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:
-
[3];
- Lawrence Berkeley National Lab. (LBNL), Berkeley, CA (United States)
- United States Department of Agriculture, Beltsville, MD (United States)
- International Maize and Wheat Improvement Center (CIMMYT), Texcoco (Mexico)
- El Colegio de la Frontera Sur (ECOSUR), Chiapas (Mexico)
- Publication Date:
- Research Org.:
- Lawrence Berkeley National Laboratory (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. https://doi.org/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. https://doi.org/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 = {Tue Jul 14 00:00:00 EDT 2015},
month = {Tue Jul 14 00:00:00 EDT 2015}
}
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Entomology in the 21st Century: Tackling Insect Invasions, Promoting Advancements in Technology, and Using Effective Science Communication—2018 Student Debates
journal, July 2019
- Parker, Casey; Bernaola, Lina; Lee, Benjamin W.
- Journal of Insect Science, Vol. 19, Issue 4
High diversity and variability in the bacterial microbiota of the coffee berry borer ( Coleoptera : Curculionidae), with emphasis on Wolbachia
journal, May 2018
- Mariño, Y. A.; Ospina, O. E.; Verle Rodrigues, J. C.
- Journal of Applied Microbiology, Vol. 125, Issue 2
Midgut microbiota diversity of potato tuber moth associated with potato tissue consumed
journal, March 2020
- Zheng, Yaqiang; Xiao, Guanli; Zhou, Wenwu
- BMC Microbiology, Vol. 20, Issue 1
The Links Between Insect Symbionts and Insecticide Resistance: Causal Relationships and Physiological Tradeoffs
journal, March 2018
- Pietri, Jose E.; Liang, Dangsheng
- Annals of the Entomological Society of America, Vol. 111, Issue 3
Characterized non-transient microbiota from stinkbug (Nezara viridula) midgut deactivates soybean chemical defenses
journal, July 2018
- Medina, Virginia; Sardoy, Pedro M.; Soria, Marcelo
- PLOS ONE, Vol. 13, Issue 7
Community structure of the gut microbiota in sympatric species of wild Drosophila
journal, March 2017
- Martinson, Vincent G.; Douglas, Angela E.; Jaenike, John
- Ecology Letters, Vol. 20, Issue 5
The Woodrat Gut Microbiota as an Experimental System for Understanding Microbial Metabolism of Dietary Toxins
journal, July 2016
- Kohl, Kevin D.; Dearing, M. Denise
- Frontiers in Microbiology, Vol. 7
Bacterial community structure and diversity in the gut of the muga silkworm, Antheraea assamensis (Lepidoptera: Saturniidae), from India: Diversity of gut bacteria in Antheraea assamensis
journal, June 2018
- Gandotra, S.; Kumar, A.; Naga, K.
- Insect Molecular Biology, Vol. 27, Issue 5
Diet breadth and exploitation of exotic plants shift the core microbiome of Cephaloleia , a group of tropical herbivorous beetles
journal, January 2018
- Blankenchip, Chelsea L.; Michels, Dana E.; Braker, H. Elizabeth
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Resource profitability, but not caffeine, affects individual and collective foraging in the stingless bee Plebeia droryana
journal, January 2019
- Peng, Tianfei; Segers, Francisca H. I. D.; Nascimento, Fabio
- Journal of Experimental Biology
Midgut microbiota diversity of potato tuber moth associated with potato tissue consumed
journal, March 2020
- Zheng, Yaqiang; Xiao, Guanli; Zhou, Wenwu
- BMC Microbiology, Vol. 20, Issue 1
Accelerated Development and Toxin Tolerance of the Navel Orangeworm Amyelois transitella (Lepidoptera: Pyralidae) in the Presence of Aspergillus flavus
journal, October 2018
- Bush, Daniel S.; Siegel, Joel P.; Berenbaum, May R.
- Journal of Chemical Ecology, Vol. 44, Issue 12
Host plant and population source drive diversity of microbial gut communities in two polyphagous insects
journal, February 2019
- Jones, Asher G.; Mason, Charles J.; Felton, Gary W.
- Scientific Reports, Vol. 9, Issue 1
Artificial selection of insects to bioconvert pre-consumer organic wastes. A review
journal, May 2019
- Fowles, Trevor M.; Nansen, Christian
- Agronomy for Sustainable Development, Vol. 39, Issue 3
Midgut microbiota and host immunocompetence underlie Bacillus thuringiensis killing mechanism
journal, August 2016
- Caccia, Silvia; Di Lelio, Ilaria; La Storia, Antonietta
- Proceedings of the National Academy of Sciences, Vol. 113, Issue 34
Mosquito microbiota cluster by host sampling location
journal, August 2018
- Muturi, Ephantus J.; Lagos-Kutz, Doris; Dunlap, Christopher
- Parasites & Vectors, Vol. 11, Issue 1
Anatomical study of the coffee berry borer (Hypothenemus hampei) using micro-computed tomography
journal, November 2019
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- Scientific Reports, Vol. 9, Issue 1
Microbiota inoculum composition affects holobiont assembly and host growth in Daphnia
journal, March 2018
- Callens, Martijn; Watanabe, Hajime; Kato, Yasuhiko
- Microbiome, Vol. 6, Issue 1
Gut Bacterial Communities of Dendroctonus valens and D. mexicanus (Curculionidae: Scolytinae): A Metagenomic Analysis across Different Geographical Locations in Mexico
journal, August 2018
- Hernández-García, Juan; Gonzalez-Escobedo, Roman; Briones-Roblero, Carlos
- International Journal of Molecular Sciences, Vol. 19, Issue 9
Comparison of gut bacterial communities and their associations with host diets in four fruit borers
journal, November 2019
- Liu, Yanjun; Shen, Zhongjian; Yu, Jianmei
- Pest Management Science, Vol. 76, Issue 4
Caterpillars lack a resident gut microbiome
journal, April 2017
- Hammer, Tobin J.; Janzen, Daniel H.; Hallwachs, Winnifred
- Proceedings of the National Academy of Sciences
Characterization of Terpene Synthase from Tea Green Leafhopper Being Involved in Formation of Geraniol in Tea (Camellia sinensis) Leaves and Potential Effect of Geraniol on Insect-Derived Endobacteria
journal, November 2019
- Zhou, Ying; Liu, Xiaoyu; Yang, Ziyin
- Biomolecules, Vol. 9, Issue 12
Detecting host-parasitoid interactions in an invasive Lepidopteran using nested tagging DNA-metabarcoding
journal, January 2018
- Kitson, James J. N.; Hahn, Christoph; Sands, Richard J.
- Molecular Ecology
For antagonists and mutualists: the paradox of insect toxic secondary metabolites in nectar and pollen
journal, August 2019
- Stevenson, Philip C.
- Phytochemistry Reviews, Vol. 19, Issue 3
Similar gut bacterial microbiota in two fruit-feeding moth pests collected from different host species and locations
journal, April 2020
- Gong, Qiang; Cao, Li-Jun; Chen, Jin-Cui
- Insects
Co‐occurrence of pederin‐producing and Wolbachia endobacteria in Paederus fuscipes Curtis, 1840 (Coleoptera: Staphilinidae) and its evolutionary consequences
journal, December 2018
- Maleki‐Ravasan, Naseh; Akhavan, Niloofar; Raz, Abbasali
- MicrobiologyOpen, Vol. 8, Issue 7
New Insights into the Microbiota of Moth Pests
journal, November 2017
- Mereghetti, Valeria; Chouaia, Bessem; Montagna, Matteo
- International Journal of Molecular Sciences, Vol. 18, Issue 11
Disrupting butterfly caterpillar microbiomes does not impact their survival and development
journal, December 2019
- Phalnikar, Kruttika; Kunte, Krushnamegh; Agashe, Deepa
- Proceedings of the Royal Society B: Biological Sciences, Vol. 286, Issue 1917
Disentangling of the ecotoxicological signal using “omics” analyses, a lesson from the survey of the impact of cyanobacterial proliferations on fishes
journal, September 2020
- Marie, Benjamin
- Science of The Total Environment, Vol. 736
Caterpillars lack a resident gut microbiome
journal, August 2017
- Hammer, Tobin J.; Janzen, Daniel H.; Hallwachs, Winnie
- Proceedings of the National Academy of Sciences, Vol. 114, Issue 36
Dynamic Changes of Gut Microbial Communities of Bumble Bee Queens through Important Life Stages
journal, December 2019
- Wang, Liuhao; Wu, Jie; Li, Kai
- mSystems, Vol. 4, Issue 6
Whole metagenome sequencing reveals links between mosquito microbiota and insecticide resistance in malaria vectors
journal, February 2018
- Dada, Nsa; Sheth, Mili; Liebman, Kelly
- Scientific Reports, Vol. 8, Issue 1
Microbiota inoculum composition affects holobiont assembly and host growth in Daphnia
journal, March 2018
- Callens, Martijn; Watanabe, Hajime; Kato, Yasuhiko
- Microbiome, Vol. 6, Issue 1
Gut Bacterial Communities of Dendroctonus valens and D. mexicanus (Curculionidae: Scolytinae): A Metagenomic Analysis across Different Geographical Locations in Mexico
journal, August 2018
- Hernández-García, Juan; Gonzalez-Escobedo, Roman; Briones-Roblero, Carlos
- International Journal of Molecular Sciences, Vol. 19, Issue 9
Mosquito microbiota cluster by host sampling location
journal, August 2018
- Muturi, Ephantus J.; Lagos-Kutz, Doris; Dunlap, Christopher
- Parasites & Vectors, Vol. 11, Issue 1
The Native Hawaiian Insect Microbiome Initiative: A Critical Perspective for Hawaiian Insect Evolution
journal, December 2017
- Poff, Kirsten; Stever, Heather; Reil, Jonathan
- Insects, Vol. 8, Issue 4
The Native Hawaiian Insect Microbiome Initiative: A Critical Perspective for Hawaiian Insect Evolution
journal, December 2017
- Poff, Kirsten; Stever, Heather; Reil, Jonathan
- Insects, Vol. 8, Issue 4
Intestinal probiotics restore the ecological fitness decline of Bactrocera dorsalis by irradiation
journal, October 2018
- Cai, Zhaohui; Yao, Zhichao; Li, Yushan
- Evolutionary Applications, Vol. 11, Issue 10
Microbial Communities of Lycaenid Butterflies Do Not Correlate with Larval Diet
journal, November 2016
- Whitaker, Melissa R. L.; Salzman, Shayla; Sanders, Jon
- Frontiers in Microbiology, Vol. 7
Co‐occurrence of pederin‐producing and Wolbachia endobacteria in Paederus fuscipes Curtis, 1840 (Coleoptera: Staphilinidae) and its evolutionary consequences
journal, December 2018
- Maleki‐Ravasan, Naseh; Akhavan, Niloofar; Raz, Abbasali
- MicrobiologyOpen, Vol. 8, Issue 7
Context-dependent medicinal effects of anabasine and infection-dependent toxicity in bumble bees
journal, August 2017
- Palmer-Young, Evan C.; Hogeboom, Alison; Kaye, Alexander J.
- PLOS ONE, Vol. 12, Issue 8
The microbiome of the Melitaea cinxia butterfly shows marked variation but is only little explained by the traits of the butterfly or its host plant
journal, September 2019
- Minard, Guillaume; Tikhonov, Gleb; Ovaskainen, Otso
- Environmental Microbiology, Vol. 21, Issue 11
Impact of Sample Preservation and Manipulation on Insect Gut Microbiome Profiling. A Test Case With Fruit Flies (Diptera, Tephritidae)
journal, December 2019
- De Cock, Maarten; Virgilio, Massimiliano; Vandamme, Peter
- Frontiers in Microbiology, Vol. 10
Similar Shift Patterns in Gut Bacterial and Fungal Communities Across the Life Stages of Bactrocera minax Larvae From Two Field Populations
journal, October 2019
- Yao, Zhichao; Ma, Qiongke; Cai, Zhaohui
- Frontiers in Microbiology, Vol. 10
Entomology in the 21st Century: Tackling Insect Invasions, Promoting Advancements in Technology, and Using Effective Science Communication—2018 Student Debates
journal, July 2019
- Parker, Casey; Bernaola, Lina; Lee, Benjamin W.
- Journal of Insect Science, Vol. 19, Issue 4
Spiroplasma dominates the microbiome of khapra beetle: comparison with a congener, effects of life stage and temperature
journal, June 2018
- Wilches, D. M.; Laird, R. A.; Fields, P. G.
- Symbiosis, Vol. 76, Issue 3