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

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.

咖啡果小蠹（Hypothenemus hampei）是全球范围内危害最为严重的咖啡害虫。该虫侵染绝大多数咖啡生产国的咖啡作物，在咖啡产业占国内生产总值重要组成部分的发展中国家，其威胁尤为突出。在已报道的850余种取食咖啡植株的昆虫中，咖啡果小蠹是目前已知唯一以富含咖啡因的咖啡豆作为食物与栖息场所的昆虫。受其侵染可直接导致咖啡作物减产最高达80%。
咖啡因是一类对昆虫具有毒性的生物碱，被认为是植物抵御植食性生物的防御机制之一。本研究首次证实，咖啡果小蠹的肠道能够降解咖啡因，且肠道菌群的灭活会消除这一降解活性。对来自7个主要咖啡生产国的野生咖啡果小蠹样本以及实验室饲养种群的肠道菌群分析显示，其核心微生物组具有高度保守性，同时存在与地理环境或饮食相关的菌群差异。
研究表明，全球广泛分布的肠道菌群成员可仅以咖啡因作为唯一碳源与氮源完成生长繁殖，其中假单胞菌属（Pseudomonas）物种最为优势。在野生与实验室饲养的咖啡果小蠹肠道内，假单胞菌的咖啡因脱甲基酶基因均实现体内表达；将分离得到的假单胞菌株重新接种经抗生素处理的昆虫后，可恢复其咖啡因降解能力。
本研究揭示了菌群参与咖啡因转化以及咖啡果小蠹依托咖啡豆生存的机制，这一发现对于理解这一重大农业害虫的代谢与生态学特征具有重要意义。