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

Ceja-Navarro, Javier A.; Vega, Fernando E.; Karaöz, Ulaş; Hao, Zhao; Jenkins, Stefan; Lim, Hsiao Chien; Kosina, Petr; Infante, Francisco; Northen, Trent; Brodie, Eoin L.

doi:10.1038/ncomms8618

Cited by 383 publications

(363 citation statements)

References 49 publications

(64 reference statements)

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“…The unnatural conditions associated with elimination of the bacterial flora will have a major impact on a wealth of functions, including immune defense barriers, pathogen vectoring capacity, tissue regeneration, and, more generally, physiological homeostasis, with a significant influence on nutrition and detoxification pathways (33,(41)(42)(43)(44)(45). The experimental approach adopted here did not alter the midgut environment in any detectable way, but simply acted on the defense response by selectively decreasing the transcript level of a gene expressed in the hemocytes, which controls cellular immunity.…”

Section: Discussionmentioning

confidence: 99%

Midgut microbiota and host immunocompetence underlieBacillus thuringiensiskilling mechanism

Caccia¹,

Lelio

Storia

et al. 2016

Proc. Natl. Acad. Sci. U.S.A.

151

128

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Bacillus thuringiensis is a widely used bacterial entomopathogen producing insecticidal toxins, some of which are expressed in insect-resistant transgenic crops. Surprisingly, the killing mechanism of B. thuringiensis remains controversial. In particular, the importance of the septicemia induced by the host midgut microbiota is still debated as a result of the lack of experimental evidence obtained without drastic manipulation of the midgut and its content. Here this key issue is addressed by RNAi-mediated silencing of an immune gene in a lepidopteran host Spodoptera littoralis, leaving the midgut microbiota unaltered. The resulting cellular immunosuppression was characterized by a reduced nodulation response, which was associated with a significant enhancement of host larvae mortality triggered by B. thuringiensis and a Cry toxin. This was determined by an uncontrolled proliferation of midgut bacteria, after entering the body cavity through toxin-induced epithelial lesions. Consequently, the hemolymphatic microbiota dramatically changed upon treatment with Cry1Ca toxin, showing a remarkable predominance of Serratia and Clostridium species, which switched from asymptomatic gut symbionts to hemocoelic pathogens. These experimental results demonstrate the important contribution of host enteric flora in B. thuringiensis-killing activity and provide a sound foundation for developing new insect control strategies aimed at enhancing the impact of biocontrol agents by reducing the immunocompetence of the host.

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Section: Discussionmentioning

confidence: 99%

Midgut microbiota and host immunocompetence underlieBacillus thuringiensiskilling mechanism

Caccia¹,

Lelio

Storia

et al. 2016

Proc. Natl. Acad. Sci. U.S.A.

151

128

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“…Water with or without antibiotics was sprayed onto leaves, which were then briefly dried before feeding. The compounds used here (rifampicin, tetracycline, and streptomycin in a 1:2:4 ratio) have been shown to suppress bacterial symbionts in other insect herbivores (53,96). More detail is provided in SI Appendix, SI Methods.…”

Section: Methodsmentioning

confidence: 99%

Caterpillars lack a resident gut microbiome

Hammer

Janzen

Hallwachs

et al. 2017

Proc. Natl. Acad. Sci. U.S.A.

380

347

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Many animals are inhabited by microbial symbionts that influence their hosts’ development, physiology, ecological interactions, and evolutionary diversification. However, firm evidence for the existence and functional importance of resident microbiomes in larval Lepidoptera (caterpillars) is lacking, despite the fact that these insects are enormously diverse, major agricultural pests, and dominant herbivores in many ecosystems. Using 16S rRNA gene sequencing and quantitative PCR, we characterized the gut microbiomes of wild leaf-feeding caterpillars in the United States and Costa Rica, representing 124 species from 15 families. Compared with other insects and vertebrates assayed using the same methods, the microbes that we detected in caterpillar guts were unusually low-density and variable among individuals. Furthermore, the abundance and composition of leaf-associated microbes were reflected in the feces of caterpillars consuming the same plants. Thus, microbes ingested with food are present (although possibly dead or dormant) in the caterpillar gut, but host-specific, resident symbionts are largely absent. To test whether transient microbes might still contribute to feeding and development, we conducted an experiment on field-collected caterpillars of the model species Manduca sexta. Antibiotic suppression of gut bacterial activity did not significantly affect caterpillar weight gain, development, or survival. The high pH, simple gut structure, and fast transit times that typify caterpillar digestive physiology may prevent microbial colonization. Moreover, host-encoded digestive and detoxification mechanisms likely render microbes unnecessary for caterpillar herbivory. Caterpillars illustrate the potential ecological and evolutionary benefits of independence from symbionts, a lifestyle that may be widespread among animals.

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“…The genus Coffea consists of approximately 124 species, which occur mostly in tropical and sub-tropical regions of the world (Davis et al 2006(Davis et al , 2011Ceja-Navarro et al 2015). The two widely cultivated species are Coffea arabica and Coffea canephora.…”

Section: Introductionmentioning

confidence: 99%

Characterization and utilization of microsatellites in the Coffea canephora genome to assess genetic association between wild species in Kenya and cultivated coffee

Ogutu

Fang

Lin

et al. 2016

Tree Genetics & Genomes

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Coffee is an important beverage crop in the world and has a significant contribution to Kenya's economy. Here, we analyzed the genome-wide distribution of microsatellites in the Coffea canephora genome. A total of 159,041 SSRs were identified, with an overall density of 308 SSRs per Mb. Tetra-nucleotide repeats are the most abundant, accounting for 32 % of the total SSRs. AT-rich motifs are dominant across all SSR repeat units, while GC-rich motifs were generally rare. A set of 100 SSRs was selected to amplify 96 coffee accessions, including 10 wild accessions collected from Mt. Marsabit (Kenya). Of these SSRs, 33 % generated clear polymorphic bands among all tested accessions, with an average of 3.9 alleles per SSR locus. Wild coffee species from Mt. Marsabit showed a close genetic similarity with cultivated accessions in Kenya, suggesting that the wild species in Mt. Marsabit played an important role in the domestication of cultivated coffee in Kenya. Significantly low pairwise genetic divergence was observed between cultivated and wild accessions in Kenya, suggesting a relatively narrow level of genetic basis among coffee germplasm in Kenya. In addition, cultivated and wild coffee accessions in Kenya show a great divergence from those in other countries. Our results not only provide molecular tools for genetic studies in coffee but are also helpful for conservation and coffee breeding programs in Kenya.

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

Cited by 383 publications

References 49 publications

Midgut microbiota and host immunocompetence underlieBacillus thuringiensiskilling mechanism

Midgut microbiota and host immunocompetence underlieBacillus thuringiensiskilling mechanism

Caterpillars lack a resident gut microbiome

Characterization and utilization of microsatellites in the Coffea canephora genome to assess genetic association between wild species in Kenya and cultivated coffee

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