Analysis of microbial communities associated with the Coffee Berry Borer and related beetles

The coffee berry borer (Hypothenemus hampei) is the most devastating insect pest of coffee worldwide. It infests crops in most coffee producing countries, and is of particular concern in developing countries where coffee comprises a significant component of gross domestic product. Of more than 850 insects that have been reported to feed on the coffee plant, H. hampei is the only insect known to exploit the caffeine-rich bean as a source of food and shelter. As a result, H. hampei infestations can directly decrease crop yield by up to 80%. Caffeine is an alkaloid that can be toxic to insects and is hypothesized to act as a defense mechanism to inhibit herbivory. Here we demonstrate for the first time that caffeine is degraded in the H. hampei gut, and that inactivation of the gut microbiota eliminates this activity. The gut microbiota in H. hampei specimens from seven major coffee producing countries and laboratory-reared colonies share a core of microorganisms with variations related to either geography or diet. We demonstrate that globally ubiquitous members of the gut microbiota can subsist on caffeine as a sole carbon and nitrogen source, with Pseudomonas species being most prominent. Pseudomonas caffeine demethylase genes are expressed in vivo in the gut of H. hampei in both field and laboratory reared specimens and re-inoculation of antibiotic treated insects with an isolated Pseudomonas strain reinstates caffeine degradation ability to these insects. Our discovery of a microbiota component to the transformation of caffeine and subsistence of H. hampei on coffee beans has important implications for understanding the metabolism and ecology of this major pest.