Tobias Engl

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Author Correction: Inhibition of a nutritional endosymbiont by glyphosate abolishes mutualistic benefit on cuticle synthesis in Oryzaephilus surinamensis

Communications Biology

The original version of the Article included an error in reporting the glyphosate concentration u... more The original version of the Article included an error in reporting the glyphosate concentration used in previous work. The "Glyphosate and aromatic amino acid supplementation" section of the methods incorrectly stated a previously reported value of 250 mg glyphosate applied per 48L of soil 90 as 250 g glyphosate per 48L of soil, leading to the overestimation of the concentration as 0.4% instead of the correct 0.0004%. This sentence should read "Helander et al. report 250 mg per 48 L of soil to be equivalent to the maximum recommended amount of glyphosate for agronomical applications which translates to 0.0004% based on a fertile soil density of 1.3 g/cm³ 90 ." This has been corrected in both the PDF and HTML versions of the Article.

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Incipient genome erosion and metabolic streamlining for antibiotic production in a defensive symbiont

Proceedings of the National Academy of Sciences

Genome erosion is a frequently observed result of relaxed selection in insect nutritional symbion... more Genome erosion is a frequently observed result of relaxed selection in insect nutritional symbionts, but it has rarely been studied in defensive mutualisms. Solitary beewolf wasps harbor an actinobacterial symbiont of the genus Streptomyces that provides protection to the developing offspring against pathogenic microorganisms. Here, we characterized the genomic architecture and functional gene content of this culturable symbiont using genomics, transcriptomics, and proteomics in combination with in vitro assays. Despite retaining a large linear chromosome (7.3 Mb), the wasp symbiont accumulated frameshift mutations in more than a third of its protein-coding genes, indicative of incipient genome erosion. Although many of the frameshifted genes were still expressed, the encoded proteins were not detected, indicating post-transcriptional regulation. Most pseudogenization events affected accessory genes, regulators, and transporters, but “Streptomyces philanthi” also experienced mutatio...

Metabolic Cost of a Nutritional Symbiont Manifests in Delayed Reproduction in a Grain Pest Beetle

Insects

Animals engage in a plethora of mutualistic interactions with microorganisms that can confer vari... more Animals engage in a plethora of mutualistic interactions with microorganisms that can confer various benefits to their host but can also incur context-dependent costs. The sawtoothed grain beetle Oryzaephilus surinamensis harbors nutritional, intracellular Bacteroidetes bacteria that supplement precursors for the cuticle synthesis and thereby enhance desiccation resistance of its host. Experimental elimination of the symbiont impairs cuticle formation and reduces fitness under desiccation stress but does not disrupt the host’s life cycle. For this study, we first demonstrated that symbiont populations showed the strongest growth at the end of metamorphosis and then declined continuously in males, but not in females. The symbiont loss neither impacted the development time until adulthood nor adult mortality or lifespan. Furthermore, lifetime reproduction was not influenced by the symbiont presence. However, symbiotic females started to reproduce almost two weeks later than aposymbiot...

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Nitric oxide radicals are emitted by wasp eggs to kill mold fungi

Detrimental microbes caused the evolution of a great diversity of antimicrobial defenses in plant... more Detrimental microbes caused the evolution of a great diversity of antimicrobial defenses in plants and animals. Here we show that the eggs of a solitary digger wasp, the European beewolf Philanthus triangulum, emit large amounts of the gaseous free radical nitric oxide (NO.) to protect themselves and their provisions, paralyzed honeybees, against mold fungi. Despite the extraordinary concentrations of nitrogen radicals (NO. and its oxidation product NO2.) in the brood cells (~1500ppm), NO. is synthesized from L-arginine by an NO-synthase (NOS) as in other animals. The beewolf NOS gene revealed no conspicuous differences to related species. However, due to alternative splicing, the NOS-mRNA in beewolf eggs lacks a 144bp exon near the regulatory domain. This preventive external application of high doses of NO. by seemingly defenseless wasp eggs represents an evolutionary key innovation that adds a remarkable novel facet to the array of functions of the important biological effector NO..

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Effect of antibiotic treatment and gamma-irradiation on cuticular hydrocarbon profiles and mate choice in tsetse flies (Glossina m. morsitans)

BMC Microbiology

Background: Symbiotic microbes represent a driving force of evolutionary innovation by conferring... more Background: Symbiotic microbes represent a driving force of evolutionary innovation by conferring novel ecological traits to their hosts. Many insects are associated with microbial symbionts that contribute to their host's nutrition, digestion, detoxification, reproduction, immune homeostasis, and defense. In addition, recent studies suggest a microbial involvement in chemical communication and mating behavior, which can ultimately impact reproductive isolation and, hence, speciation. Here we investigated whether a disruption of the microbiota through antibiotic treatment or irradiation affects cuticular hydrocarbon profiles, and possibly mate choice behavior in the tsetse fly, Glossina morsitans morsitans. Four independent experiments that differentially knock down the multiple bacterial symbionts of tsetse flies were conducted by subjecting tsetse flies to ampicillin, tetracycline, or gammairradiation and analyzing their cuticular hydrocarbon profiles in comparison to untreated controls by gas chromatographymass spectrometry. In two of the antibiotic experiments, flies were mass-reared, while individual rearing was done for the third experiment to avoid possible chemical cross-contamination between individual flies. Results: All three antibiotic experiments yielded significant effects of antibiotic treatment (particularly tetracycline) on cuticular hydrocarbon profiles in both female and male G. m. morsitans, while irradiation itself had no effect on the CHC profiles. Importantly, tetracycline treatment reduced relative amounts of 15,19,23-trimethylheptatriacontane, a known compound of the female contact sex pheromone, in two of the three experiments, suggesting a possible implication of microbiota disturbance on mate choice decisions. Concordantly, both female and male flies preferred non-treated over tetracycline-treated flies in direct choice assays. Conclusions: While we cannot exclude the possibility that antibiotic treatment had a directly detrimental effect on fly vigor as we are unable to recolonize antibiotic treated flies with individual symbiont taxa, our results are consistent with an effect of the microbiota, particularly the obligate nutritional endosymbiont Wigglesworthia, on CHC profiles and mate choice behavior. These findings highlight the importance of considering host-microbiota interactions when studying chemical communication and mate choice in insects.

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Ancient symbiosis confers desiccation resistance to stored grain pest beetles

Molecular Ecology

Symbiont-Driven Male Mating Success in the Neotropical Drosophila paulistorum Superspecies

Behavior Genetics

Microbial symbionts are ubiquitous associates of living organisms but their role in mediating rep... more Microbial symbionts are ubiquitous associates of living organisms but their role in mediating reproductive isolation (RI) remains controversial. We addressed this knowledge gap by employing the Drosophila paulistorum-Wolbachia model system. Semispecies in the D. paulistorum species complex exhibit strong RI between each other and knockdown of obligate mutualistic Wolbachia bacteria in female D. paulistorum flies triggers loss of assortative mating behavior against males carrying incompatible Wolbachia strains. Here we set out to determine whether de novo RI can be introduced by Wolbachiaknockdown in D. paulistorum males. We show that Wolbachia-knockdown D. paulistorum males (i) are rejected as mates by wild type females, (ii) express altered sexual pheromone profiles, and (iii) are devoid of the endosymbiont in pheromone producing cells. Our findings suggest that changes in Wolbachia titer and tissue tropism can induce de novo premating isolation by directly or indirectly modulating sexual behavior of their native D. paulistorum hosts.

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Evolutionary stability of antibiotic protection in a defensive symbiosis

Proceedings of the National Academy of Sciences of the United States of America, Jan 27, 2018

The increasing resistance of human pathogens severely limits the efficacy of antibiotics in medic... more The increasing resistance of human pathogens severely limits the efficacy of antibiotics in medicine, yet many animals, including solitary beewolf wasps, successfully engage in defensive alliances with antibiotic-producing bacteria for millions of years. Here, we report on the in situ production of 49 derivatives belonging to three antibiotic compound classes (45 piericidin derivatives, 3 streptochlorin derivatives, and nigericin) by the symbionts of 25 beewolf host species and subspecies, spanning 68 million years of evolution. Despite a high degree of qualitative stability in the antibiotic mixture, we found consistent quantitative differences between species and across geographic localities, presumably reflecting adaptations to combat local pathogen communities. Antimicrobial bioassays with the three main components and in silico predictions based on the structure and specificity in polyketide synthase domains of the piericidin biosynthesis gene cluster yield insights into the me...

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Love at first sniff: a spermatophore-associated pheromone mediates partner attraction in a collembolan species

Animal Behaviour

Keywords: indirect sperm transfer sex pheromone sexual chemical communication spermatophore sprin... more Keywords: indirect sperm transfer sex pheromone sexual chemical communication spermatophore springtails Mate choice is essential in most animals, as a good choice of mating partner largely determines reproductive success. Much evidence shows that olfactory cues play an important role in mate choice. However, the integration of chemical, visual and acoustic cues, often used when both partners meet, makes it hard to test whether olfaction alone can mediate reproductive decisions. Interestingly, several invertebrates have adopted a mating system where males deposit their sperm (packed in spermato-phores) in the environment for females to pick up with no visual contact between the sexes. In this case the male cue is conveyed by the spermatophore only. Earlier studies on a species with indirect sperm transfer, the soil arthropod Orchesella cincta, showed that, even in these animals, female choice exists. In this study, we tested whether chemical cues provided by the spermatophores mediate this female choice. Chemical analysis of spermatophore extracts revealed that (Z)-14-tricosenol is the main compound in the male spermatophores and this compound attracted females in olfactometer bioassays. Our finding suggests that (Z)-14-tricosenol is thus a pheromone component, which is sufficient for female attraction. This is the first report of a spermatophore-associated sex pheromone in a species performing indirect sperm transfer.

The digestive and defensive basis of carcass utilization by the burying beetle and its microbiota

Nature communications, Jan 9, 2017

Insects that use ephemeral resources must rapidly digest nutrients and simultaneously protect the... more Insects that use ephemeral resources must rapidly digest nutrients and simultaneously protect them from competitors. Here we use burying beetles (Nicrophorus vespilloides), which feed their offspring on vertebrate carrion, to investigate the digestive and defensive basis of carrion utilization. We characterize gene expression and microbiota composition in the gut, anal secretions, and on carcasses used by the beetles. We find a strict functional compartmentalization of the gut involving differential expression of immune effectors (antimicrobial peptides and lysozymes), as well as digestive and detoxifying enzymes. A distinct microbial community composed of Firmicutes, Proteobacteria and a clade of ascomycetous yeasts (genus Yarrowia) is present in larval and adult guts, and is transmitted to the carcass via anal secretions, where the yeasts express extracellular digestive enzymes and produce antimicrobial compounds. Our results provide evidence of potential metabolic cooperation bet...

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Fungi and NO defense?Mycoflora in brood cells of the European Beewolf and its radical defense

The composition of cuticular compounds indicates body parts, sex and age in the model butterfly Bicyclus anynana (Lepidoptera)

Frontiers in Ecology and Evolution, 2014

Chemical communication in insects' sexual interactions is well-known to involve olfaction of vola... more Chemical communication in insects' sexual interactions is well-known to involve olfaction of volatile compounds called sex pheromones. In theory, sexual chemical communication may also involve chemicals with low or no volatility exchanged during precopulatory gustatory contacts. Yet, knowledge on this latter type of chemicals is so far mostly restricted to the Drosophila fly model. Here we provide the most comprehensive characterization to date of the cuticular chemical profile, including both volatile and non-volatile compounds, of a model butterfly, Bicyclus anynana. First, we characterized the body distribution of 103 cuticular lipids, mostly alkanes and methyl-branched alkanes, by gas chromatography coupled to mass spectrometry (GC-MS). Second, we developed a multivariate statistical approach to cope with such complex chemical profiles and showed that variation in the presence or abundance of a subset of the cuticular lipids indicated body parts, and traits involved in B. anynana mate choice, namely sex and age. Third, we identified the chemical structure of the 20 most indicative compounds, which were on average more abundant (1346.4 ± 1994.6 ng; mean ± SD) than other, likely less indicative, compounds (225.9 ± 507.2 ng; mean ± SD). Fourth, we showed that wings and legs displayed most of the chemical information found on the entire body of the butterflies. Fifth, we showed that non-random gustatory contacts occurred between specific male and female body parts during courtship. The body parts mostly touched by the conspecific displayed the largest between-sex differentiation in cuticular composition. Altogether, the large diversity of cuticular lipids in B. anynana, which exceeds the one of Drosophila flies, and its non-random distribution and evaluation across individuals, together suggest that gustatory information is likely exchanged during sexual interactions in Lepidoptera.

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Defensive symbioses of animals with prokaryotic and eukaryotic microorganisms

Natural product reports, Jan 20, 2015

Covering: through 2014Many organisms team up with microbes for defense against predators, parasit... more Covering: through 2014Many organisms team up with microbes for defense against predators, parasites, parasitoids, or pathogens. Here we review the described protective symbioses between animals (including marine invertebrates, nematodes, insects, and vertebrates) and bacteria, fungi, and dinoflagellates. We focus on associations where the microbial natural products mediating the protective activity have been elucidated or at least strong evidence for the role of symbiotic microbes in defense is available. In addition to providing an overview of the known defensive animal-microbe symbioses, we aim to derive general patterns on the chemistry, ecology, and evolution of such associations.

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Defensive microbial symbionts in Hymenoptera

Functional Ecology, 2014

ABSTRACT In all stages of their life cycle, insects are threatened by a multitude of predators, p... more ABSTRACT In all stages of their life cycle, insects are threatened by a multitude of predators, parasites, parasitoids and pathogens. The lifestyles and feeding ecologies of some hymenopteran taxa render them especially vulnerable to pathogen infestation. Specifically, development in sub-terranean brood cells, mass provisioning of resources for the offspring and the life of social insects in large communities can enhance the risk of pathogen infestation and/or the spread of disease among conspecifics.To counteract these threats, insects have evolved mechanical, chemical and behavioural defences as well as a complex immune system. In addition to the host&#39;s own defences, some Hymenoptera are associated with protective symbionts. Leaf-cutting ants, solitary digger wasps, bees and bumblebees engage in symbiotic interactions with bacteria that protect the adult host, the developing offspring or the food resources against microbial infections. In the well-studied cases of ants and wasps, the protective activity is mediated by the production of antimicrobial secondary metabolites. In other symbiotic interactions, however, competitive exclusion and immune priming may also play an important role in enhancing protection. Phylogenetic studies indicate that the defensive associations in Hymenoptera are generally more dynamic than the intimate nutritional mutualisms, with horizontal transfer or de novo uptake of the symbionts from the environment occurring frequently.Mutualistic micro-organisms can also significantly influence the outcome of host-parasitoid interactions. Some insects are protected by symbiont-produced toxins against parasitic wasps. Ichneumonid and braconid parasitoids, on the other hand, are associated with symbiotic viruses that are injected into the caterpillar host during oviposition and suppress its immune system to the advantage of the parasitoid.The increasing affordability of next-generation sequencing technologies will greatly facilitate the analysis of insect-associated microbial communities and undoubtedly uncover a plethora of as yet unknown protective symbioses. However, a detailed understanding of the host&#39;s natural history is indispensable for elucidating the fitness benefits of the symbionts and the molecular basis of symbiont-conferred protection.

Cryptic combat against competing microbes is a costly component of parental care in a digger wasp

Animal Behaviour, 2011

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