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Abstract

The coffee berry borer (Hypothenemus hampei) is the most devastating insect pest of coffee worldwide with its infestations decreasing crop yield by up to 80%. Caffeine is an alkaloid that can be toxic to insects and is hypothesized to act as a defence mechanism to inhibit herbivory. Here we show that caffeine is degraded in the gut of H. hampei, and that experimental inactivation of the gut microbiota eliminates this activity. We demonstrate that gut microbiota in H. hampei specimens from seven major coffee-producing countries and laboratory-reared colonies share a core of microorganisms. Globally ubiquitous members of the gut microbiota, including prominent Pseudomonas species, subsist on caffeine as a sole source of carbon and nitrogen. Pseudomonas caffeine demethylase genes are expressed in vivo in the gut of H. hampei, and re-inoculation of antibiotic-treated insects with an isolated Pseudomonas strain reinstates caffeine-degradation ability confirming their key role.
Corrections & amendments
Publisher Correction: Gut microbiota mediate caffeine
detoxication in the primary insect pest of coffee
Javier A. Ceja-Navarro, Fernando E. Vega, Ulas Karaoz, Zhao Hao, Stefan Jenkins,
Hsiao Chien Lim, Petr Kosina, Francisco Infante, Trent R. Northen & Eoin L. Brodie
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Correction to: Nature Communications
https://doi.org/10.1038/ncomms8618,
published online 14 July 2015
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Supplementary resources (13)

... Gut symbiotic bacteria aid Dendroctonus valens to live on pine by degrading the pine phloem enriched deterrent carbohydrate D-pinitol . Similarly, gut microbiota can help the primary insect pest of coffee, Hylobius abietis degrade caffeine (Ceja-Navarro et al. 2015). Eliminating gut microbiota by antibiotic treatment significantly abolished the caffeine detoxification ability of H. abietis, thereby impairing its reproductive fitness (Ceja-Navarro et al. 2015). ...
... Similarly, gut microbiota can help the primary insect pest of coffee, Hylobius abietis degrade caffeine (Ceja-Navarro et al. 2015). Eliminating gut microbiota by antibiotic treatment significantly abolished the caffeine detoxification ability of H. abietis, thereby impairing its reproductive fitness (Ceja-Navarro et al. 2015). In Lepidoptera, the gut bacterial community is linked to host plants/diet. ...
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... The main reason for this is that Pseudomonas fulva, a gut symbiont of H. hampei, can assist the host in degrading caffeine. 53 Curculio chinensis is an obligate seed www.soci.org S Han, MR Akhtar, X Xia wileyonlinelibrary.com/journal/ps ...
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... Characterization of insect-vectored plant diseases is one of the advancements in monitoring the spread of protruding species (Badial et al., 2018). The phytochemical malfunction by the involvement of insect microbiomes has been discovered and the role of the insect microbial community in plant chemical mortification has also been discovered (Ceja-Navarro et al., 2015;Brown et al., 2014). HTDS also makes it easy to build up more sturdy trophic interlinking models by sequencing different species and chemicals like pollen and honey (Derocles et al., 2018;Lefort et al., 2017). ...
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... CBB differs from other Hypothenemus species (and other coffee-related insect pests) in its ability to feed and complete its life cycle inside the coffee seed. CBB has this unique ability because it can detoxify caffeine and use it as a source of carbon and nitrogen due to an association with a gut microbiome, which is rich in Pseudomonas bacteria (Ceja-Navarro et al. 2015). ...
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The coffee berry borer (Hypothenemus hampei) is the most devastating insect pest of coffee worldwide with its infestations decreasing crop yield by up to 80%. Caffeine is an alkaloid that can be toxic to insects and is hypothesized to act as a defence mechanism to inhibit herbivory. Here we show that caffeine is degraded in the gut of H. hampei, and that experimental inactivation of the gut microbiota eliminates this activity. We demonstrate that gut microbiota in H. hampei specimens from seven major coffee-producing countries and laboratory-reared colonies share a core of microorganisms. Globally ubiquitous members of the gut microbiota, including prominent Pseudomonas species, subsist on caffeine as a sole source of carbon and nitrogen. Pseudomonas caffeine demethylase genes are expressed in vivo in the gut of H. hampei, and re-inoculation of antibiotic-treated insects with an isolated Pseudomonas strain reinstates caffeine-degradation ability confirming their key role.
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The most common system responses attributed to microfloral grazers (protozoa, nematodes, microarthropods) in the literature are increased plant growth, increased N uptake by plants, decreased or increased bacterial populations, increased CO"2 evolution, increased N and P mineralization, and increased substrate utilization. Based on this evidence in the literature, a conceptual model was proposed in which microfloral grazers were considered as separate state variables. To help evaluate the model, the effects of microbivorous nematodes on microbial growth, nutrient cycling, plant growth, and nutrient uptake were examined with reference to activities within and outside of the rhizosphere. Blue grama grass (Bouteloua gracilis) was grown in gnotobiotic microcosms containing sandy loam soil low in inorganic N, with or without chitin amendments as a source of organic N. The soil was inoculated with bacteria (Pseudomonas paucimobilis or P. stutzeri) or fungus (Fusarium oxysporum), with half the bacterial microcosms inoculated with bacterial-feeding nematodes (Pelodera sp. or Acrobeloides sp.) and half the fungal microcosms inoculated with fungal-feeding nematodes (Aphelenchus avenae). Similar results were obtained from both the unamended and the chitin-amended experiments. Bacteria, fungi, and both trophic groups of nematodes were more abundant in the rhizosphere than in nonrhizosphere soil. All treatments containing nematodes and bacteria had higher bacterial densities than similar treatments without nematodes. Plants growing in soil with bacteria and bacterial-feeding nematodes grew faster and initially took up more N than plants in soil with only bacteria, because of increased N mineralization by bacteria, NH"4^+-N excretion by nematodes, and greater initial exploitation of soil by plant roots. Addition of fungal-feeding nematodes did not increase plant growth or N uptake because these nematodes excreted less NH"4^+-N than did bacterial-feeding nematode populations and because the N mineralized by the fungus alone was sufficient for plant growth. Total shoot P was significantly greater in treatments with fungus or Pelodera sp. than in the sterile plant control or treatments with plants plus Pseudomonas stutzeri until the end of the experiment. The additional mineralization that occurs due to the activities of microbial grazers may be significant for increasing plant growth only when mineralization by microflora alone is insufficient to meet the plants' requirements. However, while the advantage of increased N mineralization by microbial grazers may be short-term, it may occur in many ecosystems in those short periods of ideal conditions when plant growth can occur. Thus, these results support other claims in the literature that microbial grazers may perform important regulatory functions at critical times in the growth of plants.
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The coffee berry borer, Hypothenemus hampei (Coleoptera: Curculionidae: Scolytinae), is the most devastating insect pest of coffee throughout the world. The insect is endemic to Africa but can now be found throughout nearly all coffee‐producing countries. One area of basic biology of the insect that remains unresolved is that of its alternative host plants, i.e. which fruits of plants, other than coffee, can the insect survive and reproduce in. An in‐depth survey of the literature revealed an article by Schedl listing 21 genera in 13 families in which the insect was collected, mainly in the Democratic Republic of Congo. This overlooked reference, together with information provided in other early articles, suggests that H. hampei is polyphagous, and could provide, if confirmed in the field, critical information on the evolution of this insect's diet, ecology and host range. © 2012 The Linnean Society of London, Biological Journal of the Linnean Society, 2012, ••, ••–••.
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Coarse woody debris is an important biomass pool in forest ecosystems that numerous groups of insects have evolved to take advantage of. These insects are ecologically important and represent useful natural analogs for biomass to biofuel conversion. Using a range of molecular approaches combined with microelectrode measurements of oxygen, we have characterized the gut microbiome and physiology of Odontotaenius disjunctus, a wood-feeding beetle native to the eastern United States. We hypothesized that morphological and physiological differences among gut regions would correspond to distinct microbial populations and activities. In fact, significantly different communities were found in the foregut (FG), midgut (MG)/posterior hindgut (PHG) and anterior hindgut (AHG), with Actinobacteria and Rhizobiales being more abundant toward the FG and PHG. Conversely, fermentative bacteria such as Bacteroidetes and Clostridia were more abundant in the AHG, and also the sole region where methanogenic Archaea were detected. Although each gut region possessed an anaerobic core, micron-scale profiling identified radial gradients in oxygen concentration in all regions. Nitrogen fixation was confirmed by (15)N2 incorporation, and nitrogenase gene (nifH) expression was greatest in the AHG. Phylogenetic analysis of nifH identified the most abundant transcript as related to Ni-Fe nitrogenase of a Bacteroidetes species, Paludibacter propionicigenes. Overall, we demonstrate not only a compartmentalized microbiome in this beetle digestive tract but also sharp oxygen gradients that may permit aerobic and anaerobic metabolism to occur within the same regions in close proximity. We provide evidence for the microbial fixation of N2 that is important for this beetle to subsist on woody biomass.
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— We studied sequence variation in 16S rDNA in 204 individuals from 37 populations of the land snail Candidula unifasciata (Poiret 1801) across the core species range in France, Switzerland, and Germany. Phylogeographic, nested clade, and coalescence analyses were used to elucidate the species evolutionary history. The study revealed the presence of two major evolutionary lineages that evolved in separate refuges in southeast France as result of previous fragmentation during the Pleistocene. Applying a recent extension of the nested clade analysis (Templeton 2001), we inferred that range expansions along river valleys in independent corridors to the north led eventually to a secondary contact zone of the major clades around the Geneva Basin. There is evidence supporting the idea that the formation of the secondary contact zone and the colonization of Germany might be postglacial events. The phylogeographic history inferred for C. unifasciata differs from general biogeographic patterns of postglacial colonization previously identified for other taxa, and it might represent a common model for species with restricted dispersal.
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The methodology for the unequivocal identification of caffeine and 13 possible metabolites (mono, di- and tri-N-methylated xanthine and uric acid derivatives) based on TLC, UV and mass spectrometry has been developed. Upon ip administration of caffeine-3H to the rat, 64-67% of the radioactivity was recovered in the urine over a period of 24 hr. The chloroform-methanol (9:1) extract of the urine accounted for about 37% of the administered radioactivity. Water soluble metabolites constitute approximately 30% of the injected caffeine-3H. With the aid of preparative TLC, 8.8% of unchanged caffeine and the following metabolites were isolated from chloroform-methanol extract of urine: theophylline (1.2%), theobromine (5.1%), paraxanthine (8.8%) and trace amounts of 1,3,7-trimethyluric acid and 3-methyluric acid. Two unidentified metabolites (metabolite A, 11.4% and metabolite B, 1.3%) have also been isolated. Peer Reviewed http://deepblue.lib.umich.edu/bitstream/2027.42/34002/1/0000275.pdf