Microbiota-Mediated Modulation of Organophosphate Insecticide Toxicity by Species-Dependent Interactions with Lactobacilli in a Drosophila melanogaster Insect Model
Authors: Daisley Brendan A. , Trinder Mark , McDowell Tim W. , Collins Stephanie L. , Sumarah Mark W. , Reid Gregor 
Published: February 2018

ABSTRACT

Despite the benefits to the global food supply and agricultural economies, pesticides are believed to pose a threat to the health of both humans and wildlife. Chlorpyrifos (CP), a commonly used organophosphate insecticide, has poor target specificity and causes acute neurotoxicity in a wide range of species via the suppression of acetylcholinesterase. This effect is exacerbated 10- to 100-fold by chlorpyrifos oxon (CPO), a principal metabolite of CP. Since many animal-associated symbiont microorganisms are known to hydrolyze CP into CPO, we used a
Drosophila melanogaster
insect model to investigate the hypothesis that indigenous and probiotic bacteria could affect CP metabolism and toxicity. Antibiotic-treated and germfree
D. melanogaster
insects lived significantly longer than their conventionally reared counterparts when exposed to 10 μM CP.
Drosophila melanogaster
gut-derived
Lactobacillus plantarum
, but not
Acetobacter
indonesiensis
, was shown to metabolize CP. Liquid chromatography tandem-mass spectrometry confirmed that the
L. plantarum
isolate preferentially metabolized CP into CPO when grown in CP-spiked culture medium. Further experiments showed that monoassociating germfree
D. melanogaster
with the
L. plantarum
isolate could reestablish a conventional-like sensitivity to CP. Interestingly, supplementation with the human probiotic
Lactobacillus rhamnosus
GG (a strain that binds but does not metabolize CP) significantly increased the survival of the CP-exposed germfree
D. melanogaster
. This suggests strain-specific differences in CP metabolism may exist among lactobacilli and emphasizes the need for further investigation. In summary, these results suggest that (i) CPO formation by the gut microbiota can have biologically relevant consequences for the host, and (ii) probiotic lactobacilli may be beneficial in reducing
in vivo
CP toxicity.

IMPORTANCE
An understudied area of research is how the microbiota (microorganisms living in/on an animal) affects the metabolism and toxic outcomes of environmental pollutants such as pesticides. This study focused specifically on how the microbial biotransformation of chlorpyrifos (CP; a common organophosphate insecticide) affected host exposure and toxicity parameters in a
Drosophila melanogaster
insect model. Our results demonstrate that the biotransformation of CP by the gut microbiota had biologically relevant and toxic consequences on host health and that certain probiotic lactobacilli may be beneficial in reducing CP toxicity. Since inadvertent pesticide exposure is suspected to negatively impact the health of off-target species, these findings may provide useful information for wildlife conservation and environmental sustainability planning. Furthermore, the results highlight the need to consider microbiota composition differences between beneficial and pest insects in future insecticide designs. More broadly, this study supports the use of beneficial microorganisms to modulate the microbiota-mediated biotransformation of xenobiotics.