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.

Keywords: Alteromonadales; PAH; PAH biodegradation; coastal Antarctica; hydrocarbonoclastic bacteria; sea-surface microlayer.

FIGURE 1

PAH removal rates in the sea-surface microlayer (SML) and the subsurface layer (SSL) for treatments and controls calculated as the difference of concentrations between time 0 and 24 h (units in ng L^–1 h^–1). Significant differences between layers (Mann–Whitney test, P < 0.05) are labeled with an asterisk.

FIGURE 2

Characterization of community structure after 24 h of PAH exposure in the sea-surface microlayer (SML) and subsurface layer (SSL) for particle-associated (PA) and free-living (FL) bacterial fractions based on 16S rRNA gene amplicon sequencing. Statistical differences between controls and PAH treatments were detected by t-test and labeled with an arrow in the figure. Hydrocarbonoclastic bacteria (HCB) (in orange) as listed in Supplementary Table 7. Notice that general taxonomical groups (in black) include HCB.

FIGURE 3

Total number of significantly enriched (in red) or depleted (in blue) transcripts detected by EdgeR (FDR < 0.05) between PAH treatments and controls metatranscriptomes. Counts are indicated inside each tile. Rows correspond to SEED categories (SML, sea-surface microlayer; SSL, subsurface layer; PA, particle-associated; FL, free-living).

FIGURE 4

Fold change in expression of genes involved in PAH degradation between PAH treatments and controls measured by metatranscriptomics. PAH degradation pathway is represented for the naphthalene (model and simplest PAH compound). The list of the specific Pfam profiles involved in PAH degradation is shown in Supplementary Table 4 (SML, sea-surface microlayer; SSL, subsurface layer; PA, particle-associated; FL, free-living).