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Polycyclic Aromatic Hydrocarbon Degradation in the Sea-Surface Microlayer at Coastal Antarctica

ABSTRACT: As much as 400 Tg of carbon from airborne semivolatile aromatic hydrocarbons is deposited to the oceans every year, the largest identified source of anthropogenic organic carbon to the ocean. Microbial degradation is a key sink of these pollutants in surface waters, but has received little attention in polar environments. We have challenged Antarctic microbial communities from the sea-surface microlayer (SML) and the subsurface layer (SSL) with polycyclic aromatic hydrocarbons (PAHs) at environmentally relevant concentrations. PAH degradation rates and the microbial responses at both taxonomical and functional levels were assessed. Evidence for faster removal rates was observed in the SML, with rates 2.6-fold higher than in the SSL. In the SML, the highest removal rates were observed for the more hydrophobic and particle-bound PAHs. After 24 h of PAHs exposure, particle-associated bacteria in the SML showed the highest number of significant changes in their composition. These included significant enrichments of several hydrocarbonoclastic bacteria, especially the fast-growing genera Pseudoalteromonas, which increased their relative abundances by eightfold. Simultaneous metatranscriptomic analysis showed that the free-living fraction of SML was the most active fraction, especially for members of the order Alteromonadales, which includes Pseudoalteromonas. Their key role in PAHs biodegradation in polar environments should be elucidated in further studies. This study highlights the relevant role of bacterial populations inhabiting the sea-surface microlayer, especially the particle-associated habitat, as relevant bioreactors for the removal of aromatic hydrocarbons in the oceans. Graphical Abstract Particle-associated bacteria inhabiting the sea-surface microlayer showed a faster capacity to degrade PAH than subsurface bacteria.

SUBMITTER: Martinez-Varela A

PROVIDER: S-EPMC9329070 | biostudies-literature |

REPOSITORIES: biostudies-literature

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Project description:The Deepwater Horizon (DWH) blowout resulted in oil transport, including polycyclic aromatic hydrocarbons (PAHs) to the Gulf of Mexico shoreline. The microbial communities of these shorelines are thought to be responsible for the intrinsic degradation of PAHs. To investigate the Gulf Coast beach microbial community response to hydrocarbon exposure, we examined the functional gene diversity, bacterial community composition, and PAH degradation capacity of a heavily oiled and non-oiled beach following the oil exposure. With a non-expression functional gene microarray targeting 539 gene families, we detected 28,748 coding sequences. Of these sequences, 10% were uniquely associated with the severely oil-contaminated beach and 6.0% with the non-oiled beach. There was little variation in the functional genes detected between the two beaches; however the relative abundance of functional genes involved in oil degradation pathways, including polycyclic aromatic hydrocarbons (PAHs), were greater in the oiled beach. The microbial PAH degradation potentials of both beaches, were tested in mesocosms. Mesocosms were constructed in glass columns using sands with native microbial communities, circulated with artificial sea water and challenged with a mixture of PAHs. The low-molecular weight PAHs, fluorene and naphthalene, showed rapid depletion in all mesocosms while the high-molecular weight benzo[α]pyrene was not degraded by either microbial community. Both the heavily oiled and the non-impacted coastal communities showed little variation in their biodegradation ability for low molecular weight PAHs. Massively-parallel sequencing of 16S rRNA genes from mesocosm DNA showed that known PAH degraders and genera frequently associated with oil hydrocarbon degradation represented a major portion of the bacterial community. The observed similar response by microbial communities from beaches with a different recent history of oil exposure suggests that Gulf Coast beach communities are primed for PAH degradation.

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Polycyclic Aromatic Hydrocarbon Degradation in the Sea-Surface Microlayer at Coastal Antarctica

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