Large Enrichment of Anthropogenic Organic Matter Degrading Bacteria in the Sea-Surface Microlayer at Coastal Livingston Island (Antarctica)

Abstract

The composition of bacteria inhabiting the sea-surface microlayer (SML) is poorly characterized globally and yet undescribed for the Southern Ocean, despite their relevance for the biogeochemistry of the surface ocean. We report the abundances and diversity of bacteria inhabiting the SML and the subsurface waters (SSL) determined from a unique sample set from a polar coastal ecosystem (Livingston Island, Antarctica). From early to late austral summer (January-March 2018), we consistently found a higher abundance of bacteria in the SML than in the SSL. The SML was enriched in some Gammaproteobacteria genus such as Pseudoalteromonas, Pseudomonas, and Colwellia, known to degrade a wide range of semivolatile, hydrophobic, and surfactant-like organic pollutants. Hydrocarbons and other synthetic chemicals including surfactants, such as perfluoroalkyl substances (PFAS), reach remote marine environments by atmospheric transport and deposition and by oceanic currents, and are known to accumulate in the SML. Relative abundances of specific SML-enriched bacterial groups were significantly correlated to concentrations of PFASs, taken as a proxy of hydrophobic anthropogenic pollutants present in the SML and its stability. Our observations provide evidence for an important pollutant-bacteria interaction in the marine SML. Given that pollutant emissions have increased during the Anthropocene, our results point to the need to assess chemical pollution as a factor modulating marine microbiomes in the contemporaneous and future oceans.

Keywords: ADOC; amplicon sequencing; bacterioneuston; microbial communities; organic pollutants; sea-surface microlayer; surfactants.

FIGURE 1

Location of the sampling stations for the SML and SSL at South Bay of Livingston Island (South Shetlands, Antarctica).

FIGURE 2

Bacterial abundance of LNA, HNA, and total heterotrophic bacteria for SML and SSL during the austral summer. Values are means of duplicates. Error bars show standard deviations.

FIGURE 3

Relative abundances in the SML vs. SSL for selected taxa. Flavobactereiia AD and Gammaproteobacteria AD were significantly enriched in the SML, while Alteromonadales, Sphingomonadales and Caulobacterales presented high positive fold changes in the SML (FC > 2). Notice the logarithmic scale of the axes. Data points on the 1:1 dashed line indicate equal contribution to the 16S ASV pool.

FIGURE 4

Fold change values in relative abundances of specific taxa in the SML vs. SSL during the austral summer.

FIGURE 5

Correlation map between nutrients, PFAS and bacterial abundances and prevalence of bacterial groups. Red and blue sectors represent positive and negative correlations, asterisks indicate significant correlations (Spearman correlation, p ≤ 0.05). In the x axis: PFUDA, Perfluoroundecanoic acid; PFHXA, Perfluorohexanoic acid; PFDA, Perfluorodecanoic acid; PFNA, Perfluorononanoic acid; PFOS, Perfluorooctane sulfonate; PFOA, Perfluorooctanoic Acid; PFBS, Perfluorobutane sulfonate; LNA, Low Nucleic Acid; HNA, High Nucleic Acid.

FIGURE 6

Low abundance and abundant taxa analysis based on 16S rDNA ASV counts. Taxonomical distribution of main taxonomical groups assigned to ASVs with high abundances (>3%) and low abundances (<3%). Overlapping circles indicate the number of unique ASVs shared in the different abundance pools.