Diverse, rare microbial taxa responded to the Deepwater Horizon deep-sea hydrocarbon plume

Abstract

The Deepwater Horizon (DWH) oil well blowout generated an enormous plume of dispersed hydrocarbons that substantially altered the Gulf of Mexico's deep-sea microbial community. A significant enrichment of distinct microbial populations was observed, yet, little is known about the abundance and richness of specific microbial ecotypes involved in gas, oil and dispersant biodegradation in the wake of oil spills. Here, we document a previously unrecognized diversity of closely related taxa affiliating with Cycloclasticus, Colwellia and Oceanospirillaceae and describe their spatio-temporal distribution in the Gulf's deepwater, in close proximity to the discharge site and at increasing distance from it, before, during and after the discharge. A highly sensitive, computational method (oligotyping) applied to a data set generated from 454-tag pyrosequencing of bacterial 16S ribosomal RNA gene V4-V6 regions, enabled the detection of population dynamics at the sub-operational taxonomic unit level (0.2% sequence similarity). The biogeochemical signature of the deep-sea samples was assessed via total cell counts, concentrations of short-chain alkanes (C 1 -C 5 ), nutrients, (colored) dissolved organic and inorganic carbon, as well as methane oxidation rates. Statistical analysis elucidated environmental factors that shaped ecologically relevant dynamics of oligotypes, which likely represent distinct ecotypes. Major hydrocarbon degraders, adapted to the slow-diffusive natural hydrocarbon seepage in the Gulf of Mexico, appeared unable to cope with the conditions encountered during the DWH spill or were outcompeted. In contrast, diverse, rare taxa increased rapidly in abundance, underscoring the importance of specialized subpopulations and potential ecotypes during massive deep-sea oil discharges and perhaps other large-scale perturbations.

Chemical dispersants can suppress the activity of natural oil-degrading microorganisms

“…S5), whereas oligotypes 03 and 10 increased in treatments receiving oil only, underscoring the role of dispersants in driving variation in Colwellia taxa. Phylogenetic analysis of the 16S rRNA gene amplicons confirmed that these oligotypes were closely related to species detected in DWH plume samples in situ (9,16,18) (SI Appendix, Fig. S9), verifying the environmental relevance of these organisms during the DWH discharge.…”

“…However, it seems unlikely that dispersants would stimulate hydrocarbon degradation in a system that lacks a substantial population of hydrocarbon degraders when they had no stimulatory effect in samples from a system that was primed for oil degradation (e.g., oil degraders account for 7-10% of the natural microbial population at site GC600) (18). In fact, the presence of dispersant selected against the most effective hydrocarbon degrading microorganisms (i.e., Marinobacter).…”

“…S1 and S2). Experimental conditions (SI Appendix, Table S1) mimicked those prevailing in the DWH deep-water hydrocarbon plume (6)(7)(8)(9)(10)(11)(12)(13)18), the chemistry of which varied substantially over space and time (18). Amending samples with WAFs and CEWAFs assured that observed differences in microbial community composition and activity would be driven by compositional differences (e.g., the presence or absence of dispersants) in the dissolved organic carbon (DOC) pool rather than by differences in the bulk DOC concentration (26,27).…”

“…A deep-water (1,000-1,300 m) plume, enriched in hydrocarbons (6)(7)(8)(9)(10)(11) and dioctyl sodium sulfosuccinate (DOSS) (12,13), a major component of chemical dispersants (14), formed early in the discharge (7). The chemistry of the hydrocarbon plume significantly altered the microbial community (11,(15)(16)(17), driving rapid enrichment of lowabundance bacterial taxa such as Oceanospirillum, Cycloclasticus, and Colwellia (18). The natural hydrocarbon degraders in Gulf waters were either in low abundance or absent in DWH deepwater plume samples (18).…”

“…The chemistry of the hydrocarbon plume significantly altered the microbial community (11,(15)(16)(17), driving rapid enrichment of lowabundance bacterial taxa such as Oceanospirillum, Cycloclasticus, and Colwellia (18). The natural hydrocarbon degraders in Gulf waters were either in low abundance or absent in DWH deepwater plume samples (18).…”