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

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.     

Natural-born eaters

With information on the Deepwater Horizon oil spill in the Gulf of Mexico still coming in, more is being learned about the role of indigenous bacteria in cleaning the spill. Meanwhile, efforts are under way to enlist new genomic technologies to improve outcomes. Jeffrey L. Fox reports.     

Slick science: will new BP funds keep Gulf genomics afloat?

Funding injections by British Petroleum this summer are fueling studies in the Gulf Coast, raising hopes that the Deepwater Horizon oil spill might provide answers to long-standing questions on the nature of cellular toxicity. Rebecca Alvania investigates.     

Demographic trends of Brown Pelicans in Louisiana before and after the Deepwater Horizon oil spill

Marine oil spills may have extensive and deleterious effects on coastal waterbirds, but pre‐spill data sets are often not available for making comparisons of demographics to the period following a spill. The 2010 Deepwater Horizon oil spill allowed us to compare Brown Pelican (Pelecanus occidentalis) demographics during pre‐ and post‐spill years. We banded 1114 pelicans on Louisiana barrier islands from 2007 to 2009, tracked their distribution via band re‐sighting surveys from 2008 to 2011, and conducted age‐structure surveys. Across Louisiana coastal islands in 2011, we detected 7% of pelicans that had been oiled during the 2010 spill and released following rehabilitation. Similarly, 6% of pelicans (not oiled) banded at the same release site in 2007 were observed across coastal islands 1 yr after banding. We observed variation in proportions of pelicans that were 1, 2, and 3 or more years old among years (2008–2011) and across islands, but little variation could readily be assigned to spill‐related mortality. These Brown Pelican demographic trends one year following the Deepwater Horizon oil spill are contrary to other assessments of the impacts of oil contamination on marine birds. However, additional research is required to evaluate potential long‐term population trends.     

Decline in condition of gorgonian octocorals on mesophotic reefs in the northern Gulf of Mexico: before and after the Deepwater Horizon oil spill

Hard-bottom ‘mesophotic’ reefs along the ‘40-fathom’ (73 m) shelf edge in the northern Gulf of Mexico were investigated for potential effects of the Deepwater Horizon (DWH) oil spill from the Macondo well in April 2010. Alabama Alps Reef, Roughtongue Reef, and Yellowtail Reef were near the well, situated 60–88 m below floating oil discharged during the DWH spill for several weeks and subject to dispersant applications. In contrast, Coral Trees Reef and Madison Swanson South Reef were far from the DWH spill site and below the slick for less than a week or not at all, respectively. The reefs were surveyed by ROV in 2010, 2011, and 2014 and compared to similar surveys conducted one and two decades earlier. Large gorgonian octocorals were present at all sites in moderate abundance including Swiftia exserta, Hypnogorgia pendula, Thesea spp., and Placogorgia spp. The gorgonians were assessed for health and condition in a before-after-control-impact (BACI) research design using still images captured from ROV video transects. Injury was modeled as a categorical response to proximity and time using logistic regression. Condition of gorgonians at sites near Macondo well declined significantly post-spill. Before the spill, injury was observed for 4–9 % of large gorgonians. After the spill, injury was observed in 38–50 % of large gorgonians. Odds of injury for sites near Macondo were 10.8 times higher post-spill, but unchanged at far sites. The majority of marked injured colonies in 2011 declined further in condition by 2014. Marked healthy colonies generally remained healthy. Background stresses to corals, including fishing activity, fishing debris, and coral predation, were noted during surveys, but do not appear to account for the decline in condition at study sites near Macondo well.     

Oiling rates and condition indices of shorebirds on the northern Gulf of Mexico following the Deepwater Horizon oil spill

The coastline of the Gulf of Mexico in the United States is an important wintering and stopover region for migratory shorebirds. The Deepwater Horizon oil spill (April–August 2010) impacted more than 1700 km of this coastline and could potentially affect shorebirds through long‐term exposure to toxins, degraded habitats, and altered food chains. We investigated the exposure to Deepwater Horizon oil of seven species of shorebirds that winter or stopover along the northern Gulf of Mexico. From October 2010 to May 2012, we captured and banded 691 shorebirds at six sites that experienced varying levels of oil contamination. Of birds sampled, 22 were lightly oiled, with species that forage on the coast having higher rates of oiling than those that forage in more estuarine habitats. Although only 8.6% of birds captured from October 2010 to May 2011 and 0.6% of the birds captured from August 2011 to June 2012 showed signs of oiling, an unknown, but potentially larger, number of shorebirds were likely exposed to indirect effects of the spill, such as decreased foraging time due to oiling of sites or disturbance from cleanup activities. Fuel stores and fattening rates of Dunlins (Calidris alpina) during spring migration, as measured using plasma metabolites, were not influenced by site oiling level. However, the level of disturbance at study sites was a significant predictor of both fuel stores and glycerol levels, suggesting that Dunlins stopping over during spring migration may have had difficulty reaching necessary fuel stores in spring 2011 due to disturbance from cleanup activity on oiled beaches. These effects from disturbance were only observed at sites with high cleanup activity, suggesting that the impact of oil‐spill cleanup on shorebirds may be minimized by limiting cleanup activities to specific areas and times of day.     

Morphological asymmetry of insular freshwater populations of threespine stickleback

Fluctuating asymmetry (FA), random deviations from perfect symmetry in a bilateral organism, has been widely used as a proxy for developmental instability in stressed populations. In order to test the utility of FA of resident freshwater threespine stickleback (Gasterosteus aculeatus) as a biomonitoring tool for contaminated sites, we compared levels of asymmetry of seven morphological traits of threespine stickleback collected from lakes at three islands with a history of military contamination and three islands with no military history, in the Aleutian Archipelago, Alaska. Traits examined include eye diameter, operculum width, pectoral fin ray number, pectoral fin width, lateral plate number, lateral plate length, and pelvic spine length. All morphometric traits demonstrated some degree of FA or directional asymmetry (DA), but the military history of a lake was not a predictor of the degree or type of asymmetry. Overall, the patterns of asymmetry were similar for all traits, irrespective of military contamination at a lake. Our results demonstrate that the suite of threespine stickleback traits measured are not suitable for examination of FA as a proxy for aquatic pollution in this region. DA also does not appear to be suitable as an indicator of aquatic pollution, but may instead be driven by local ecological factors such as predation.     

A Scientific Look at Spaghetti

The United States is currently experiencing its worst man-made environmental disaster, the BP Deepwater Horizon oil leak. The Gulf of Mexico oil spill is severe in its impact, but it is only one of several global oil spill disasters in history. Students can utilize the technology of Google Earth to explore the spatial and temporal distribution of oil spills. In addition to increasing content knowledge of oil spills, Google Earth assists in developing student geographic and technologic literacy. Designed for a middle school science class, this activity may also be used in English, history, math, art, and poster-making.     

Three-year longitudinal study of perceptions of competence and well-being among youth exposed to disasters

This article examines perceptions of competence/well-being over time and linkages to exposure to natural disaster experiences and stress associated with the Deepwater Horizon Oil Spill in youth. A multi-wave naturalistic design was used to follow N?=?3,399 students, ages 8–18 years who were evaluated for perceptions of competence/well-being, posttraumatic stress disorder (PTSD) symptoms, hurricane exposure experiences, and stress related to the oil spill at three time points across three years. Examination of longitudinal trajectories of competence/well-being revealed growth within youth over time. Age predicted trajectories of competence/well-being, such that older youth had higher ratings of competence/well-being; however, with higher oil spill stress, older youth experienced declines in competence/well-being post-oil spill. There was a negative association between PTSD symptoms and competence/well-being. Findings suggest that perceptions of competence/well-being may be compromised by exposure to disasters, but if maintained may serve as a protective factor.     

Benthic taxa as potential indicators of a deep-sea oil spill

The effect of the Deepwater Horizon oil spill on benthic macrofauna in the deep-sea Gulf of Mexico was measured in September–October 2010. Macrofauna community diversity and abundance were lowest closest to the wellhead and increased with distance from the wellhead up to 10 km. The macrofauna loss was primarily in surface sediments, which could be due to the deposition of oil and other toxic chemicals. Crustacean taxa appeared to be sensitive to the deep-sea blowout. Polychaete taxa varied in their sensitivity, but Dorvilleidae which is often associated with organic enrichment, was responsible for the largest amount of dissimilarity between stations close and far from the wellhead. Several other taxa were classified as sensitive or tolerant to the deep-sea blowout by comparing their distributions among impacted and non-impacted zones. The macrobenthic communities in the deep Gulf of Mexico exhibit a toxic response to the blowout on the Deepwater Horizon well, and this is correlated with barium and petroleum hydrocarbons.     

Shifts in Symbiotic Endophyte Communities of a Foundational Salt Marsh Grass following Oil Exposure from the Deepwater Horizon Oil Spill

Symbiotic associations can be disrupted by disturbance or by changing environmental conditions. Endophytes are fungal and bacterial symbionts of plants that can affect performance. As in more widely known symbioses, acute or chronic stressor exposure might trigger disassociation of endophytes from host plants. We tested this hypothesis by examining the effects of oil exposure following the Deepwater Horizon (DWH) oil spill on endophyte diversity and abundance in Spartina alterniflora – the foundational plant in northern Gulf coast salt marshes affected by the spill. We compared bacterial and fungal endophytes isolated from plants in reference areas to isolates from plants collected in areas with residual oil that has persisted for more than three years after the DWH spill. DNA sequence-based estimates showed that oil exposure shifted endophyte diversity and community structure. Plants from oiled areas exhibited near total loss of leaf fungal endophytes. Root fungal endophytes exhibited a more modest decline and little change was observed in endophytic bacterial diversity or abundance, though a shift towards hydrocarbon metabolizers was found in plants from oiled sites. These results show that plant-endophyte symbioses can be disrupted by stressor exposure, and indicate that symbiont community disassembly in marsh plants is an enduring outcome of the DWH spill.     

Role of Bacterial Exopolysaccharides (EPS) in the Fate of the Oil Released during the Deepwater Horizon Oil Spill

Halomonas species are recognized for producing exopolysaccharides (EPS) exhibiting amphiphilic properties that allow these macromolecules to interface with hydrophobic substrates, such as hydrocarbons. There remains a paucity of knowledge, however, on the potential of Halomonas EPS to influence the biodegradation of hydrocarbons. In this study, the well-characterized amphiphilic EPS produced by Halomonas species strain TG39 was shown to effectively increase the solubilization of aromatic hydrocarbons and enhance their biodegradation by an indigenous microbial community from oil-contaminated surface waters collected during the active phase of the Deepwater Horizon oil spill. Three Halomonas strains were isolated from the Deepwater Horizon site, all of which produced EPS with excellent emulsifying qualities and shared high (97-100%) 16S rRNA sequence identity with strain TG39 and other EPS-producing Halomonas strains. Analysis of pyrosequence data from surface water samples collected during the spill revealed several distinct Halomonas phylotypes, of which some shared a high sequence identity (≥97%) to strain TG39 and the Gulf spill isolates. Other bacterial groups comprising members with well-characterized EPS-producing qualities, such as Alteromonas , Colwellia and Pseudoalteromonas , were also found enriched in surface waters, suggesting that the total pool of EPS in the Gulf during the spill may have been supplemented by these organisms. Roller bottle incubations with one of the Halomonas isolates from the Deepwater Horizon spill site demonstrated its ability to effectively produce oil aggregates and emulsify the oil. The enrichment of EPS-producing bacteria during the spill coupled with their capacity to produce amphiphilic EPS is likely to have contributed to the ultimate removal of the oil and to the formation of oil aggregates, which were a dominant feature observed in contaminated surface waters.     

Role of methylotrophs in the degradation of hydrocarbons during the Deepwater Horizon oil spill

The role of methylotrophic bacteria in the fate of the oil and gas released into the Gulf of Mexico during the Deepwater Horizon oil spill has been controversial, particularly in relation to whether organisms such as Methylophaga had contributed to the consumption of methane. Whereas methanotrophy remains unqualified in these organisms, recent work by our group using DNA-based stable-isotope probing coupled with cultivation-based methods has uncovered hydrocarbon-degrading Methylophaga. Recent findings have also shown that methylotrophs, including Methylophaga, were in a heightened state of metabolic activity within oil plume waters during the active phase of the spill. Taken collectively, these findings suggest that members of this group may have participated in the degradation of high-molecular-weight hydrocarbons in plume waters. The discovery of hydrocarbon-degrading Methylophaga also highlights the importance of considering these organisms in playing a role to the fate of oil hydrocarbons at oil-impacted sites.     

Microbial gene functions enriched in the Deepwater Horizon deep-sea oil plume

The Deepwater Horizon oil spill in the Gulf of Mexico is the deepest and largest offshore spill in the United State history and its impacts on marine ecosystems are largely unknown. Here, we showed that the microbial community functional composition and structure were dramatically altered in a deep-sea oil plume resulting from the spill. A variety of metabolic genes involved in both aerobic and anaerobic hydrocarbon degradation were highly enriched in the plume compared with outside the plume, indicating a great potential for intrinsic bioremediation or natural attenuation in the deep sea. Various other microbial functional genes that are relevant to carbon, nitrogen, phosphorus, sulfur and iron cycling, metal resistance and bacteriophage replication were also enriched in the plume. Together, these results suggest that the indigenous marine microbial communities could have a significant role in biodegradation of oil spills in deep-sea environments.     

High Numbers of Vibrio vulnificus in Tar Balls Collected from Oiled Areas of the North-Central Gulf of Mexico Following the 2010 BP Deepwater Horizon Oil Spill

The Deepwater Horizon Oil Spill was the largest oil spill in USA history releasing approximately 4.9 million barrels of crude oil into the Gulf of Mexico. Soon after the spill started, tar balls and other forms of weathered oil appeared in large numbers on beaches in Mississippi and Alabama. In this study, we analyzed tar balls for total aerobic bacterial (TAB) counts and also for the presence of Vibrio vulnificus, a human pathogen known to be abundant in the Gulf Coast environment and capable of causing severe wound infections by contact with contaminated surfaces. Our results showed that TAB counts were significantly higher in tar balls than in sand and seawater collected at the same location. In addition, V. vulnificus numbers were 10× higher in tar balls than in sand and up to 100× higher than in seawater. Densities of V. vulnificus were higher than 10(5) colony forming units/g of tar ball in all samples analyzed. Our data suggest that tar balls can act as reservoirs for bacteria including human pathogens.     

Deep-Sea Benthic Footprint of the Deepwater Horizon Blowout

The Deepwater Horizon (DWH) accident in the northern Gulf of Mexico occurred on April 20, 2010 at a water depth of 1525 meters, and a deep-sea plume was detected within one month. Oil contacted and persisted in parts of the bottom of the deep-sea in the Gulf of Mexico. As part of the response to the accident, monitoring cruises were deployed in fall 2010 to measure potential impacts on the two main soft-bottom benthic invertebrate groups: macrofauna and meiofauna. Sediment was collected using a multicorer so that samples for chemical, physical and biological analyses could be taken simultaneously and analyzed using multivariate methods. The footprint of the oil spill was identified by creating a new variable with principal components analysis where the first factor was indicative of the oil spill impacts and this new variable mapped in a geographic information system to identify the area of the oil spill footprint. The most severe relative reduction of faunal abundance and diversity extended to 3 km from the wellhead in all directions covering an area about 24 km². Moderate impacts were observed up to 17 km towards the southwest and 8.5 km towards the northeast of the wellhead, covering an area 148 km². Benthic effects were correlated to total petroleum hydrocarbon, polycyclic aromatic hydrocarbons and barium concentrations, and distance to the wellhead; but not distance to hydrocarbon seeps. Thus, benthic effects are more likely due to the oil spill, and not natural hydrocarbon seepage. Recovery rates in the deep sea are likely to be slow, on the order of decades or longer.     

The core seafloor microbiome in the Gulf of Mexico is remarkably consistent and shows evidence of recovery from disturbance caused by major oil spills

The microbial ecology of oligotrophic deep ocean sediments is understudied relative to their shallow counterparts, and this lack of understanding hampers our ability to predict responses to current and future perturbations. The Gulf of Mexico has experienced two of the largest accidental marine oil spills, the 1979 Ixtoc-1 blowout and the 2010 Deepwater Horizon (DWH) discharge. Here, microbial communities were characterized for 29 sites across multiple years in > 700 samples. The composition of the seafloor microbiome was broadly consistent across the region and was well approximated by the overlying water depth and depth within the sediment column, while geographic distance played a limited role. Biogeographical distributions were employed to generate predictive models for over 4000 OTU that leverage easy-to-obtain geospatial variables which are linked to measured sedimentary oxygen profiles. Depth stratification and putative niche diversification are evidenced by the distribution of taxa that mediate the microbial nitrogen cycle. Furthermore, these results demonstrate that sediments impacted by the DWH spill had returned to near baseline conditions after 2 years. The distributions of benthic microorganisms in the Gulf can be constrained, and moreover, deviations from these predictions may pinpoint impacted sites and aid in future response efforts or long-term stability studies.     

Sexual selection, stabilizing selection and fluctuating asymmetry in two populations of pupfish (Cyprinodon pecosensis)

Fluctuating asymmetry of morphological traits is thought to reflect the capacity of a genotype to produce an integrated, functional phenotype. I tested three predictions. (1) In a polygynous breeding system, under intense sexual selection on males, breeding males should show greater symmetry in bilaterally symmetrical traits than non-breeding males or females. (2) If these traits are under stabilizing selection, highly symmetrical individuals also should be modal phenotypes, thus near the mean value for that trait, whereas individuals with increased asymmetry should represent marginal phenotypes, near the extremes of the distribution for that trait. (3) Differences in the intensity of sexual selection should be reflected in differences in the degree of fluctuating asymmetry between sexes among populations. I examined the relationship between male breeding status and the degree of fluctuating asymmetry of four bilaterally symmetrical- traits, preorbital and preopercular pores and pectoral and pelvic fin rays, in two populations of Pecos pupfish which differed in the intensity of sexual selection. These traits do not function in male-male competition or female choice, thus are not directly affected by sexual selection. In Mirror Lake breeding males, as a group, were most symmetrical for all four traits, while non-breeding males and females showed higher levels of fluctuating asymmetry. Similarly, symmetrical individuals also represented modal phenotypes for four traits (breeding males), and for three traits (non-breeding males and females). These patterns were not seen in the Lake Francis population, where breeding males were as asymmetrical as non-breeding males and females, and the degree of fluctuating symmetry did not differ between modal and marginal phenotypes for any of the four traits. When ecological conditions favour intense sexual selection, either through female choice, male-male competition, or both, breeding males represent the most fit phenotypes. Thus sexual selection reinforces the effects of stabilizing selection on characters that do not function as secondary sexual traits. However, when sexual selection is relaxed, differences between sexes disappear.     

Deep-sea bacteria enriched by oil and dispersant from the Deepwater Horizon spill

The Deepwater Horizon oil spill resulted in a massive influx of hydrocarbons into the Gulf of Mexico (the Gulf). To better understand the fate of the oil, we enriched and isolated indigenous hydrocarbon-degrading bacteria from deep, uncontaminated waters from the Gulf with oil (Macondo MC252) and dispersant used during the spill (COREXIT 9500). During 20 days of incubation at 5°C, CO(2) evolution, hydrocarbon concentrations and the microbial community composition were determined. Approximately 60% to 25% of the dissolved oil with or without COREXIT, respectively, was degraded, in addition to some hydrocarbons in the COREXIT. FeCl(2) addition initially increased respiration rates, but not the total amount of hydrocarbons degraded. 16S rRNA gene sequencing revealed a succession in the microbial community over time, with an increase in abundance of Colwellia and Oceanospirillales during the incubations. Flocs formed during incubations with oil and/or COREXIT in the absence of FeCl(2) . Synchrotron radiation-based Fourier transform infrared (SR-FTIR) spectromicroscopy revealed that the flocs were comprised of oil, carbohydrates and biomass. Colwellia were the dominant bacteria in the flocs. Colwellia sp. strain RC25 was isolated from one of the enrichments and confirmed to rapidly degrade high amounts (approximately 75%) of the MC252 oil at 5°C. Together these data highlight several features that provide Colwellia with the capacity to degrade oil in cold, deep marine habitats, including aggregation together with oil droplets into flocs and hydrocarbon degradation ability.     

Detection of Salt Marsh Vegetation Stress and Recovery after the Deepwater Horizon Oil Spill in Barataria Bay,Gulf of Mexico Using AVIRIS Data

The British Petroleum Deepwater Horizon Oil Spill in the Gulf of Mexico was the biggest oil spill in US history. To assess the impact of the oil spill on the saltmarsh plant community, we examined Advanced Visible Infrared Imaging Spectrometer (AVIRIS) data flown over Barataria Bay, Louisiana in September 2010 and August 2011. Oil contamination was mapped using oil absorption features in pixel spectra and used to examine impact of oil along the oiled shorelines. Results showed that vegetation stress was restricted to the tidal zone extending 14 m inland from the shoreline in September 2010. Four indexes of plant stress and three indexes of canopy water content all consistently showed that stress was highest in pixels next to the shoreline and decreased with increasing distance from the shoreline. Index values along the oiled shoreline were significantly lower than those along the oil-free shoreline. Regression of index values with respect to distance from oil showed that in 2011, index values were no longer correlated with proximity to oil suggesting that the marsh was on its way to recovery. Change detection between the two dates showed that areas denuded of vegetation after the oil impact experienced varying degrees of re-vegetation in the following year. This recovery was poorest in the first three pixels adjacent to the shoreline. This study illustrates the usefulness of high spatial resolution airborne imaging spectroscopy to map actual locations where oil from the spill reached the shore and then to assess its impacts on the plant community. We demonstrate that post-oiling trends in terms of plant health and mortality could be detected and monitored, including recovery of these saltmarsh meadows one year after the oil spill.