Cultivation and Genome Sequencing of Bacteria Isolated From the Coffee Berry Borer (), With Emphasis on the Role of Caffeine Degradation

Overview

Journal Front Microbiol

Specialty Microbiology

Date 2021 Apr 23

PMID 33889142

Citations 7

Authors

Fernando E Vega

Sarah Emche

Jonathan Shao

Ann Simpkins

Ryan M Summers

Meredith B Mock

Dieter Ebert

Francisco Infante

Sayaka Aoki

Jude E Maul

Affiliations

Soon will be listed here.

Abstract

The coffee berry borer, the most economically important insect pest of coffee worldwide, is the only insect capable of feeding and reproducing solely on the coffee seed, a food source containing the purine alkaloid caffeine. Twenty-one bacterial species associated with coffee berry borers from Hawai'i, Mexico, or a laboratory colony in Maryland ( sp. S40, S54, S55, , , sp. S38, S43, S63, , sp. S45, S46, sp. S61, , , and sp. S30, S31, S32, S37, S44, S60, S75) were found to have at least one of five caffeine N-demethylation genes (, , , , ), with spp. S31, S32, S37, S60 and . having the full complement of these genes. Some of the bacteria carrying the ndm genes were detected in eggs, suggesting possible vertical transmission, while presence of caffeine-degrading bacteria in frass, e.g., () and () could result in horizontal transmission to all insect life stages. Thirty-five bacterial species associated with the insect ( sp. S40, S54, S55, , group, sp. S29, S70, S71, S72, S73, , sp. S38, S43, S59, S63, , , sp. S45, S46, sp. S28, sp. S61, S62, , , sp. S30, S31, S32, S37, S44, S60, S75, sp. S39, S41, S48, S49) might contribute to caffeine breakdown using the C-8 oxidation pathway, based on presence of genes required for this pathway. It is possible that caffeine-degrading bacteria associated with the coffee berry borer originated as epiphytes and endophytes in the coffee plant microbiota.

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References

Lee I, Kim Y, Park S, Chun J . OrthoANI: An improved algorithm and software for calculating average nucleotide identity. Int J Syst Evol Microbiol. 2015; 66(2):1100-1103. DOI: 10.1099/ijsem.0.000760. View

Yu C, Kale Y, Gopishetty S, Louie T, Subramanian M . A novel caffeine dehydrogenase in Pseudomonas sp. strain CBB1 oxidizes caffeine to trimethyluric acid. J Bacteriol. 2007; 190(2):772-6. PMC: 2223706. DOI: 10.1128/JB.01390-07. View

Ashihara H, Monteiro A, Gillies F, Crozier A . Biosynthesis of Caffeine in Leaves of Coffee. Plant Physiol. 1996; 111(3):747-753. PMC: 157891. DOI: 10.1104/pp.111.3.747. View

Summers R, Louie T, Yu C, Gakhar L, Louie K, Subramanian M . Novel, highly specific N-demethylases enable bacteria to live on caffeine and related purine alkaloids. J Bacteriol. 2012; 194(8):2041-9. PMC: 3318484. DOI: 10.1128/JB.06637-11. View

Vega F, Pava-Ripoll M, Posada F, Buyer J . Endophytic bacteria in Coffea arabica L. J Basic Microbiol. 2005; 45(5):371-80. DOI: 10.1002/jobm.200410551. View

Onchuru T, Martinez A, Ingham C, Kaltenpoth M . Transmission of mutualistic bacteria in social and gregarious insects. Curr Opin Insect Sci. 2018; 28:50-58. DOI: 10.1016/j.cois.2018.05.002. View

Summers R, Mohanty S, Gopishetty S, Subramanian M . Genetic characterization of caffeine degradation by bacteria and its potential applications. Microb Biotechnol. 2015; 8(3):369-78. PMC: 4408171. DOI: 10.1111/1751-7915.12262. View

Skaljac M, Zanic K, Goreta Ban S, Kontsedalov S, Ghanim M . Co-infection and localization of secondary symbionts in two whitefly species. BMC Microbiol. 2010; 10:142. PMC: 2877686. DOI: 10.1186/1471-2180-10-142. View

Chun J, Oren A, Ventosa A, Christensen H, Arahal D, da Costa M . Proposed minimal standards for the use of genome data for the taxonomy of prokaryotes. Int J Syst Evol Microbiol. 2018; 68(1):461-466. DOI: 10.1099/ijsem.0.002516. View

10.

Summers R, Shao J, Mock M, Yu C, Vega F . Draft Genome Sequence of sp. Strain CES, Containing the Entire Alkylxanthine Gene Cluster for Caffeine Breakdown. Microbiol Resour Announc. 2020; 9(28). PMC: 7348019. DOI: 10.1128/MRA.00484-20. View

11.

Ceja-Navarro J, Vega F, Karaoz U, Hao Z, Jenkins S, Lim H . Gut microbiota mediate caffeine detoxification in the primary insect pest of coffee. Nat Commun. 2015; 6:7618. PMC: 4510693. DOI: 10.1038/ncomms8618. View

12.

Gokulakrishnan S, Chandraraj K, Gummadi S . A preliminary study of caffeine degradation by Pseudomonas sp. GSC 1182. Int J Food Microbiol. 2006; 113(3):346-50. DOI: 10.1016/j.ijfoodmicro.2006.07.005. View

13.

Jaenike J . Population genetics of beneficial heritable symbionts. Trends Ecol Evol. 2011; 27(4):226-32. DOI: 10.1016/j.tree.2011.10.005. View

14.

Nathanson J . Caffeine and related methylxanthines: possible naturally occurring pesticides. Science. 1984; 226(4671):184-7. DOI: 10.1126/science.6207592. View

15.

Wright G, Baker D, Palmer M, Stabler D, Mustard J, Power E . Caffeine in floral nectar enhances a pollinator's memory of reward. Science. 2013; 339(6124):1202-4. PMC: 4521368. DOI: 10.1126/science.1228806. View

16.

Summers R, Seffernick J, Quandt E, Yu C, Barrick J, Subramanian M . Caffeine junkie: an unprecedented glutathione S-transferase-dependent oxygenase required for caffeine degradation by Pseudomonas putida CBB5. J Bacteriol. 2013; 195(17):3933-9. PMC: 3754594. DOI: 10.1128/JB.00585-13. View

17.

Ashihara H, Mizuno K, Yokota T, Crozier A . Xanthine Alkaloids: Occurrence, Biosynthesis, and Function in Plants. Prog Chem Org Nat Prod. 2017; 105:1-88. DOI: 10.1007/978-3-319-49712-9_1. View

18.

Kim Y, Uefuji H, Ogita S, Sano H . Transgenic tobacco plants producing caffeine: a potential new strategy for insect pest control. Transgenic Res. 2006; 15(6):667-72. DOI: 10.1007/s11248-006-9006-6. View

19.

Kim J, Kim B, Brooks S, Kang S, Summers R, Song H . Structural and Mechanistic Insights into Caffeine Degradation by the Bacterial N-Demethylase Complex. J Mol Biol. 2019; 431(19):3647-3661. DOI: 10.1016/j.jmb.2019.08.004. View

20.

Hosokawa T, Hironaka M, Inadomi K, Mukai H, Nikoh N, Fukatsu T . Diverse strategies for vertical symbiont transmission among subsocial stinkbugs. PLoS One. 2013; 8(5):e65081. PMC: 3669201. DOI: 10.1371/journal.pone.0065081. View