Salt Marsh Bacterial Communities before and after the Deepwater Horizon Oil Spill

Abstract

Coastal salt marshes along the northern Gulf of Mexico shoreline received varied types and amounts of weathered oil residues after the 2010 Deepwater Horizon oil spill. At the time, predicting how marsh bacterial communities would respond and/or recover to oiling and other environmental stressors was difficult because baseline information on community composition and dynamics was generally unavailable. Here, we evaluated marsh vegetation, physicochemistry, flooding frequency, hydrocarbon chemistry, and subtidal sediment bacterial communities from 16S rRNA gene surveys at 11 sites in southern Louisiana before the oil spill and resampled the same marshes three to four times over 38 months after the spill. Calculated hydrocarbon biomarker indices indicated that oil replaced native natural organic matter (NOM) originating from Spartina alterniflora and marine phytoplankton in the marshes between May 2010 and September 2010. At all the studied marshes, the major class- and order-level shifts among the phyla Proteobacteria, Firmicutes, Bacteroidetes, and Actinobacteria occurred within these first 4 months, but another community shift occurred at the time of peak oiling in 2011. Two years later, hydrocarbon levels decreased and bacterial communities became more diverse, being dominated by Alphaproteobacteria (Rhizobiales), Chloroflexi (Dehalococcoidia), and Planctomycetes Compositional changes through time could be explained by NOM source differences, perhaps due to vegetation changes, as well as marsh flooding and salinity excursions linked to freshwater diversions. These findings indicate that persistent hydrocarbon exposure alone did not explain long-term community shifts.IMPORTANCE Significant deterioration of coastal salt marshes in Louisiana has been linked to natural and anthropogenic stressors that can adversely affect how ecosystems function. Although microorganisms carry out and regulate most biogeochemical reactions, the diversity of bacterial communities in coastal marshes is poorly known, with limited investigation of potential changes in bacterial communities in response to various environmental stressors. The Deepwater Horizon oil spill provided an unprecedented opportunity to study the long-term effects of an oil spill on microbial systems in marshes. Compared to previous studies, the significance of our research stems from (i) a broader geographic range of studied marshes, (ii) an extended time frame of data collection that includes prespill conditions, (iii) a more accurate procedure using biomarker indices to understand oiling, and (iv) an examination of other potential stressors linked to in situ environmental changes, aside from oil exposure.

Keywords: Deepwater Horizon; Gulf of Mexico; PAHs; bacterial diversity; n-alkanes; organic matter; sediment.

FIG 1

Maps from Shoreline Cleanup and Assessment Technique (SCAT) observation data from the Deepwater Horizon Response and the Natural Resource Damage Assessment, available from the Environmental Response Management Application (ERMA) online mapping tool (https://erma.noaa.gov/gulfofmexico/erma.html#) (117), with base maps adapted from OpenStreetMap under a Creative Commons license. (A) Cumulative SCAT oiling shoreline observations from 19 May 2010 through 29 May 2010, which bracketed the first sampling time in this study. (B) Cumulative SCAT oiling shoreline observations from 17 September 2010, after the second sampling time in this study when new sites were added. (C) Cumulative SCAT observations done 30 September 2014 show maximum shoreline oiling (120).

FIG 2

(A) Location map for salt marsh sampling from 2010-2013, with the base map adapted from Open Street Maps and visualized by ArcGIS Online (Esri). Sampled marsh locations correspond to the year and sample number listed on Table 1, without the “ELM” prefix, and are color-coded in panels A, C, D, and E. (B) The percentage of time during a year that the marsh surface is above mean sea level or, conversely, the amount of time a marsh surface is flooded, according to Coastwide Reference Monitoring System (CRMS) station data (http://www.lacoast.gov/crms2/Home.aspx). Stations are color-coded to match the closest sampled marsh. Marshes in American Bay and Terrebonne Bay are flooded more frequently than marshes in Barataria Bay. (C) Canopy height of Spartina alterniflora at 10 m inland for each marsh over time. (D and E) Total n-alkane concentrations (D) and aromatic compound concentrations (E) for each of the marshes over time. The black arrows for panels C to E refer to major meteorological events during the sampling, including Topical Storm Bonnie (25 July 2010), Tropical Storm Lee (4 September 2011), and Hurricane Isaac (29 August 2012).

FIG 3

Shannon diversity index values per sampled marsh through time. Refer to Fig. 2 for sample locations. Plotted data are color-coded for each marsh location on Fig. 2A, with the sample numbers listed for each site from Table 1 without the “ELM” prefix.

FIG 4

Comparisons between concentrations of total n-alkanes and aromatics and Shannon diversity values over time for marsh edge measurements (A and B) and 10-m-inland measurements (C and D), with May 2010 data (inland hydrocarbon only) being solids squares and August 2013 (inland hydrocarbon only) being closed green diamonds.

FIG 5

Average changes in relative abundances (R.A.) for all of the sampled marshes at specific times for the classes within the Proteobacteria phylum (A), orders within the Firmicutes phylum (B), orders within the Gammaproteobacteria class (C), orders within the Alphaproteobacteria class (D), orders within the Deltaproteobacteria class (E), and classes within the Chloroflexi phylum (F). The lines shown on the graphs that connect each of the sampling times are only meant to guide the eye between comparisons and do not imply a continuum of data over the 38 months of study.

FIG 6

(A) NMDS plot of bacterial diversity (color-coded by site number from Fig. 1A) against 10 environmental dimensions (vectors) having statistical significance based on NPMANOVA tests (P < 0.05). Sampling times are plotted with distinct shapes for each of the sampling times. Bar graphs around NMDS plot are for representative communities and are used to show compositional changes for dominant phyla and classes from the sediment samples over time. Changes in diversity according to a Bray-Curtis distance matrix are represented on the two NMDS axes visualized in two dimensions. Differences in sample ordination correspond to the vector of influence for environmental parameters. The stress for the data set is 0.09, suggesting the NMDS adequately represents true distances in multidimensional space. (B to G) Trajectories displaying changes in NMDS ordination of marsh sediment bacterial communities at each marsh, with arrows guiding the eye from sampling event to sampling event. Symbols correspond to sampling time and symbols are color-coded for sampling locations on Fig. 2A. All of the data from plot A are represented on these plots, but only specific changes across NMDS space are noted for marshes from similar geographic areas, such as plots B and C from Terrebonne Bay, plots D, E, and F from northern Barataria Bay, and plot G from American Bay.