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Published on: March 17, 2019
Polycyclic aromatic hydrocarbons, gut microbiome composition, impulsivity, and attention covary in a human cohort
Austin J Hammer1, Kristin D Kasschau1, Edward W Davis Ii2
1Department of Microbiology, Oregon State University, Corvallis, Oregon, USA.
Abstract:
Polycyclic aromatic hydrocarbons (PAHs) are pervasive environmental pollutants linked to adverse neurobehavioral outcomes, yet the biological pathways coupling exposure to behavior are poorly defined. The gut microbiome is both sensitive to PAH exposure and a modulator of central nervous system function, suggesting it may mediate how PAH exposure influences neurobehavior. We tested whether PAH exposure, gut microbiome composition, and neurobehavioral function covary in a statewide sample of 34 adults stratified into high-impulsivity/poor-attention (HH) and low-impulsivity/fast-attention (LL) groups. Participants wore silicone wristbands for 30 days to passively sample PAH exposure and provided a single fecal sample for 16S rRNA profiling at the end of the wear period. Higher PAH exposure was associated with HH group membership in a sex-dependent manner, with the largest elevations among HH males. At the community level, PAH exposure profiles correlated with microbiome dissimilarity, and HH membership was associated with increased alpha-diversity and altered community composition relative to LL members. At the taxon level, 22 genera were significantly associated with 14 PAH compounds (FDR < 0.1). No individual genera were significantly associated with neurobehavioral group after multiple testing correction. Nevertheless, cross-referencing PAH-responsive genera (FDR < 0.1) against those with nominal neurobehavioral associations (P < 0.05) identified two candidate genera-Hydrogenoanaerobacterium and Methanobrevibacter-whose abundance covaries with both PAH exposure and neurobehavioral phenotype. Both have been independently linked to cognitive or neurological outcomes in prior work. These findings support a three-way relationship among environmental chemical exposure, gut microbiome composition, and neurobehavioral function, establishing an empirical foundation for testing microbiome-mediated links between PAH exposure and neurobehavioral outcomes.IMPORTANCEPolycyclic aromatic hydrocarbon (PAH) exposure is widespread and is associated with impulsivity and attention problems, but how exposure translates into neurobehavioral risk is unclear. The gut microbiome is a plausible intermediary: gut microbes biotransform environmental chemicals and produce metabolites that influence brain function. In a statewide adult cohort, higher PAH exposure associated with with greater impulsivity and poorer attention in a sex-dependent manner, and both PAH exposure and neurobehavioral phenotype were associated with distinct gut microbiome features at the community and taxon levels. We identify candidate genera at the intersection of PAH exposure and neurobehavioral group whose biology independently implicates them in cognitive and neurological function. Because their associations with neurobehavioral phenotype are nominal, we present these genera as hypothesis-generating candidates for future study. By showing that all three domains covary within a single cohort, this work moves beyond pairwise associations toward testable microbiome-targeted and exposure-reduction strategies for PAH-related neurobehavioral risk.
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