Deep-sea hydrothermal vents are among the most extreme and geochemically dynamic environments on Earth, characterized by steep gradients in temperature and chemical concentration. Alvinocaridid shrimp dominate the macrofaunal biomass at these sites and rely on their sensory systems to navigate these dark habitats. In this study, we provide the first comprehensive characterization of sensory gene repertoires associated with chemical and thermal detection in four deep-sea shrimp species occupying different ecological niches at hydrothermal vents on the Mid-Atlantic Ridge: Rimicaris exoculata, Rimicaris chacei, Mirocaris fortunata, and Alvinocaris markensis. Through de novo transcriptome assembly of sensory organs, we identified a great expansion of the variant Ionotropic Receptor (IR) family. Notably, we annotated 442 candidate IR transcripts in R. exoculata, the largest repertoire documented in any decapod crustacean. This expansion is primarily driven by the IR40a clade, suggesting adaptive radiation centred on the detection of the complex chemical waterscape of vents. Furthermore, we have identified a diverse set of Transient Receptor Potential (TRP) channels, including 18 TRPA genes in R. exoculata, which likely facilitate fine-tuned thermosensation in a high-gradient environment. In contrast, Chemosensory Proteins and Niemann-Pick type C2 proteins exhibited ubiquitous expression patterns, suggesting broader physiological roles beyond olfaction. These findings offer insights into the molecular adaptations that enable Alvinocarididae to thrive in the deep sea.

We present a chromosome-level genome assembly and annotation of the pine processionary moth, Thaumetopoea pityocampa (Lepidoptera: Notodontidae), a key forest pest that is a public health concern. The nuclear genome spans 615.9 Mb, scaffolded into 50 pseudochromosomes and 115 smaller scaffolds, with high completeness (BUSCO score: 98.9%) that provides a decisive improvement over the previous assembly (537 Mb; 68,292 contigs; BUSCO 83.6%). Coverage differences in resequenced males and females allowed identification of the Z chromosome and several W-linked contigs. As expected from previous studies, we found that synteny was largely conserved with related Lepidoptera, although chromosomal fissions may explain the higher chromosome number of 49 autosomes compared to typical lepidopteran karyotypes. We also integrated into the assembly linkage map, allowing estimation of a genome-wide male recombination rate of 5.06 cM/Mb, varying from 11.6 cM/Mb to 1.98 cM/Mb from the smallest to the largest chromosomes. Repetitive elements represented 49.1% of this new assembly, dominated by LINEs (45.1% of classified repeats). Finally, gene prediction identified 12,898 gene models, among which 17 circadian rhythm genes were manually curated. Expert annotation further allowed to identify 51 genes of the odorant receptor (OR) family as well as a total of 236 detoxification genes, including 78 CYPs, 56 CCEs, 30 GSTs, 23 UGTs and 49 ABCs. Overall, this assembly represents the first chromosome-level genome for a member of the Thaumetopoeinae subfamily, significantly expanding the currently limited set of genomic resources available for Notodontidae. The fully annotated assembly is publicly accessible through the LepidoDB database (https://bipaa.genouest.org/is/lepidodb/) and will serve as a valuable resource for research on population genomics of this species.

The impact of land-to-water transition on chemosensory genes has been explored in marine tetrapod vertebrates, with scarce data on aquatic insect lineages. Diving beetles (Dytiscidae) are predaceous freshwater insects with strictly aquatic larvae and amphibious adults. Using RNA-seq, we compared the expression of odorant receptors (ORs), gustatory receptors (GRs), ionotropic receptors (IRs), and odorant-binding proteins (OBPs) in the cephalic appendages of larval and adult Cybister lateralimarginalis . Overall, larvae expressed fewer chemosensory genes than adults but larva-specific genes displayed a unique expression pattern, not previously observed in any other holometabolous insect, with five larva-specific ORs all having a close paralogue which is adult-specific, 14 larva-specific IRs all belonging to a single gene expansion in the IR tree, and no larva-specific GR. Expression profiles across appendage types mirrored those in aerial insects, with ORs mainly in antennae, GRs in labial palps, “Antennal class” IRs in antennae, and “Divergent class” IRs in palps. This suggests that the land-to-freshwater transition in this lineage did not involve major changes in deployment of the major families of chemosensory genes among cephalic appendages. Notably, the expression of a substantial repertoire of ORs specifically in the antennae of the larva suggests that hydrophobic chemical cues are important for long-range chemodetection in freshwater, contrary to prevailing views about constraints for chemosensation within a water medium.

BackgroundTicks, hematophagous Acari, pose a significant threat by transmitting various pathogens to their vertebrate hosts during feeding. Despite advances in tick genomics, high-quality genomes were lacking until recently, particularly in the genus Ixodes, which includes the main vectors of Lyme disease.ResultsHere, we present the genome sequences of four tick species, derived from a single female individual, with a particular focus on the European species Ixodes ricinus, achieving a chromosome-level assembly. Additionally, draft assemblies were generated for the three other Ixodes species, I. persulcatus, I. pacificus, and I. hexagonus. The quality of the four genomes and extensive annotation of several important gene families have allowed us to study the evolution of gene repertoires at the level of the genus Ixodes and of the tick group. We have determined gene families that have undergone major amplifications during the evolution of ticks, while an expression atlas obtained for I. ricinus reveals striking patterns of specialization both between and within gene families. Notably, several gene family amplifications are associated with a proliferation of single-exon genes-most strikingly for fatty acid elongases and sulfotransferases.ConclusionsThe integration of our data with existing genomes establishes a solid framework for the study of gene evolution, improving our understanding of tick biology. In addition, our work lays the foundations for applied research and innovative control targeting these organisms.

Being social insects, honey bees use an array of pheromones to facilitate intraspecific communication, ensuring colony cohesion in a wide range of contexts. The honey bee represents an attractive model for studying the neurobiological basis of pheromonal processing, given that their pheromones are well characterized and their olfactory pathway has been extensively studied. Despite substantial knowledge acquired on olfactory processing in this species, the mechanism of pheromonal coding remains poorly understood. In particular, olfactory receptors (ORs) detecting social pheromones are still unknown. In this study, we used heterologous expression in the Drosophila "empty neuron system", coupled with transcuticular calcium imaging and electrophysiology. We deorphanized two odorant receptors, AmelOR136 and AmelOR109, which detect constituents of the alarm pheromone. AmelOR136 exhibits a sparse coding strategy, suggesting a finely tuned mechanism for efficient communication in alarm situations. In contrast, AmelOR109 is a more broadly-tuned receptor, responding to diverse odorants, including pheromones.

There is a growing interest in the effects of climate warming on olfaction, as temperature may affect this essential sense. In insects, the response of the olfactory system to developmental temperature might be mediated by body size or mass because body size and mass are negatively affected by developmental temperature in most ectotherms. We tested this hypothesis of a mass-mediated effect of developmental temperature on olfaction in the moth Spodoptera littoralis. We measured the olfactory sensitivity of male to female sex pheromone and five plant odors using electroantennography. We compared males reared at an optimal temperature (25 degrees C with a daily fluctuation of +/- 5 degrees C) and at a high temperature (33 +/- 5 degrees C) close to the upper limit of S. littoralis. On average, the olfactory sensitivity of males did not differ between the two developmental temperatures. However, our analyses revealed an interaction between the effects of developmental temperature and body mass on the detection of the six chemicals tested. This interaction is explained by a positive relationship between antennal sensitivity and body mass observed only with the high developmental temperature. Our results show that the effect of developmental temperature may not be detected when organism size is ignored. An interaction between the effects of developmental temperature and body mass on olfaction in a moth is explained by a positive relationship between antennal sensitivity and body mass observed only with a high temperature.

Honeybees (genus: Apis) use a plethora of pheromones for intraspecific communication. The primary compound produced by the queen’s mandibular glands, 9-ODA, is involved in mating in all Apis species. It is the ligand of the most highly expressed olfactory receptor in males of Apis mellifera: AmelOR11. Putative orthologs are found in the genomes of other Apis species: Apis dorsata, Apis florea, and Apis cerana. Modeling of OR11 proteins shows high structure conservation except for AflorOR11. Using heterologous expression in Drosophila and calcium imaging, a broad odorant screening revealed that all OR11 respond predominantly to 9-ODA, but also to secondary ligands, except AflorOR11, which remains specific to 9-ODA. Secondary ligands were confirmed by optical imaging of male antennal lobes in A. mellifera. This work supports a conserved queen sex pheromone detection channel in honeybees, albeit with an extended response spectrum possibly playing a role in reproductive isolation among species.

Glutathione transferases (GST) are detoxification enzymes that conjugate glutathione to a wide array of molecules. In the honey bee Apis mellifera, AmGSTD1 is the sole member of the delta class of GSTs, with expression in antennae. Here, we structurally and biochemically characterized AmGSTD1 to elucidate its function. We showed that AmGSTD1 can efficiently catalyse the glutathione conjugation of classical GST substrates. Additionally, AmGSTD1 exhibits binding properties with a range of odorant compounds. AmGSTD1 has a peculiar interface with a structural motif we propose to call 'sulfur sandwich'. This motif consists of a cysteine disulfide bridge sandwiched between the sulfur atoms of two methionine residues and is stabilized by CH…S hydrogen bonds and S…S sigma-hole interactions. Thermal stability studies confirmed that this motif is important for AmGSTD1 stability and, thus, could facilitate its functions in olfaction.

Many priority pollutants are concentrated in the environment due to human activity. Most are highly toxic to various organisms, including endocrine disruptors EDCs, aromatic polycyclic hydrocarbons PAHs, pesticides. While the effects of single and binary exposure have been widely explored, several pollutants can be simultaneously present at the same time in the environment, in in more or less polluted matrices. Effective pollution control requires the presence and sources of contamination to be identified. Previously we used Drosophila melanogaster to investigate metal pollution. Here, we re-used Drosophila to identify the biomarkers of pollution, and to determine if they can be used for specific types of pollution. Single and combined exposure of Bis(2-ethylhexyl) phthalate (DEHP), bisphenol A, nonylphenol, benzo(a)pyrene, and glyphosate was investigated. The impact of these pollutants on post-embryonic development and the expression pattern of 38 molecular targets were examined using qPCR. During single exposure, different profiles were observed at the molecular level. In complex mixtures, the expression profile resembled that of bisphenol A. In contrast, relatively specific gene expression profiles were obtained for the effects of each pollutant separately. While direct pollutant-gene profiling remains difficult in mixtures, molecular biology analyses enhance pollution monitoring, and should be incorporated in toxicological studies.

The primary actors in the detection of olfactory information in insects are odorant receptors (ORs), transmembrane proteins expressed at the dendrites of olfactory sensory neurons (OSNs). In order to decode the insect olfactome, many studies focus on the deorphanization of ORs (i.e., identification of their ligand), using various approaches involving heterologous expression coupled to neurophysiological recordings. The "empty neuron system" of the fruit fly Drosophila melanogaster is an appreciable host for insect ORs, because it conserves the cellular environment of an OSN. Neural activity is usually recorded using labor-intensive electrophysiological approaches (single sensillum recordings, SSR). In this study, we establish a simple method for OR deorphanization using transcuticular calcium imaging (TCI) at the level of the fly antenna. As a proof of concept, we used two previously deorphanized ORs from the cotton leafworm Spodoptera littoralis, a specialist pheromone receptor and a generalist plant odor receptor. We demonstrate that by co-expressing the GCaMP6s/m calcium probes with the OR of interest, it is possible to measure robust odorant-induced responses under conventional microscopy conditions. The tuning breadth and sensitivity of ORs as revealed using TCI were similar to those measured using single sensillum recordings (SSR). We test and discuss the practical advantages of this method in terms of recording duration and the simultaneous testing of several insects.

Glutathione transferases (GSTs) are ubiquitous enzymes that catalyze the conjugation of glutathione to various molecules. Among the 42 GSTs identified in Drosophila melanogaster, Delta and Epsilon are the largest classes, with 25 members. The Delta and Epsilon classes are involved in different functions, such as insecticide resistance and ecdysone biosynthesis. The insect GST number variability is due mainly to these classes. Thus, they are generally considered supports during the evolution for the adaptability of the insect species. To explore the link between Delta and Epsilon GST and their evolution, we analyzed the sequences using bioinformatic tools. Subgroups appear within the Delta and Epsilon GSTs with different levels of diversification. The diversification also appears in the sequences showing differences in the active site. Additionally, amino acids essential for structural stability or dimerization appear conserved in all GSTs. Quantitative real-time polymerase chain reaction (qRT-PCR) analysis revealed that the transcripts corresponding to these two classes are heterogeneously expressed within D. melanogaster. Some GSTs, such as GSTD1, are highly expressed in all tissues, suggesting their general function in detoxification. Conversely, some others, such as GSTD11 or GSTE4, are specifically expressed at a high level specifically in antennae, suggesting a potential role in olfaction.

Insects astoundingly dominate Earth’s land ecosystems and have a huge impact on human life. Almost every aspect of their life relies upon their highly efficient and adaptable chemosensory system. In the air, most chemical signals that are detected at long range are hydrophobic molecules, which insects detect using proteins encoded by multigenic families that emerged following land colonization by insect ancestors, namely the odorant-binding proteins (OBPs) and the odorant receptors (ORs). However, land-to-freshwater transitions occurred in many lineages within the insect tree of life. Whether chemosensory gene repertoires of aquatic insects remained essentially unchanged or underwent more or less drastic modifications to cope with physico-chemical constraints associated with life underwater remains virtually unknown. To address this issue, we sequenced and analyzed the transcriptome of chemosensory organs of the diving beetle Rhantus suturalis (Coleoptera, Dytiscidae). A reference transcriptome was assembled de novo using reads from five RNA-seq libraries (male and female antennae, male and female palps, and wing muscle). It contained 47,570 non-redundant unigenes encoding proteins of more than 50 amino acids. Within this reference transcriptome, we annotated sequences coding 53 OBPs, 48 ORs, 73 gustatory receptors (GRs), and 53 ionotropic receptors (IRs). Phylogenetic analyses notably revealed a large OBP gene expansion (35 paralogs in R. suturalis ) as well as a more modest OR gene expansion (9 paralogs in R. suturalis ) that may be specific to diving beetles. Interestingly, these duplicated genes tend to be expressed in palps rather than in antennae, suggesting a possible adaptation with respect to the land-to-water transition. This work provides a strong basis for further evolutionary and functional studies that will elucidate how insect chemosensory systems adapted to life underwater.

Phylloxera, Daktulosphaira vitifoliae, is an agronomic pest that feeds monophagously on grapevine, Vitis spp. host plants. Phylloxera manipulates primary and secondary plant metabolism to establish either leaf or root galls. We manually annotated 198 detoxification genes potentially involved in plant host manipulation, including cytochrome P450 (66 CYPs), carboxylesterase (20 CCEs), glutathione-S-transferase (10 GSTs), uridine diphosphate-glycosyltransferase (35 UGTs) and ABC transporter (67 ABCs) families. Transcriptomic expression patterns of these detoxification genes were analyzed for root and leaf galls. In addition to these transcriptomic analyses, we reanalyzed recent data from L1 and L2-3 stages feeding on tolerant and resistant rootstock. Data from two agricultural pest aphids, the generalist Myzus persicae and the Fabaceae specialist Acyrthosiphon pisum, and from the true bug vector of Chagas disease, Rhodnius prolixus, were used to perform phylogenetic analyses for each detoxification gene family. We found expansions of several gene sub-families in the genome of D. vitifoliae. Phylogenetically close genes were found to be organized in clusters in the same genomic position and orientation suggesting recent successive duplications. These results highlight the roles of the phylloxera detoxification gene repertoire in insect physiology and in adaptation to plant secondary metabolites, and provide gene candidates for further functional analyses.

Several molecular steps are involved in odorant detection within insect olfactory sensilla, including various proteins that could interfere with ligand-receptor interaction, either before or after ligand binding. Among these "perireceptor events", the step of signal termination is crucial to sustain the kinetics of the olfactory response. Antennal enzymes called Odorant-Degrading Enzymes (ODEs) present in the vicinity of receptors may participate in signal inactivation by rapid degradation of odorant molecules into inactive compounds, i.e. compounds that would no longer be able to activate receptors. These enzymes are also proposed to degrade excess of odorant chemicals in the sensilla in order to avoid overstimulation of the receptors, thus contributing to olfactory sensitivity and background noise reduction. ODEs could also take part in the general catabolism of odorant molecules within the sensilla, allowing chemicals to be removed from the olfactory hairs and protecting olfactory neurons from possible harmful molecules. Despite this wide range of possible roles, few antennal enzymes have been characterized as ODEs in insects, a full description implying the determination of both enzymatic activity toward odorants in vitro and participation in odorant responses in vivo, at the electrophysiological and/or behavioral level. In this chapter, we will present the pioneer works on the identification of ODEs, describe their diversity in antenna on the basis of recent transcriptomic studies, and discuss their involvement in odorant processing and termination.

Heavy metals, like many other chemical elements, are naturally present in the environment; however, the concentrations of these metals in various environmental matrices have increased through their intensive use in many human activities (such as industry, mining and agriculture). Among the heavy metals, cadmium (Cd) and mercury (Hg) induce a wide variety of defects in animals. While the effects of these heavy metals have been widely documented, a single exposure paradigm is typically used. Few studies have focused on evaluating combined exposure to these metals. However, in the environment, animals are confronted with a plethora of substances simultaneously; thus, the presence and origin of such substances must be determined to reduce the sources of contamination. Using the model of the fruit fly Drosophila melanogaster, for which many tools are readily available, we investigated how different concentrations of Cd and Hg in single and combined exposures impact post-embryonic development. In parallel, we evaluated the extended expression pattern of 38 molecular targets used as potential biomarkers of exposure through qPCR. Our results showed that both metals caused developmental delays and mortality in dose-dependent responses. Both metals were able to deregulate genes involved in hormonal control, general stress, and oxidative stress. Importantly, we confirmed synergistic interactions between Cd and Hg. Our results indicate the importance of assessing several biomarkers and their kinetics in mixtures. Drosophila represents a useful model for monitoring the toxicity of substances in polluted environments.

Most endogenous viruses, an important proportion of eukaryote genomes, are doomed to slowly decay. Little is known, however, on how they evolve when they confer a benefit to their host. Bracoviruses are essential for the parasitism success of parasitoid wasps, whose genomes they integrated ~103 million years ago. Here we show, from the assembly of a parasitoid wasp genome, for the first time at a chromosomal scale, that symbiotic bracovirus genes spread to and colonized all the chromosomes. Moreover, large viral clusters are stably maintained suggesting strong evolutionary constraints. Genomic comparison with another wasps revealed that this organization was already established ~53 mya. Transcriptomic analyses highlight temporal synchronization of viral gene expression, leading to particle production. Immune genes are not induced, however, indicating the virus is not perceived as foreign by the wasp. This recognition suggests that no conflicts remain between symbiotic partners when benefits to them converge.

The genus Spodoptera (Lepidoptera: Noctuidae) includes species that are among the most important crop pests in the world. These polyphagous species are able to feed on many plants, including corn, rice and cotton. In addition to their ability to adapt to toxic compounds produced by plants, they have developed resistance to the chemical insecticides used for their control. One of the main mechanisms developed by insects to become resistant involves detoxification enzymes. In this review, we illustrate some examples of the role of major families of detoxification enzymes such as cytochromes P450, carboxyl/cholinesterases, glutathione S-transferases (GST) and transporters such as ATP-binding cassette (ABC) transporters in insecticide resistance. We compare available data for four species, Spodoptera exigua, S. frugiperda, S. littoralis and S. litura. Molecular mechanisms underlying the involvement of these genes in resistance will be described, including the duplication of the CYP9A cluster, over-expression of GST epsilon or point mutations in acetylcholinesterase and ABCC2. This review is not intended to be exhaustive but to highlight the key roles of certain genes.

EDITORIAL article Front. Physiol., 06 September 2021 | https://doi.org/10.3389/fphys.2021.748290

An amendment to this paper has been published and can be accessed via the original article.