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ARS Home » Northeast Area » Beltsville, Maryland (BARC) » Beltsville Agricultural Research Center » Sustainable Perennial Crops Laboratory » Research » Publications at this Location » Publication #300855
Title: Gut microbiota mediate caffeine detoxification in the primary insect pest of coffee

Author
item CEJA-NAVARRO, JAVIER - Department Of Energy
item Vega, Fernando
item HAO, ZHAO - Department Of Energy
item LIM, HSIAOCHIEN - Department Of Energy
item KOSINA, PETR - International Maize & Wheat Improvement Center (CIMMYT)
item INFANTE, FRANCISCO - Ecosur
item BRODIE, EOIN - Department Of Energy

Submitted to: Nature Communications
Publication Type: Peer Reviewed Journal
Publication Acceptance Date: 5/26/2015
Publication Date: 7/14/2015
Citation: Ceja-Navarro, J.A., Vega, F.E., Hao, Z., Lim, H., Kosina, P., Infante, F., Brodie, E.L. 2015. Gut microbiota mediate caffeine detoxification in the primary insect pest of coffee. Nature Communications. 6:7618.

Interpretive Summary: The coffee berry borer, Hypothenemus hampei, is the most devastating pest of coffee throughout the world and causes millions of dollars in losses each year. Increased knowledge on the basic biology of the coffee berry borer can result in new insights on how to control this insect, thereby reducing losses and increasing yields. In this paper we report on the role of various bacteria in the insect gut in detoxifying caffeine. When these bacteria are eliminated through the use of antibiotics, the insect is unable to degrade caffeine. Our discovery of a microbial 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 and provides novel avenues for its biocontrol. This information will be of use to coffee scientists, entomologists, microbiologists, and the coffee industry.

Technical Abstract: 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 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 microbiome eliminates this activity. The gut microbiome 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 prominent. Pseudomonas caffeine demethyase 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 microbiome 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 and provides novel avenues for its biocontrol.