Pectin, an integral component of the plant cell wall, is a recalcitrant substrate against enzymatic challenges by most animals. In characterizing the source of a leaf beetle's (Cassida rubiginosa) pectin-degrading phenotype, we demonstrate its dependency on an extracellular bacterium housed in specialized organs connected to the foregut. Despite possessing the smallest genome (0.27 Mb) of any organism not subsisting within a host cell, the symbiont nonetheless retained a functional pectinolytic metabolism targeting the polysaccharide's two most abundant classes: homogalacturonan and rhamnogalacturonan I. Comparative transcriptomics revealed pectinase expression to be enriched in the symbiotic organs, consistent with enzymatic buildup in these structures following immunostaining with pectinase-targeting antibodies. Symbiont elimination results in a drastically reduced host survivorship and a diminished capacity to degrade pectin. Collectively, our findings highlight symbiosis as a strategy for an herbivore to metabolize one of nature's most complex polysaccharides and a universal component of plant tissues.
The pine weevil (Hylobius abietis), a major pest of conifer forests throughout Europe, feeds on the bark and cambium, tissues rich in terpenoid resins that are toxic to many insect herbivores. Here, we report the ability of the pine weevil gut microbiota to degrade the diterpene acids of Norway spruce. The diterpene acid levels present in ingested bark were substantially reduced on passage through the pine weevil gut. This reduction was significantly less upon antibiotic treatment, and supplementing the diet with gut suspensions from untreated insects restored the ability to degrade diterpenes. In addition, cultured bacteria isolated from pine weevil guts were shown to degrade a Norway spruce diterpene acid. In a metagenomic survey of the insect's bacterial community, we were able to annotate several genes of a previously described diterpene degradation (dit) gene cluster. Antibiotic treatment disrupted the core bacterial community of H. abietis guts and eliminated nearly all dit genes concordant with its reduction in diterpene degradation. Pine weevils reared on an artificial diet spiked with diterpenes, but without antibiotics, were found to lay more eggs with a higher hatching rate than weevils raised on diets with antibiotics or without diterpenes. These results suggest that gut symbionts contribute towards host fitness, but not by detoxification of diterpenes, as these compounds do not show toxic effects with or without antibiotics. Rather the ability to thrive in a terpene-rich environment appears to allow gut microbes to benefit the weevil in other ways, such as increasing the nutritional properties of their diet.
Among their responses to microbial infection, plants deploy an arsenal of natural antibiotic products. Historically these have been identified on the basis of their antibiotic activity in vitro, which leaves open the question of their relevance to defense in planta. The vast majority of such natural products from the important crop plant rice () are diterpenoids whose biosynthesis proceeds via either - or-copalyl diphosphate (CPP) intermediates, which were isolated on the basis of their antibiotic activity against the fungal blast pathogen However, rice plants in which the gene for the-CPP synthase is knocked out do not exhibit increased susceptibility to Here, we show that knocking out or knocking down actually decreases susceptibility to the bacterial leaf blight pathogen By contrast, genetic manipulation of the gene for the -CPP synthase alters susceptibility to both and Despite the secretion of diterpenoids dependent on or from roots, neither knockout exhibited significant changes in the composition of their rhizosphere bacterial communities. Nevertheless, rice plants allocate substantial metabolic resources toward - as well as-CPP derived diterpenoids upon infection/induction. Further investigation revealed that plays a role in fungal non-host disease resistance. Thus, examination of metabolic allocation provides important clues into physiological function.
Highlights d Stammera genomes are structurally conserved across Cassidinae species d Symbiont pectinases complement the host's endogenous cellulases and xylanases d Stammera differentially encode pectinases in their reduced genomes d Symbiont pectinolytic range reflects host plant breadth
Symbiotic interactions between insects and microorganisms are widespread in nature and are often the source of ecological innovations. In addition to supplementing their host with essential nutrients, microbial symbionts can produce enzymes that help degrade their food source as well as small molecules that defend against pathogens, parasites, and predators. As such, the study of insect ecology and symbiosis represents an important source of chemical compounds and enzymes with potential biotechnological value. In addition, the knowledge on insect symbiosis can provide novel avenues for the control of agricultural pest insects and vectors of human diseases, through targeted manipulation of the symbionts or the host-symbiont associations. Here, we discuss different insect-microbe interactions that can be exploited for insect pest and human disease control, as well as in human medicine and industrial processes. Our aim is to raise awareness that insect symbionts can be interesting sources of biotechnological applications and that knowledge on insect ecology can guide targeted efforts to discover microorganisms of applied value.
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