Limited impact of weathered residues from the Deepwater Horizon oil spill on the gut-microbiome and foraging behavior of sheepshead minnows (Cyprinodon variegatus)

ABSTRACT

The Deepwater Horizon disaster of April 2010 was the largest oil spill in U.S. history and exerted catastrophic effects on several ecologically important fish species in the Gulf of Mexico (GoM). Within fish, the microbiome plays a key symbiotic role in maintaining host health and aids in acquiring nutrients, supporting immune function, and modulating behavior. The aim of this study was to examine if exposure to weathered oil might produce significant shifts in fish gut-associated microbial communities as determined from taxa and genes known for hydrocarbon degradation, and whether foraging behavior was affected. The gut microbiome (16S rRNA and shotgun metagenomics) of sheepshead minnow (Cyprinodon variegatus) was characterized after fish were exposed to oil in High Energy Water Accommodated Fractions (HEWAF; tPAH = 81.1 ± 12.4 µg/L) for 7 days. A foraging behavioral assay was used to determine feeding efficiency before and after oil exposure. The fish gut microbiome was not significantly altered in alpha or beta diversity. None of the most abundant taxa produced any significant shifts as a result of oil exposure, with only rare taxa showing significant shifts in abundance between treatments. However, several bioindicator taxa known for hydrocarbon degradation were detected in the oil treatment, primarily Sphingomonas and Acinetobacter. Notably, the genus Stenotrophomonas was detected in high abundance in 16S data, which previously was not described as a core member of fish gut microbiomes. Data also demonstrated that behavior was not significantly affected by oil exposure. Potential low bioavailability of the oil may have been a factor in our observation of minor shifts in taxa and no behavioral effects. This study lays a foundation for understanding the microbiome of captive sheepshead minnows and indicates the need for further research to elucidate the responses of the fish gut-microbiome under oil spill conditions.

KEYWORDS:

• Polycyclic aromatic hydrocarbons (PAHs)
• High-energy water accommodated fractions (HEWAF)
• sheepshead minnow (cyprinodon variegatus)
• aquatic toxicology
• microbiome
• foraging behavior

Acknowledgments

We would like to thank C.L. Searle for lending supplies to care for the Daphnia, C. Malinowski, S. Harrison, E. Reverman, and C. Simpson for help with experiments, and E. Allmon for assistance with chemical analyses.

Disclosure statement

No potential conflict of interest was reported by the author(s).

Supplementary material

Supplemental data for this article can be accessed online at https://doi.org/10.1080/15287394.2023.2265413

Declaration of authorship

MAW and MSS designed the experiments; MSS and RJG obtained funding for the work; MAW, TAJ, AGH, and JAK analyzed the data; MAW wrote the manuscript; all authors provided editorial advice.

Additional information

Funding

This work was supported by the Gulf of Mexico Research Initiative [Grant Number GR05916-01 (40002054)].