Phytoplankton have been shown to harbour a diversity of hydrocarbonoclastic bacteria (HCB), yet it is not understood how these phytoplankton-associated HCB would respond in the event of an oil spill at sea. Here, we assess the diversity and dynamics of the bacterial community associated with a natural population of marine phytoplankton under oil spill-simulated conditions, and compare it to that of the free-living (non phytoplankton-associated) bacterial community. While the crude oil severely impacted the phytoplankton population and was likely conducive to marine oil snow formation, analysis of the MiSeq-derived 16S rRNA data revealed dramatic and differential shifts in the oil-amended communities that included blooms of recognized HCB (e.g., Thalassospira, Cycloclasticus), including putative novel phyla, as well as other groups with previously unqualified oil-degrading potential (Olleya, Winogradskyella, and members of the inconspicuous BD7-3 phylum). Notably, the oil biodegradation potential of the phytoplankton-associated community exceeded that of the free-living community, and it showed a preference to degrade substituted and non-substituted polycyclic aromatic hydrocarbons. Our study provides evidence of compartmentalization of hydrocarbon-degrading capacity in the marine water column, wherein HCB associated with phytoplankton are better tuned to degrading crude oil hydrocarbons than that by the community of planktonic free-living bacteria.

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The surface of marine eukaryotic phytoplankton can harbour communities of hydrocarbon-degrading bacteria; however, this algal–bacterial association has, hitherto, been only examined with non-axenic laboratory cultures of micro-algae. In this study, we isolated an operationally-defined community of phytoplankton, of cell size 50–70 μm, from a natural community in sea surface waters of a subarctic region in the northeast Atlantic. Using MiSeq 16S rRNA sequencing, we identified several recognized (Alcanivorax, Marinobacter, Oleispira, Porticoccus, Thalassospira) and putative hydrocarbon degraders (Colwelliaceae, Vibrionaceae) tightly associated with the phytoplankton population. We combined fluorescence in situ hybridisation with flow-cytometry (FISH-Flow) to examine the association of Marinobacter with this natural eukaryotic phytoplankton population. About 1.5% of the phytoplankton population contained tightly associated Marinobacter. The remaining Marinobacter population were loosely associated with either eukaryotic phytoplankton cells or non-chlorophyll particulate material. This work is the first to show the presence of obligate, generalist and putative hydrocarbonoclastic bacteria associated with natural populations of eukaryotic phytoplankton directly from sea surface water samples. It also highlights the suitability of FISH-Flow for future studies to examine the spatial and temporal structure and dynamics of these and other algal–bacterial associations in natural seawater samples.

Polycyclovorans algicola strain TG408 is a recently discovered bacterium associated with marine eukaryotic phytoplankton and exhibits the ability to utilize polycyclic aromatic hydrocarbons (PAHs) almost exclusively as sole sources of carbon and energy. Here, we present the genome sequence of this strain, which is 3,653,213 bp, with 3,477 genes and an average G+C content of 63.8%.

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