title: Gut microbiota mediate caffeine detoxification in the primary insect pest of coffee.
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.
authors.affiliation: Ecology Department, Earth Sciences Division, Lawrence Berkeley National Laboratory, Berkeley, California 94720, USA.
authors.forename: Javier A
authors.initials: JA
authors.lastname: Ceja-Navarro
authors.affiliation: Sustainable Perennial Crops Laboratory, United States Department of Agriculture, Agricultural Research Service, Building 001, BARC-W, Beltsville, Maryland 20705, USA.
authors.forename: Fernando E
authors.initials: FE
authors.lastname: Vega
authors.affiliation: Ecology Department, Earth Sciences Division, Lawrence Berkeley National Laboratory, Berkeley, California 94720, USA.
authors.forename: Ulas
authors.initials: U
authors.lastname: Karaoz
authors.affiliation: Ecology Department, Earth Sciences Division, Lawrence Berkeley National Laboratory, Berkeley, California 94720, USA.
authors.forename: Zhao
authors.initials: Z
authors.lastname: Hao
authors.affiliation: Genome Dynamics Department, Life Sciences Division, Lawrence Berkeley National Laboratory, Berkeley, California 94720, USA.
authors.forename: Stefan
authors.initials: S
authors.lastname: Jenkins
authors.affiliation: Ecology Department, Earth Sciences Division, Lawrence Berkeley National Laboratory, Berkeley, California 94720, USA.
authors.forename: Hsiao Chien
authors.initials: HC
authors.lastname: Lim
authors.affiliation: International Maize and Wheat Improvement Center (CIMMYT), Carretera Mexico-Veracruz Km. 45, El Batán, Texcoco 56130, Mexico.
authors.forename: Petr
authors.identifier: http://orcid.org/0000-0002-8805-0306
authors.initials: P
authors.lastname: Kosina
authors.affiliation: El Colegio de la Frontera Sur (ECOSUR), Carretera Antiguo Aeropuerto Km. 2.5, Tapachula, Chiapas 30700, Mexico.
authors.forename: Francisco
authors.initials: F
authors.lastname: Infante
authors.affiliation: Genome Dynamics Department, Life Sciences Division, Lawrence Berkeley National Laboratory, Berkeley, California 94720, USA.
authors.forename: Trent R
authors.initials: TR
authors.lastname: Northen
authors.affiliation: Ecology Department, Earth Sciences Division, Lawrence Berkeley National Laboratory, Berkeley, California 94720, USA.|Department of Environmental Science, Policy and Management, University of California, Berkeley, California 94720, USA.
authors.forename: Eoin L
authors.initials: EL
authors.lastname: Brodie
mesh_terms: D000818:Animals; D001483:Base Sequence; D002110:Caffeine / Q000378:metabolism*; D040503:Coffea; D019388:Cytochrome P-450 CYP1A2 / Q000235:genetics* / Q000378:metabolism; D000069196:Gastrointestinal Microbiome / Q000235:genetics*; D008658:Inactivation, Metabolic / Q000235:genetics*; D008969:Molecular Sequence Data; D011549:Pseudomonas / Q000235:genetics*; D048889:Weevils / Q000378:metabolism*
chemical_list: D002110:Caffeine; D019388:Cytochrome P-450 CYP1A2