases failed to reveal any leech orthologs of the mammalian cannabinoid receptors but revealed putative TRPVs. In sum, our observations identify a number of lipids and proteins that may contribute to different aspects of the complex phenomenon of leech nerve regeneration, establishing an important base for future functional assays.

Varroa destructor, a major ectoparasite of the Western honey bee Apis mellifera, is a widespread pest that damages colonies in the Northern Hemisphere. Throughout their lifecycle, V. destructor females feed on almost every developmental stage of their host, from the last larval instar to the adult. The parasite is thought to feed on hemolymph and fat body, although its exact diet and nutritional requirements are poorly known. Using artificial Parafilm™ dummies, we explored the nutrition of V. destructor females and assessed their survival when fed on hemolymph from bee larvae, pupae, or adults. We compared the results with mites fed on synthetic solutions or filtered larval hemolymph. The results showed that the parasites could survive for several days or weeks on different diets. Bee larval hemolymph yielded the highest survival rates, and filtered larval plasma was sufficient to maintain the mites for 14 days or more. This cell-free solution therefore theoretically contains all the necessary nutrients for mite survival. Because some bee proteins are known to be hijacked without being digested by the parasite, we decided to run a proteomic analysis of larval honey bee plasma to highlight the most common proteins in our samples. A list of 54 proteins was compiled, including several energy metabolism proteins such as Vitellogenin, Hexamerin, or Transferrins. These molecules represent key nutrient candidates that could be crucial for V. destructor survival.

Pollinators, including Bombus terrestris, are crucial for maintaining biodiversity in ecosystems and for agriculture. Deciphering their immune response under stress conditions is a key issue for protecting these populations. To assess this metric, we analyzed the B. terrestris hemolymph as an indicator of their immune status. Hemolymph analysis was carried out using mass spectrometry, MALDI molecular mass fingerprinting was used for its effectiveness in assessing the immune status, and high-resolution mass spectrometry was used to measure the impact of experimental bacterial infections on the \"hemoproteome\". By infecting with three different types of bacteria, we observed that B. terrestris reacts in a specific way to bacterial attacks. Indeed, bacteria impact survival and stimulate an immune response in infected individuals, visible through changes in the molecular composition of their hemolymph. The characterization and label-free quantification of proteins involved in specific signaling pathways in bumble bees by bottom-up proteomics revealed differences in protein expression between the non-experimentally infected and the infected bees. Our results highlight the alteration of pathways involved in immune and defense reactions, stress, and energetic metabolism. Lastly, we developed molecular signatures reflecting the health status of B. terrestris to pave the way for diagnosis/prognosis tools in response to environmental stress.

Varroa destructor, a major ectoparasite of the Western honey bee Apis mellifera, is a widespread pest that damages colonies in the Northern Hemisphere. Throughout their lifecycle, V. destructor females feed on almost every developmental stage of their host, from the last larval instar to the adult. The parasite is thought to feed on hemolymph and fat body, although its exact diet and nutritional requirements are poorly known. Using artificial Parafilm™ dummies, we explored the nutrition of V. destructor females and assessed their survival when fed on hemolymph from bee larvae, pupae, or adults. We compared the results with mites fed on synthetic solutions or filtered larval hemolymph. The results showed that the parasites could survive for several days or weeks on different diets. Bee larval hemolymph yielded the highest survival rates, and filtered larval plasma was sufficient to maintain the mites for 14 days or more. This cell-free solution therefore theoretically contains all the necessary nutrients for mite survival. Because some bee proteins are known to be hijacked without being digested by the parasite, we decided to run a proteomic analysis of larval honey bee plasma to highlight the most common proteins in our samples. A list of 54 proteins was compiled, including several energy metabolism proteins such as Vitellogenin, Hexamerin, or Transferrins. These molecules represent key nutrient candidates that could be crucial for V. destructor survival.