Dramatic shifts in benthic microbial eukaryote communities following the Deepwater Horizon oil spill

Abstract

Benthic habitats harbour a significant (yet unexplored) diversity of microscopic eukaryote taxa, including metazoan phyla, protists, algae and fungi. These groups are thought to underpin ecosystem functioning across diverse marine environments. Coastal marine habitats in the Gulf of Mexico experienced visible, heavy impacts following the Deepwater Horizon oil spill in 2010, yet our scant knowledge of prior eukaryotic biodiversity has precluded a thorough assessment of this disturbance. Using a marker gene and morphological approach, we present an intensive evaluation of microbial eukaryote communities prior to and following oiling around heavily impacted shorelines. Our results show significant changes in community structure, with pre-spill assemblages of diverse Metazoa giving way to dominant fungal communities in post-spill sediments. Post-spill fungal taxa exhibit low richness and are characterized by an abundance of known hydrocarbon-degrading genera, compared to prior communities that contained smaller and more diverse fungal assemblages. Comparative taxonomic data from nematodes further suggests drastic impacts; while pre-spill samples exhibit high richness and evenness of genera, post-spill communities contain mainly predatory and scavenger taxa alongside an abundance of juveniles. Based on this community analysis, our data suggest considerable (hidden) initial impacts across Gulf beaches may be ongoing, despite the disappearance of visible surface oil in the region.

Figure 1. Pre-spill and Post-spill taxonomic comparisons of microbial eukaryote communities.

Chart illustrating dominant microbial eukaryote taxa observed in pre-spill versus post-spill sample sites, with consistent nematode majority fractions giving way to fungal dominance in oil-impacted sediments. Proportions calculated from non-chimeric OTUs clustered in UCLUST at a 99% pairwise identity cutoff.

Figure 2. Phylogenetic beta diversity analysis of eukaryote communities conducted using the UniFrac distance metric

. (A) Jacknifed Cluster Analysis of non-chimeric OTUs (F04/R22 locus) clustered at 99% in UCLUST; support values >50% are reported. (B) Principal Coordinate analysis of non-chimeric OTUs (NF1/18 Sr2b locus) clustered under a 99% cutoff in UCLUST; 2D representation of a 3D plot (original 3D Kinemage files available in the accompanying Dryad data package) All analyses were conducted using weighted OTU datasets (normalized abundance values) sampled at an even depth across sites.

Figure 3. Bray-curtis similarity of morphologically identified nematode communities.

Group average cluster analysis based on faunal resemblance; Bray-Curtis similarity of nematode genera calculated from pre-spill and post spill samples based on presence/absence of genera.