Many 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.
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 between the host and its microbiota for digestion, detoxification and defence that extends from the beetle's gut to its nutritional resource.
Microbial symbionts of insects provide a range of ecological traits to their hosts that are beneficial in the context of biotic interactions. However, little is known about insect symbiont-mediated adaptation to the abiotic environment, for example, temperature and humidity. Here, we report on an ancient clade of intracellular, bacteriome-located Bacteroidetes symbionts that are associated with grain and wood pest beetles of the phylogenetically distant families Silvanidae and Bostrichidae. In the saw-toothed grain beetle Oryzaephilus surinamensis, we demonstrate that the symbionts affect cuticle thickness, melanization and hydrocarbon profile, enhancing desiccation resistance and thereby strongly improving fitness under dry conditions. Together with earlier observations on symbiont contributions to cuticle biosynthesis in weevils, our findings indicate that convergent acquisitions of bacterial mutualists represented key adaptations enabling diverse pest beetle groups to survive and proliferate under the low ambient humidity that characterizes dry grain storage facilities.
Summary 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'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's natural history is indispensable for elucidating the fitness benefits of the symbionts and the molecular basis of symbiont‐conferred protection.
Covering: up to 2018 Pheromones serve as chemical signals between individuals of the same species and play important roles for mate localization and mate choice as well as other social interactions in insects. A growing body of literature indicates that microbial symbionts can modulate their hosts' chemical profiles, mate choice decisions and social behavior. This modulation can occur by the direct biosynthesis of pheromone components or the provisioning of precursors, or through general changes in the metabolite pool of the host and its resource allocation into pheromone production. Here we review and discuss the contexts in which microbial modulation of intraspecific communication in insects occurs and emphasize cases in which microbes are known to affect the involved chemistry. The described examples for a symbiotic influence on mate attraction and mate choice, aggregation, nestmate and kin recognition highlight the context-dependent costs and benefits of these symbiotic interactions and the potential for conflict and manipulation among the interacting partners. However, despite the increasing number of studies reporting on symbiont-mediated effects on insect chemical communication, experimentally validated connections between the presence of specific symbionts, changes in the host's chemistry, and behavioral effects thereof, remain limited to very few systems, highlighting the need for increased collaborative efforts between symbiosis researchers and chemical ecologists to gain more comprehensive insights into the influence of microbial symbionts on insect pheromones.
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 mechanistic basis and ecoevolutionary implications of producing a complex mixture of antimicrobial compounds in a natural setting.
Glyphosate is widely used as a herbicide, but recent studies begin to reveal its detrimental side effects on animals by targeting the shikimate pathway of associated gut microorganisms. However, its impact on nutritional endosymbionts in insects remains poorly understood. Here, we sequenced the tiny, shikimate pathway encoding symbiont genome of the sawtoothed grain beetle Oryzaephilus surinamensis. Decreased titers of the aromatic amino acid tyrosine in symbiont-depleted beetles underscore the symbionts’ ability to synthesize prephenate as the precursor for host tyrosine synthesis and its importance for cuticle sclerotization and melanization. Glyphosate exposure inhibited symbiont establishment during host development and abolished the mutualistic benefit on cuticle synthesis in adults, which could be partially rescued by dietary tyrosine supplementation. Furthermore, phylogenetic analyses indicate that the shikimate pathways of many nutritional endosymbionts likewise contain a glyphosate sensitive 5-enolpyruvylshikimate-3-phosphate synthase. These findings highlight the importance of symbiont-mediated tyrosine supplementation for cuticle biosynthesis in insects, but also paint an alarming scenario regarding the use of glyphosate in light of recent declines in insect populations.
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