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Title: Gut microbiota mediate caffeine detoxification in the primary insect pest of coffee

Abstract

Here we report that 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. Furthermore, we show that caffeine is degraded in the gut of H. hampei, and that experimental inactivation of the gut microbiota eliminates this activity. We also 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. In conclusion, 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:
 [1];  [2];  [1];  [1];  [1];  [1]; ORCiD logo [3];  [4];  [1];  [1]
  1. Lawrence Berkeley National Lab. (LBNL), Berkeley, CA (United States)
  2. United States Department of Agriculture, Beltsville, MD (United States)
  3. International Maize and Wheat Improvement Center (CIMMYT), Texcoco (Mexico)
  4. El Colegio de la Frontera Sur (ECOSUR), Chiapas (Mexico)
Publication Date:
Research Org.:
Lawrence Berkeley National Lab. (LBNL), Berkeley, CA (United States)
Sponsoring Org.:
USDOE
OSTI Identifier:
1256035
Grant/Contract Number:  
AC02-05CH11231; AC02-05CH1121231
Resource Type:
Accepted Manuscript
Journal Name:
Nature Communications
Additional Journal Information:
Journal Volume: 6; Journal ID: ISSN 2041-1723
Publisher:
Nature Publishing Group
Country of Publication:
United States
Language:
English
Subject:
59 BASIC BIOLOGICAL SCIENCES

Citation Formats

Ceja-Navarro, Javier A., Vega, Fernando E., Karaoz, Ulas, Hao, Zhao, Jenkins, Stefan, Lim, Hsiao Chien, Kosina, Petr, Infante, Francisco, Northen, Trent R., and Brodie, Eoin L. Gut microbiota mediate caffeine detoxification in the primary insect pest of coffee. United States: N. p., 2015. Web. doi:10.1038/ncomms8618.
Ceja-Navarro, Javier A., Vega, Fernando E., Karaoz, Ulas, Hao, Zhao, Jenkins, Stefan, Lim, Hsiao Chien, Kosina, Petr, Infante, Francisco, Northen, Trent R., & Brodie, Eoin L. Gut microbiota mediate caffeine detoxification in the primary insect pest of coffee. United States. doi:10.1038/ncomms8618.
Ceja-Navarro, Javier A., Vega, Fernando E., Karaoz, Ulas, Hao, Zhao, Jenkins, Stefan, Lim, Hsiao Chien, Kosina, Petr, Infante, Francisco, Northen, Trent R., and Brodie, Eoin L. Tue . "Gut microbiota mediate caffeine detoxification in the primary insect pest of coffee". United States. doi:10.1038/ncomms8618. https://www.osti.gov/servlets/purl/1256035.
@article{osti_1256035,
title = {Gut microbiota mediate caffeine detoxification in the primary insect pest of coffee},
author = {Ceja-Navarro, Javier A. and Vega, Fernando E. and Karaoz, Ulas and Hao, Zhao and Jenkins, Stefan and Lim, Hsiao Chien and Kosina, Petr and Infante, Francisco and Northen, Trent R. and Brodie, Eoin L.},
abstractNote = {Here we report that 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. Furthermore, we show that caffeine is degraded in the gut of H. hampei, and that experimental inactivation of the gut microbiota eliminates this activity. We also 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. In conclusion, 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.},
doi = {10.1038/ncomms8618},
journal = {Nature Communications},
number = ,
volume = 6,
place = {United States},
year = {2015},
month = {7}
}

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Cited by: 38 works
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