The Sub-Chronic Effects of Polycyclic Aromatic Hydrocarbons on the sheepshead minnow (Cyrpinodon variegatus) Gut-Microbiome and Foraging Behavior

Abstract

The microbiome plays a key symbiotic role in maintaining host health and aids in acquiring nutrients, supporting development and immune function, and modulating behavior. However, more research is needed to elucidate the potential impact of environmental pollutants on host microbial communities and how microbiomes can modulate the toxicity of contaminants to the host. Through a literature review of 18 studies that assessed the impacts of various anthropogenic chemicals on fish-associated microbiomes, we found that toxicants generally decrease microbial diversity, which could lead to long-term health impacts if chronically stressed, and can increase the host’s susceptibility to disease as well as the chemical resistance of certain microbes. These findings led us to explore the impacts of one of the reviewed contaminants, polycyclic aromatic hydrocarbons (PAHs), typically found in oil. The Deepwater Horizon disaster of April 2010 was the largest oil spill in U.S. history and had catastrophic effects on several ecologically important fish species in the Gulf of Mexico (GoM). This study tested the hypotheses that exposure to weathered oil would cause significant shifts in fish gut-associated microbial communities, with taxa known for hydrocarbon degradation increasing in abundance and that foraging behavior would decrease, potentially due to microbial dysbiosis via the gut-brain axis. We characterized the gut microbiome (with 16S rRNA gene sequencing) of a native GoM estuarine species, the sheepshead minnow (Cyprinodon variegatus). Fish were exposed to High Energy Water Accommodated Fractions (HEWAF; tPAH = 80.99 ± 12.5 μg/L) of oil over a 7-day period and whole gastrointestinal tracts were sampled for microbiome analyses. A foraging behavioral assay was used to determine feeding efficiency before and after oil exposure. The fish gut microbiome did not experience any significant changes in alpha or beta diversity but known hydrocarbon degrading taxa were noticeably present in oil-exposed communities and were absent in controls. We found the order Pseudomonadales, the family Paenibacillaceae, and Pseudomonas pachastrellae to be among these, with Pseudomonadales increasing in abundance. Foraging behavior was not significantly affected by oil exposure. This work highlights the need for further research to elucidate the functional metagenomic responses of the fish gut-microbiome under oil spill conditions.