Contrasting sensitivity among oligotrophic marine microbial communities to priority PAHs

Abstract

Oligotrophic areas represent a large proportion of the oceans, wherein microbial food webs largely determine carbon flux dynamics and biogeochemical cycles. However, little is known regarding the sensitivity of microbial planktonic communities to pollutants in such areas. Organic pollutants such as polycyclic aromatic hydrocarbons (PAH/s) are toxic oil derivatives that occur as complex mixtures and reach marine environments through different sources. Therefore, our study analyzed the PAH tolerance of natural photosynthetic and heterotrophic bacteria and eukaryotes from the oligotrophic Red Sea, which is uniquely susceptible to high oil contamination. Natural communities sampled from the surface layer were exposed to a concentration gradient of a mixture of 16 priority PAHs at in situ conditions for 48 h. The populations of the dominant picocyanobacteria Synechococcus sp., picophytoeukaryotes, and low nucleic acid (LNA) bacteria decreased upon exposure to PAHs in a strong dose-dependent manner. Chlorophyll-a, which was measured as an indicator of the total autotrophic community response, also decreased substantially. High nucleic acid (HNA) bacteria, however, exhibited lower growth inhibition (<50%). The lethal concentration (LC10) thresholds to the 16-PAH mixture demonstrated contrasting sensitivities among the microbial communities studied increasing from picoeukaryotes (5.98 ± 2.08 μg L−1) < chlorophyll-a (19.51 ± 8.11 μg L−1) < LNA bacteria (23.63 ± 10.64 μg L−1) < Synechococcus sp. (26.77 ± 13.34 μg L−1) < HNA bacteria (97.13 ± 17.28 μg L−1). The sensitivity of Red Sea Synechococcus and picophytoeukaryotes to the 16-PAH mixture was between 2 and 6.5 times higher compared to single PAH compounds tested previously. However, some populations of HNA bacteria and Synechococcus sp., were highly tolerant, suggesting an adaptation to chronic pollution. Concerningly, the LC10 toxicity thresholds approached the ambient PAH concentrations in the Red Sea, suggesting that environmental oil pollution actively shapes the microbial community structures in the region.