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

Ceja-Navarro JA, Vega FE, Karaoz U, Hao Z, Jenkins S, Lim HC, Kosina P, Infante F, Northen TR, Brodie EL - Nat Commun (2015)

Bottom Line: We 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.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.

View Article: PubMed Central - PubMed

Affiliation: Ecology Department, Earth Sciences Division, Lawrence Berkeley National Laboratory, Berkeley, California 94720, USA.

ABSTRACT
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. Here we show that caffeine is degraded in the gut of H. hampei, and that experimental inactivation of the gut microbiota eliminates this activity. We 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. 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.

No MeSH data available.


Related in: MedlinePlus

Oxygen profiles in the anterior midgut of H. hampei.The figure shows the oxygen profiles of three beetle guts. Note the transition from a microaerophilic region to an anaerobic core in the lumen of the anterior midgut (see Supplementary Fig. 1).
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f4: Oxygen profiles in the anterior midgut of H. hampei.The figure shows the oxygen profiles of three beetle guts. Note the transition from a microaerophilic region to an anaerobic core in the lumen of the anterior midgut (see Supplementary Fig. 1).

Mentions: Oxygen gradients were measured in the gut of H. hampei with the use of microelectrodes. All measurements were performed in the anterior midgut of the beetle (see Supplementary Fig. 1). During these procedures, the tip of the electrode was driven to the surface of the gut wall and maintained in position until measured concentrations of O2 stabilized. In all cases, once the tip penetrated the gut wall, oxygen concentrations declined with steep gradients going from microaerophilic conditions to a reduced anaerobic core (Fig. 4).


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

Ceja-Navarro JA, Vega FE, Karaoz U, Hao Z, Jenkins S, Lim HC, Kosina P, Infante F, Northen TR, Brodie EL - Nat Commun (2015)

Oxygen profiles in the anterior midgut of H. hampei.The figure shows the oxygen profiles of three beetle guts. Note the transition from a microaerophilic region to an anaerobic core in the lumen of the anterior midgut (see Supplementary Fig. 1).
© Copyright Policy - open-access
Related In: Results  -  Collection

License
Show All Figures
getmorefigures.php?uid=PMC4510693&req=5

f4: Oxygen profiles in the anterior midgut of H. hampei.The figure shows the oxygen profiles of three beetle guts. Note the transition from a microaerophilic region to an anaerobic core in the lumen of the anterior midgut (see Supplementary Fig. 1).
Mentions: Oxygen gradients were measured in the gut of H. hampei with the use of microelectrodes. All measurements were performed in the anterior midgut of the beetle (see Supplementary Fig. 1). During these procedures, the tip of the electrode was driven to the surface of the gut wall and maintained in position until measured concentrations of O2 stabilized. In all cases, once the tip penetrated the gut wall, oxygen concentrations declined with steep gradients going from microaerophilic conditions to a reduced anaerobic core (Fig. 4).

Bottom Line: We 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.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.

View Article: PubMed Central - PubMed

Affiliation: Ecology Department, Earth Sciences Division, Lawrence Berkeley National Laboratory, Berkeley, California 94720, USA.

ABSTRACT
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. Here we show that caffeine is degraded in the gut of H. hampei, and that experimental inactivation of the gut microbiota eliminates this activity. We 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. 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.

No MeSH data available.


Related in: MedlinePlus