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

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.

doi:10.1038/ncomms8618

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

Journal Article · Tue Jul 14 00:00:00 EDT 2015 · Nature Communications

DOI:https://doi.org/10.1038/ncomms8618· OSTI ID:1256035

Ceja-Navarro, Javier A. ^[1]; Vega, Fernando E. ^[2]; Karaoz, Ulas ^[1]; Hao, Zhao ^[1]; Jenkins, Stefan ^[1]; Lim, Hsiao Chien ^[1];

^[3]; Infante, Francisco ^[4]; Northen, Trent R. ^[1]; Brodie, Eoin L. ^[1]

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)

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.

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Research Organization:: Lawrence Berkeley National Laboratory (LBNL), Berkeley, CA (United States)

Sponsoring Organization:: USDOE

Grant/Contract Number:: AC02-05CH11231; AC02-05CH1121231

OSTI ID:: 1256035

Journal Information:: Nature Communications, Vol. 6; ISSN 2041-1723

Publisher:: Nature Publishing GroupCopyright Statement

Country of Publication:: United States

Language:: English

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Cited by: 267 works

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Comparison of gut bacterial communities and their associations with host diets in four fruit borers Liu, Yanjun; Shen, Zhongjian; Yu, Jianmei Pest Management Science, Vol. 76, Issue 4 https://doi.org/10.1002/ps.5646	journal	November 2019
Caterpillars lack a resident gut microbiome Hammer, Tobin J.; Janzen, Daniel H.; Hallwachs, Winnifred Proceedings of the National Academy of Sciences https://doi.org/10.1101/132522	journal	April 2017
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 Zhou, Ying; Liu, Xiaoyu; Yang, Ziyin Biomolecules, Vol. 9, Issue 12 https://doi.org/10.3390/biom9120808	journal	November 2019
Detecting host-parasitoid interactions in an invasive Lepidopteran using nested tagging DNA-metabarcoding Kitson, James J. N.; Hahn, Christoph; Sands, Richard J. Molecular Ecology https://doi.org/10.1101/035071	journal	January 2018
For antagonists and mutualists: the paradox of insect toxic secondary metabolites in nectar and pollen Stevenson, Philip C. Phytochemistry Reviews, Vol. 19, Issue 3 https://doi.org/10.1007/s11101-019-09642-y	journal	August 2019
Similar gut bacterial microbiota in two fruit-feeding moth pests collected from different host species and locations Gong, Qiang; Cao, Li-Jun; Chen, Jin-Cui Insects https://doi.org/10.1101/2020.04.06.028886	journal	April 2020
Co‐occurrence of pederin‐producing and Wolbachia endobacteria in Paederus fuscipes Curtis, 1840 (Coleoptera: Staphilinidae) and its evolutionary consequences Maleki‐Ravasan, Naseh; Akhavan, Niloofar; Raz, Abbasali MicrobiologyOpen, Vol. 8, Issue 7 https://doi.org/10.1002/mbo3.777	journal	December 2018
New Insights into the Microbiota of Moth Pests Mereghetti, Valeria; Chouaia, Bessem; Montagna, Matteo International Journal of Molecular Sciences, Vol. 18, Issue 11 https://doi.org/10.3390/ijms18112450	journal	November 2017
Disentangling of the ecotoxicological signal using “omics” analyses, a lesson from the survey of the impact of cyanobacterial proliferations on fishes Marie, Benjamin Science of The Total Environment, Vol. 736 https://doi.org/10.1016/j.scitotenv.2020.139701	journal	September 2020
Dynamic Changes of Gut Microbial Communities of Bumble Bee Queens through Important Life Stages Wang, Liuhao; Wu, Jie; Li, Kai mSystems, Vol. 4, Issue 6 https://doi.org/10.1128/msystems.00631-19	journal	December 2019
The Native Hawaiian Insect Microbiome Initiative: A Critical Perspective for Hawaiian Insect Evolution Poff, Kirsten; Stever, Heather; Reil, Jonathan Insects, Vol. 8, Issue 4 https://doi.org/10.3390/insects8040130	journal	December 2017
Intestinal probiotics restore the ecological fitness decline of Bactrocera dorsalis by irradiation Cai, Zhaohui; Yao, Zhichao; Li, Yushan Evolutionary Applications, Vol. 11, Issue 10 https://doi.org/10.1111/eva.12698	journal	October 2018
Microbial Communities of Lycaenid Butterflies Do Not Correlate with Larval Diet Whitaker, Melissa R. L.; Salzman, Shayla; Sanders, Jon Frontiers in Microbiology, Vol. 7 https://doi.org/10.3389/fmicb.2016.01920	journal	November 2016
Context-dependent medicinal effects of anabasine and infection-dependent toxicity in bumble bees Palmer-Young, Evan C.; Hogeboom, Alison; Kaye, Alexander J. PLOS ONE, Vol. 12, Issue 8 https://doi.org/10.1371/journal.pone.0183729	journal	August 2017
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 Minard, Guillaume; Tikhonov, Gleb; Ovaskainen, Otso Environmental Microbiology, Vol. 21, Issue 11 https://doi.org/10.1111/1462-2920.14786	journal	September 2019
Impact of Sample Preservation and Manipulation on Insect Gut Microbiome Profiling. A Test Case With Fruit Flies (Diptera, Tephritidae) De Cock, Maarten; Virgilio, Massimiliano; Vandamme, Peter Frontiers in Microbiology, Vol. 10 https://doi.org/10.3389/fmicb.2019.02833	journal	December 2019
Similar Shift Patterns in Gut Bacterial and Fungal Communities Across the Life Stages of Bactrocera minax Larvae From Two Field Populations Yao, Zhichao; Ma, Qiongke; Cai, Zhaohui Frontiers in Microbiology, Vol. 10 https://doi.org/10.3389/fmicb.2019.02262	journal	October 2019
Spiroplasma dominates the microbiome of khapra beetle: comparison with a congener, effects of life stage and temperature Wilches, D. M.; Laird, R. A.; Fields, P. G. Symbiosis, Vol. 76, Issue 3 https://doi.org/10.1007/s13199-018-0560-5	journal	June 2018

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