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.

Snow-Dependent Biogeochemical Cycling of Polycyclic Aromatic Hydrocarbons at Coastal Antarctica

“…Obligate HCB ( Oleispira , Colwellia ) and other facultative HCB such as Marinomonas , Glaciecola , and Pseudomonas were present at lower relative abundances (Table S9). These HCB taxa have been previously found in Antarctic waters and sediments, and in some manipulative experiments at low temperatures, their role in PAH degradation has been reported. ,, …”

“…The vast majority of PAHs entering the ocean are degraded in the photic zone. Even though photodegradation can occur, the overall PAH sink is dominated by microbial degradation. , Despite this relevance, the study of microbial degradation of PAHs under field conditions has been mainly centered under scenarios of high concentrations, such as those found in oil spills, , with few field studies addressing the degradation of PAHs when these occur at their background levels …”

“…HCB are naturally found at low abundances but can become predominant shortly after pulses of hydrocarbons (both aliphatic and aromatic). − HCB are also ubiquitous in remote environments such as polar sea ice, the surface microlayer, or deep marine nonpolluted seawater. − HCB belong to different phylogenetic groups, including members in the most common marine dominant classes, Gammaproteobacteria , Alphaproteobacteria , and Flavobacteria . In polar environments, there is a suite of microbial responses, including biodegradation, due to exposure to mixtures of anthropogenic dissolved organic carbon (ADOC). , Other works assessing the influence of ADOC on polar bacteria at ultratrace concentrations have reported the growth of the rare biosphere, in some cases, HCB. , Nevertheless, studies attempting to compare HCB presence to the occurrence of PAH in seawater and assess their mutual interactions are still scarce at background environmental levels, despite the reported HCB and PAH co-occurrence under scenarios of oil spills. ,, In addition, the interactions of HCB and PAHs have never been reported for time series of measurements. Dynamics of PAHs over the austral summer may depend on the highly variable snow deposition events, glacier melting, and other environmental conditions.…”

Natural and oil surface slicks as microbial habitats in marine systems: A mini review

“…While biosurfactants are essential for the formation of natural slicks, in oil slicks they primarily increase the rate of oil biodegradation. Many Pseudomonadota are known biosurfactant producers and hydrogenoclastic organisms in the sea-surface microlayer of coastal Antarctica (Martinez-Varela et al (2022), Table 1). A study focusing on microorganisms in microlayer associated with an oil slick identified amplicon sequence variants (ASVs) related to oil-degrading and surfactant-producing genera: Alcanivorax, Halomonas, Marinobacter, and Bacillus (Parks et al, 2020).…”

“…AlteromonasAntOS DWH, oil slick exposed to sunlight, heavier oilRedmond and Valentine, 2012;Liu & Liu, 2013;Bacosa et al, 2015b; al., 2016 Colwellia AntOS x DWH, hydrogenoclastic Hazen et al, 2010; Martinez-Varela et al, 2022 Redmond and Valentine, 2012; Kurata et al, 2016; Martinez-Varela et al, 2022 Psychrobacter AntOS x hydrogenoclastic Martinez-Varela et al, 2022 Pseudomonas NatS, AntOS x DWH, heavier oil, oil slick incubated in dark, hydrogenoclasticRedmond and Valentine, 2012;Liu and Liu, 2013;Bacosa et al, 2015b;Kurata et al, 2016;Parks et al, 2020;Martinez-Varela et al, 2022 …”